(The Natural History of The Crustacea) Les Watling, Martin Thiel (Eds.) - Functional Morphology and Diversity. 1-Oxford University Press (2013)

Functional Morphology
and Diversity
Functional Morphology and Diversity. Les Watling and Martin Thiel.

© Les Watling and Martin Thiel 2013. Published 2013 by Oxford University Press.
The Natural History of the Crustacea Series
SERIES EDITOR:
Martin Thiel
Editor ia l A dvisory Boar d:

Geoff Boxshall, Natural History Museum, London, UK
Emmett Duffy, Virginia Institute of Marine Sciences, Gloucester, USA
Darryl Felder, University of Louisiana, Lafayette, USA
Gary Poore, Victoria Museum, Melbourne, Australia
Bernard Sainte-Marie, Fisheries and Oceans Canada, Mont-Joli, Canada
Gerhard Scholtz, Humboldt University Berlin, Berlin, Germany
Fred Schram, Friday Harbor Marine Laboratory, Seattle, USA
Les Watling, University of Hawaii, Hawaii, USA
Functional Morphology and Diversity (Volume 1)

Edited by Les Watling and Martin Thiel
and Diversity
The Natural History of the Crustacea,
Volume 1
EDITED BY LES WATLING AND MARTIN THIEL
1
3
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Library of Congress Cataloging-in-Publication Data
Functional Morphology and Diversity

p. cm—(The Natural History of the Crustacea series).
Includes bibliographical references and index.
ISBN 978-0-19-539803-8 (hardcover: alk. paper) 1. Crustacea. I. Watling, Les. II. Thiel,
Martin, 1962–
QL435.N38 2013
595.3—dc23 2012012251
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Printed in the United States of America
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PREFACE
Many years ago, when M.T. came to Maine to work with L.W. on shallow subtidal crustaceans,
we established some amphipod populations in aquaria at the University of Maine’s Darling
Marine Center flowing seawater facility. What ensued was not just a series of remarkable behav-
ioral observations but also a series of long discussions of “how do they do that?” in response to
the burrowing and whip making that we observed. The two of us have maintained a lifelong
interest in understanding how crustacean morphology “determines” what the animals can do
and where they can live.
Crustaceans encompass a bewildering array of body forms that they use to occupy almost
every habitat type on Earth. In fact, the only habitat not occupied by crustaceans is the open
air; that is, they cannot fly. Understanding what modifications of the crustacean body plan have
allowed this diversification is the subject of this book.
In its basic form, the crustacean body consists of a bilaterally symmetrical, segmented, more
or less tubular body, with each segment bearing a pair of appendages. The number of body seg-
ments and the design or even presence of appendages vary considerably, with the most extreme
cases being found in those groups that have invaded the bodies of other animals.
In this book we have asked the chapter authors to explore this diversification of form and to
explain how various parts of the crustacean body work. While many authors have examined the
functional morphology and anatomy of crustaceans in individual publications or book contri-
butions, this has never been done in an integral way in one volume.
We were particularly interested in understanding the design limitations of the crustacean
body, for example, how living in a dense fluid medium might restrict the movement capabilities
of the animal, and how that would vary depending on the animal’s size. But movement isn’t all
that crustaceans do in their daily lives—they have to eat, respire, reproduce, and grow, all of
which needs to be controlled so that the animal functions as a successfully coordinated whole.
To set the stage, Schram (chapter 1) reviews the range of crustacean body plans, and Haug
et al. (chapter 2) review what is known about appendage development in the earliest arthro-
pods as they become what we would recognize now as crustaceans. Then follow four chapters
that examine the exterior of the crustacean body. Williams (chapter 3) investigates the genetic
control of appendage development as the animal develops. Olesen (chapter 4) surveys the
functional constraints of the archetypical crustacean structure, the carapace. Dillaman et al.
(chapter 5) take a detailed look at the crustacean cuticle, and Garm and Watling (chapter 6)
review the structure and function of setae and other cuticular outgrowths.
v
vi Preface
Our examination of the integrated functional aspects of the crustacean body starts with
Boxshall and Jaume’s overview of crustacean antennae (chapter 7). Watling (chapter 8) inte-
grates food consumption and digestion, showing that mouthpart appendage structure, foregut
morphology, and digestive enzyme secretion are all related to diet. Belanger (chapter 9), Faulkes
(chapter 10), Yen (chapter 11), and Boudrias (chapter 12) examine modes of locomotion in crus-
taceans and the functional constraints imposed on locomotory appendages by the physics of the
medium in which they live.
We end the book with a series of chapters dealing with system-level integrative functional
anatomy. Bauer (chapter 13) reviews the structure and function of appendages used for groom-
ing and reproduction. Wirkner and Richter (chapter 14) examine the integration of respiratory
structures with internal details of the circulatory system. An overview of the internal anatomy
of the reproductive system is provided by L ópez Greco (chapter 15). And lastly, the coordina-
tion of the whole body is dealt with in Sullivan and Herberholz’s review of crustacean nervous
systems (chapter 16).
We have asked the authors of these chapters to deal with their part of the crustacean body in
isolation. Of course, we recognize that crustaceans are living creatures, and in order to live they
have managed to integrate the functional aspects of their bodies that we have studied so well on
their own. What we have not done is try to develop a fully integrated model of the crustacean
body that accounts for all the physical aspects of the various habitats in which crustaceans live.
We suspect this is possible but may be beyond the reach of any one of us.
ACKNOWLEDGMENTS
Our thanks go foremost to all contributors who attended to all our requests during the prep
aration of this book. Their expertise and their willingness to invest time into the writing of
their contributions make up the value of this book. We especially thank our editorial assistants,
Ivan Hinojosa and Lucas Eastman, who expertly revamped many of the figures and who care
fully read and edited all the chapters. The generous contribution from Universidad Catolica
del Norte was essential for this project— we are very grateful for the continuous support which
allowed us to focus on the task. The vision and foresight of the university authorities made this
project possible and we hope that this and the upcoming volumes fulfil their expectations.
We also thank those colleagues who read entire or parts of chapters. The publisher, Oxford
University Press, gave us a lot of freedom, and in particular, we express our appreciation to Peter
Prescott, Tisse Tagaki, Jeremy Lewis, and Hallie Stebbins for their help during the past few
years. L.W. would like to acknowledge the role o f his students in stimulating him to think about
crustaceans as functionally whole units, and his friend C. Nouvian, who listened with interest
to many crustacean natural history stories while we were working on other things. Finally, we
thank our families for their patience and interest in this project— without their tolerance, none
of this would have been possible.
Editing of this book was generously supported by Universidad Catolica del Norte, Chile.
CONTRIBUTORS
E D IT O R S Michel A . Boudrias
Martin Thiel Department of Marine Science and
Facultad Ciencias del Mar Environmental Studies
Universidad Catolica del Norte University of San Diego
Larrondo 1281 Science and Technology 267
Coquimbo 5998 Alcala Park
Chile San Diego, CA 92110
USA
Les Watling
Department of Biology Geoff Boxshall
University of Hawaii at Manoa Department of Zoology
152 Edmondson Hall The Natural History Museum
Honolulu, HI 96822 Cromwell Road
USA London SW7 5BD
UK
AU TH O RS
Raymond T. Bauer Richard M. Dillaman
Department of Biology Department of Biology and Marine Biology
University of Louisiana University of North Carolina at Wilmington
PO Box 42451 601 South College Road
Lafayette, LA 70504 Wilmington, NC 28403-5915
USA USA
Jim Belanger Zen Faulkes

Department of Biology Department of Biology
West Virginia University The University of Texas-Pan American
PO Box 6057 1201W. University Drive
Morgantown, WV 26506 Edinburg, TX 78539
USA USA
Contributors ix
Anders Garm Andreas Maas

Department of Cell and Organism Biology Biosystematic Documentation
Lund University University of Ulm
Helgonavagen 3 Helmholtzstrasse 20
222362 Lund 89081 Ulm
Sweden Germany
Carolin Haug
Shannon Modla
University of Greifswald
Delaware Biotechnology Institute
Zoological Institute and Museum
15 Innovation Way, Suite 117
Department of Cytology and Evolutionary
Newark, DE 19716
Biology
USA
Soldmannstr. 23
17487 Greifswald
Germany Jorgen Olesen
Natural History Museum of Denmark
Joachim T. Haug (Zoological Museum)
University of Greifswald University of Copenhagen
Zoological Institute and Museum Universitetsparken 15
Department of Cytology and Evolutionary DK-2100 Copenhagen 0
Biology Denmark
Soldmannstr. 23
17487 Greifswald Stefan Richter
Germany Universitat Rostock
Institut fur Biowissenschaften
Jens Herberholz Abteilung fur Allgemeine und Spezielle
Department of Psychology and Zoologie
Neuroscience and Cognitive Science Universitatsplatz 2
Program 18055 Rostock
2123H Bio-Psych Building Germany
University of Maryland
College Park, MD 20742
Robert Roer
USA
Department of Biology and Marine
Biology
Damiajaume
University of North Carolina at
Instituto Mediterraneo de Estudios
Wilmington
Avanzados IM EDEA (CSIC-UIB)
601 South College Road
Miquel Marques 21
Wilmington, NC 28403-5915
07190 Esporles (Mallorca, Illes Balears)
USA
Spain
Laura S. Lopez Greco Frederick R. Schram

Facultad de Ciencias Exactas y Naturales Burke Museum
University of Buenos Aires University of Washington at
Pabellon 2, Intendente Giiiraldes 2160 Seattle
Ciudad Universitaria C1428EGA Post Box 1567
Buenos Aires Langley, WA 98260
Argentina USA
X Contributors
Thomas Shafer Terri A . Williams

Department of Biology and Marine Department of Biology
Biology Trinity College
University of North Carolina at 300 Summit Street
Wilmington Hartford, CT 06106
601 South College Road USA
Wilmington, NC 28403-5915
USA Christian S. Wirkner
Universitat Rostock
Jeremy M. Sullivan Abteilung fur Allgemeine und Spezielle
Department ofNeurology Zoologie
Johns Hopkins University Institut fiir Biowissenschaften
855 North Wolfe Street Universitiitsplatz 2
2nd Floor, Rangos Building 18055 Rostock
Baltimore, MD 21205 Germany
USA
Jeannette Yen
Dieter Waloszek School of Biology
Biosystematic Documentation Georgia Institute of Technology
University of Ulm 310 Ferst Drive
Helmholtzstrasse 20 Atlanta, GA 30332-0230
89081 Ulm USA
Germany
Les Watling
Department of Biology
University of Hawaii at Manoa
152 Edmondson Hall
Honolulu, HI 96822
USA
CONTENTS
1. Comments on Crustacean Biodiversity and Disparity of Body Plans • 1

Frederick R. Schram
2. Evolution of Crustacean Appendages • 34

Joachim T. Haug, Andreas Maas, Carolin Haug, and Dieter Waloszek
3. Mechanisms of Limb Patterning in Crustaceans • 74

Terri A. Williams
4. The Crustacean Carapace: Morphology, Function, Development, and Phylogenetic

History • 103
Jorgen Olesen
5. The Crustacean Integument: Structure and Function • 140

Richard M. Dillaman, Robert Roer, Thomas Shafer, and Shannon Modla
6 . The Crustacean Integument: Setae, Setules, and Other Ornamentation • 167

Anders Garm and Les Watling
7. Antennules and Antennae in the Crustacea • 199

Geoff Boxshall and Damia Jaume
8. Feeding and Digestive System • 237

Les Watling
9. Appendage Diversity and Modes of Locomotion: Walking • 261

Jim Belanger
xii Contents
10. Morphological Adaptations for Digging and Burrowing • 276

Zen Faulkes
11. Appendage Diversity and Modes of Locomotion: Swimming at Intermediate Reynolds

Numbers • 296
Jeannette Yen
12. Swimming Fast and Furious: Body and Limb Propulsion at Higher Reynolds
Numbers • 319
Michel A. Boudrias
13. Adaptive Modification of Appendages for Grooming (Cleaning, Antifouling) and

Reproduction in the Crustacea • 337
Raymond T. Bauer
14. Circulatory System and Respiration • 376

Christian S. Wirkner and Stefan Richter
15. Functional Anatomy of the Reproductive System • 413

Laura S. Lopez Greco
16. Structure of the Nervous System: General Design and Gross Anatomy • 451
Jeremy M. Sullivan and Jens Herberholz
Index • 485
and Diversity
1
COMMENTS ON CRUSTACEAN BIODIVERSITY
AND DISPARITY OF BODY PLANS
Frederick R. Schram
Abstract
The science of natural history is built on twin pillars: cataloging the species found in nature, and
reflecting on the variety and function of body plans into which these species fit. We often use
two terms, diversity and disparity, in this connection, but these terms are frequently used inter-
changeably and thus repeatedly confused in contemporary discourse about issues of function
and form. Nevertheless, diversity and disparity are distinct issues and must be treated as such;
each influences our views of the evolution and morphology of crustaceans.
CRUSTACEAN DIVERSIT Y
Crustaceans exhibit great disparity in basic body plans (I return to this subject below), but
disparity of crustacean form is different from crustacean biodiversity, that is, the number of
species we have within any particular group. No one knows for certain the exact number of
species within any group of organisms, although the situation might improve with the appear-
ance of online catalogs for particular groups. The people who set up these databases and
maintain them as new species are added and old species are placed in synonymy provide a
much-needed service toward adequately cataloging the tree of life. Nevertheless, as humans
we like numbers—they are easily understood. So I have made my own tally (Table 1.1) and
present a summary of estimates compiled from various authorities as to the total number of
crustacean species.
There is clearly no agreement on numbers among the authors listed in Table 1.1, although
the estimates have gone up through time. With the exception of Minelli (1993) and Brusca and
1
2 Functional Morphology and Diversity
Table 1.1. Various estimates of global numbers of species of crustaceans.
Estimated number of species Source

44,950 Bouchet (2006)
32,000 Brusca and Brusca (1990)
68,171 Brusca and Brusca (2003)
40,000 Groombridge and Jenkins (2000)
39,000 May (1988)
75,000 Meglitsch and Schram (1991)
55,364 Minelli (1993)
38,000 Ruppert and Barnes (1994)
49,658 This chapter
Brusca (2003), who appear to have attempted a real count, the other authors obviously provided
rounded off and rough estimates. For example, the number provided by Meglitsch and Schram
(1991) was an estimate of what the highest number might be at some point in time when knowl-
edge of the number of species will have reached a plateau.
Although we know a great deal about groups of invertebrates, our knowledge is not very
good and rather incomplete. I examined the patterns through time in documenting animal
taxon diversity (Schram 2003) and noted several periods during which plateaus of relative inac-
tion followed bursts in activity. It seems clear from these charted patterns that we are currently
in one of those periods of increased activity, but whether we will soon reach a new plateau, or
whether increased use of molecular techniques to identify monophyletic groups might con-
tinue to add new taxa at all levels—from phylum down to species—I cannot say. However,
increasing application of molecular techniques does seem to indicate that we have underesti-
mated the degree of cryptic speciation in nature.
Having stated this, I feel honor bound by the charge given to me by the editors to provide
my own numbers, so I tally here the currently known crustacean species. Table 1.2 is based on a
census of relevant websites, currently available monographic literature, and the best estimates
of authorities active in one or more of these groups. The reader should keep in mind that this
is a tally of species numbers at this point in time, and these figures can only increase as our
knowledge of these taxa evolves. In fact, the survey made by Martin and Davis (2006) seems
to indicate that no asymptotes are yet emerging in the pace at which new species are being
described.
First, the total number of species obtained by this survey, 49,658, is not too far off from the
estimates of Bouchet (2006) and Minelli (1993). Within that number, some things deserve spe-
cial notice. Of the two largest groups on this list, Maxillopoda and Malacostraca, the numbers
are of similar magnitude—almost 19,000 and something more than 29,000, respectively. The
number of maxillopodans can only increase. The 9,500 copepods is only an estimate, although
it may stand close to the actual numbers of currently described species. Nevertheless, copepod
taxonomy is an active discipline, and increasingly sophisticated techniques of study will help
isolate cryptic species. The 8,008 species of ostracodes is only an estimate, and if we factor in
fossil species, we would more than double that number. Furthermore, the application of molecu-
lar methods in Crustacea will likely affect our understanding of species level biodiversity. For
example, I am surprised at the relatively low number for the thecostracans, but parasitism is
rampant in the group, and underestimates of species diversity would prevail in taxa with such
Crustacean Biodiversity and Disparity of Body Plans 3
Table 1.2. Census of species numbers in various crustacean groups.
Taxon Number of species

Branchiura (Argulida) 175
Branchiura (Pentastomida) 100
Mystacocarida 13
Branchiopoda 509
Anostraca 307
Cyclestherida 1
Laevicaudata 36
Notostraca 15
Spinicaudata ≈150
Cladocera 450
Maxillopoda 18,911
Copepoda 9,500
Ostracoda ≈8,008
Myodocopida 1,608 (+500 fossils)
Podocopida 6,400 (+9,500 fossils)
Thecostraca 1,403
Ascothoracica >99
Cirripedia 1,304
Acrothoracica >61
Rhizocephala >255
Thoracica 948
Facetotecta 12
Tantulocarida 28
Remipedia 19
Cephalocarida 10
Malacostraca 29,471
Phyllocarida 39
Stomatopoda 456
Eumalacostraca 28,976
Syncarida >187
Bathynellacea >170
Anaspidacea 17
Peracarida 15,686
Amphipoda 6,950
Cumacea 1,342
Isopoda 5,270
Lophogastrida 56
Mictacea 5
Mysida sensu lato 1,085
Mysida sensu stricto 1,075
Stygiomysida 10
Spelaeogriphacea 4
Tanaidacea 940
Table 1.2. (Continued)
Taxon Number of species

Thermosbaenacea 34
Eucarida 13,103
Amphionidacea 1
Decapoda 13,016
Dendrobranchiata 522
Caridea 2730
Stenopodidea 57
Reptantia 9,707
Euphausiacea 86
Total 49,658
The higher taxonomic grouping of this table accords with the conclusions derived from the discussion of disparity of form
given later in this chapter. Classes are shown in boldface.
highly reduced body forms. For example, rhizocephalans seem poised on the edge of a renais-
sance in interest, and the number of species anticipated will increase.
Malacostraca constitutes a large number of species, but the species distribution is uneven
because some subgroups are very large (amphipods, isopods, reptant decapods), while others
are small (mictaceans, spelaeogriphaceans, and the amphionidacean). In fact, any group associ-
ated with cave or groundwater habitats appears likely at the lower end of species number esti-
mates, but these habitats are difficult to study, and every attempt to sample these communities
turns up new and interesting species, which can only continue into the future. (In this connec-
tion, one need only consider the work on crayfish in North America to see what happens when
intensive systematic interest is focused on a group.)
Some major class- and order-level taxa presently have low species numbers (remipedes
and cephalocarids), but here, too, we have animals living in habitats that are difficult to sam-
ple (anchialine caves and the deep sea). Other groups contain very cryptic creatures living in
places that, although well studied, nevertheless are often overlooked (mystacocarids in inter-
stitial beaches).
Because of the great disparity of body plans exhibited by crustaceans, we have a problem
in comparing the species numbers in one group with another. The taxa in Table 1.2 are organ-
ized around the currently recognized class and order levels, but how does one compare ordi-
nal differences seen in malacostracans with what are called orders within the maxillopodans?
Recognizing a decapod from an amphipod is quite easy (both are orders of Eumalacostraca),
but not many people could easily distinguish a cyclopoid from a calanoid (they are both orders
of Copepoda) without being carefully schooled in the differences. Hence, trying to compare
numbers of species within groups across the major taxonomic (class-level) units of crusta-
ceans is truly like comparing apples to oranges or, in this case, lobsters to zooplankton.
Nevertheless, strange patterns arise when we look within groups. Consider the peracari-
dans, for example. Why are there so many species of amphipods (6,900) compared to ther-
mosbaenaceans (34) or mictaceans (5)—approximately two and three orders of magnitude
difference? Are amphipods truly that much better adapted to their environments, an expla-
nation often assumed to be true? If so, how and why? Or, are some other factors at play that
might augment or possibly even ignore issues of adaptation? Some of these factors might be
40
A
30
Number of genera
20
10
0
5 10 15 20 25
Number of species in genus
100
B
Number of genera
10
1
1 10 100
Number of species in genus
Fig. 1.1.
Arithmetic hollow curve (A) and log-log (B) plots of size distributions of genera of Stomatopoda (as
number of included species) roughly conforming to power law N(x) = ax–b. For details about the method,
see Minelli et al. (1991).
difficulty of habitat access for study (mentioned above), age of a clade, habitat heterogeneity,
and expressions of chance in nature. The various authors of other volumes in this series will
explore many of these issues.
The element of chance plays an important role in classification. Willis and Yule (1922) and
Minelli et al. (1991) observed that the size of supraspecific taxa as related to the included sub-
taxa (species in genera, genera in families, etc.) follows a power law. They concluded that the
structure of biological classification is naturally fractal. This structure can be expressed as a
hollow curve that, if plotted on a log-log scale, would conform to N(x) = ax–b.
We can illustrate this with one example from Malacostraca, the unipeltate stomatopods
(mantis shrimp). As of this writing, we recognize 456 species in 112 genera of mantis shrimp,
with an additional 123 nominal species currently in synonymy. If we consider only the 456 rec-
ognized species, distribution numbers range from one of the largest genera, Nannosquilla, with
some 26 species, down to 36 genera with but a single species each. Graphing this diversity, we
can see that on an arithmetic scale it forms a hollow curve (Fig. 1.1A), and on a log-log plot a
straight line emerges (Fig. 1.1B). The fractal pattern becomes apparent when examining genera
within families (data not shown), where we would again see a log-log plot that roughly matches
that of species in genera. Whether this pattern appears in other groups of crustaceans remains to
be tested, but I have no doubt that it will hold as it has in other groups of animals and plants.
As humans, we are naturally inclined to seek causative explanations for patterns of biodi-
versity. However, I believe we do not necessarily need to explain why one particular genus,
such as Nannosquilla with 26 species, is somehow better adapted than its confamilial sister
genera, in this case Mexisquilla and Keppelius, each with only a single species. As we chart spe-
cies biodiversity, we should be open to the possibility that the relative number of taxa within
any particular group may represent nothing other than the manifestation of the operations of
a stochastic, fractal universe, to say nothing of the vagaries of individual taxonomic decisions.
Many authorities might reject my pessimism here, but at the very least, a stochastic, fractal
biodiversity has to be one of several alternative hypotheses to consider.
CRUSTACEAN DISPARIT Y OF BODY PLANS
The crustaceans are the most variable of all the arthropod groups; that is, there is a great dis-
parity of body plans throughout their ranks (Fig. 1.2). If we are to assume that Crustacea is a
monophyletic group, then they are not like any other arthropods. This high degree of variability
is a very real problem with some serious implications, because if we take this disparity of form
at face value, then we should seriously question whether all these various groups can constitute
a single monophylum.
When one looks at other major arthropod groups outside of Crustacea, there appears to be
no great disparity of plan within these taxa (see Meglitsch and Schram 1991); members of each
group fit a concise definition. For example, members of Insecta (Hexapoda) have a body divided
into a five-segment head with the first postantennal segment bearing appendages modified as
a labrum, a three-segment thorax with two sets of wings in the pterygote insects borne on the
second and third segments, and an abdomen of 10–12 somites. All insects conform to this defini-
tion with some exceptions, for example, allowing for fusion of segments at the terminus of the
abdomen or modification of wing arrangements. Insects have a unified body plan.
Myriapoda as a whole do vary in some features such as body length but have in common
that their trunk is not divided into a thorax and abdomen and that their gonopores are gener-
ally located on the anterior aspect of the trunk. The individual groups of myriapods conform
to common plans: Symphyla have 12 trunk segments with the gonopores on the fourth somite;
Pauropoda bear 12 trunk segments with the gonopore on the second somite; and Diplopoda,
with several very distinct orders, all exhibit well-developed diplosomites, that is, pairs of seg-
ments fused dorsally but distinct ventrally, and their gonopores are located on the second
trunk segment. The individual orders of diplopods vary only regarding the total number of
trunk somites: pselaphognaths have at least 10–12, but colobognaths can exceed 30. Chilopoda
have variable trunk segment numbers, extending from 15 to more than 180 pairs of legs, depend-
ing on group, but all chilopods without exception have long antennae and modify the first
trunk limb as a fang equipped with a poison gland to facilitate their carnivory. Centipedes also
uniquely bear gonopores on the posterior aspect of the trunk.
The subphylum Cheliceriformes exhibits only a few “head” segments, essentially two, and
these are fused with the anterior, or locomotory, part of the trunk to form a prosoma. The ante-
riormost somite (the one just posterior to the asegmental acron), the homolog of the antennal
segment in other arthropods, does not carry antennae but rather is equipped with a pair of che-
licerae. The second segment, what in other arthropods is referred to as the first postantennal
Fig. 1.2.
Disparate body types among crustaceans.
segment, typically bears a well-developed set of limbs, albeit variously developed. There are no
exceptions to this basic format.
Within the cheliceriforms, the highly distinctive Pycnogonida appear to be all legs, their
prosoma reduced to a thin cylinder. The mouth is located terminally on a long proboscis. The
small turreted “head” bears chelicerae, a second set of limbs called palps, and a third set of
limbs modified as ovigers in the males. Posterior to these limbs, most pycnogonids utilize four
pairs of legs for locomotion (a few forms with five or six pairs are known). All sea spiders con-
form to this body plan.
Arachnida have a six-segment prosoma, with chelicerae, pedipalps, and four pairs of walk-
ing legs. The trunk bears an additional opisthosoma of diverse form but composed of some 13
somites, with the first segment greatly reduced as a narrow pedicel and the second bearing the
gonopores. Opisthosomal limbs are missing or greatly reduced. Despite a great variety of body
profiles, especially regarding the opisthosoma, all arachnids conform to this single plan.
Merostomata, a small group today, was more extensive (and diverse) in the past. The
prosoma bears six pairs of limbs. The chelicerae are followed by four sets of modest-sized
walking limbs with specialized gnathobases, the first of which in the males is modified for
grasping the female during copulation, and a somewhat larger fifth set effective in groom-
ing the underside of the prosoma. The next somite, the pregenital segment, is reduced but
bears modified limbs, the chilaria. Unique among living cheliceriforms, the opisthosome
of the merostomes bears six pairs of limbs posterior to the genital segment. All merostomes
conform to this plan.
From this short review, we can see that all these groups of arthropods have concise diag-
noses, with distinct sets of apomorphies that characterize all members of the group. Crustacea,
if viewed as a single group, simply does not have this.
CAN WE DIAGNOSE A MONOPHYLETIC CRUSTACEA?
Any invertebrate zoology textbook can provide a set of characters for Crustacea. When I was
asked to provide such a diagnosis 25–30 years ago (Schram 1979, 1982), I certainly did not hesi-
tate. However, we now realize it is not sufficient to simply string together any list of characters.
Ideally, as in the arthropod examples cited above, these characters should be unique derived
features that diagnose all members of the group. To rephrase this in contemporary terms, a diag-
nosis should offer synapomorphies that together uniquely delineate a monophyletic group. We
strive for natural taxonomies, classifications that reflect evolution. It is critical to determine if
this is possible for Crustacea.
A commonly accepted diagnosis of Crustacea consists of the following: (1) head of five
somites, each bearing a set of appendages consisting of two pairs of antennae, a pair of mandi-
bles, and two pairs of maxillae; (2) body consisting of three regions: head, thorax, and “abdo-
men”; (3) trunk appendages primitively multiramous; and (4) development consisting of a
series of discrete larval and/or juvenile stages, initiated by a stage termed a nauplius.
Let us inspect these features one by one in order to determine if these characters provide
that unique set of descriptors we require for a diagnosis of Crustacea. In the discussion below, I
restrict the term Crustacea to mean a monophyletic group and the term crustaceomorph to con-
note the amalgam of arthropod types that we generally and broadly refer to as “crustaceans”
(fossil and recent) but that may or may not be monophyletic. Table 1.3 will assist the reader in
following along the taxa and many of the relevant features discussed below.
“Head of five somites, each bearing a set of appendages consisting of two pairs of
antennae, a pair of mandibles, and two pairs of maxillae”
These are not a unique set of features. A head consisting of five somites is shared with insects
and the myriapods (see above; Meglitsch and Schram 1991), and, as would follow, most of the
head appendages of these somites are shared among the three groups, namely, the first set of
antennae, mandibles, and two sets of maxillae. It is only regarding the so-called second set of
antennae that we might have a distinctive crustaceomorph feature since myriapods and insects
lack a limb in this position.
The second antennae are generally perceived as specialized sensory limbs and as such could
serve as a defining apomorphy. This descriptor arises from the mental image of Crustacea con-
jured up by thinking of a shrimp or a lobster (a malacostracan), and this image without a doubt
presents us with an icon of an arthropod with a set of sensory limbs at this position, albeit with
slight anatomical variations, depending on group (Fig. 1.3A).
Nevertheless, sensory second antennae are not characteristic of all groups of crustaceo-
morphs. Chapter 7 provides additional details concerning antennae, but a short overview
will suffice here to make a point. Remipedes have quite distinctive limbs in this position
(Fig. 1.3B) that I suspect serve equally as a hydrofoils to direct currents of water that f low
Table 1.3. Comparative morphology of various aspects that define body plans among various groups of crustaceomorphs.
Taxa Head Trunk Postthorax Thorax length Segment no. of gonopore Trunk First larval
(no. somites) regions (no. somites) position limb rami segments
Male Female
Oligo-crustacea
Branchiura 5 2 – 4 4 4 2 ?
Mystacocarida 2 a 5 4 4 1 4
Skara 5 2 a 1 ? ? 2 ?
Martinssonia 4 2 a 3 ? ? 2 4
Branchiopoda
Laevicaudata 5 1 – 10–12 11 11 M 3
Notostraca 5 ?2 ?p 11 11 11 M 3
Spinicaudata 5 1 – 16–32 11 11 M 3
Cyclestheria 5 1 – 16–32 11 11 M 3
Cladocera 5 2 – 4–6 3
Anostraca 5 2 a 12 12 M 3
Lepidocaris 5 2 a ? 2, M
Rehbachiella 5 2 a 12 ? 2 3
Waptia 5 2 a 11 ? ?
Eucrustacea
Cephalocarida 4 2 a 8 6 6 M 5
Maxillopoda
Copepoda 5 2 a 7 7 7 2 3
Cirripedia 5 1 a 7 7 1 2 3
Ostracoda ?7 ?7 3
Bredocaris 5 2 a 7 ? 2 4
Malacostraca
Eumalacostraca 5(+) 2 p 8 8 6 2 3
Hoplocarida 5(+) 2 p 8 8 6 2 3
Phyllocarida 5 2 p 8 8 6 M 3
Remipedia 6 1 – – 15 8 2 3
Abbreviations: a, abdomen; M, multiramous; p, pleon. Neither the list of taxa nor the features are exhaustive of all possibilities but cover the major elements discussed in the text.
C C'
anterior spine
palp
antennule F
E
antenna
posterior
spine G
Fig. 1.3.
Various functional types of “antennal” limbs found in crustaceans. (A) Sensory: Apseudes hermaphro-
diticus, tanaid (from Lang 1953). (B) Swimming hydrodynamic plane: Lasionectes entrichoma, a remipede
(from Schram et al. 1986). (C and C′) Locomotory/feeding: Derocheilocaris ingens, a mystacocarid (from
Hessler 1969), antenna (C) and mandible (C′). The arrow indicates gnathal lobes. (D) Part of an attach-
ment complex: Argulus foliaceous, a branchiuran (from Martin 1932). (E) Swimming: Archimisophria dis-
coveryi, a copepod (from Boxshall 1983). (F) Host penetration: Gorgonolaureus muzikae, an ascothoracidan
(from Grygier 1981). (G) Swimming/feeding: Bredocaris admirabilis, a Cambrian maxillopodan (from
Mü ller and Walossek 1988).
around the head and perhaps also to aid in creating some of those currents by f lapping the
hydroplane-like exopods. Although no work has yet been done on functional morphology
of this limb, I believe it safe to say that the remipede antenna is not a purely sensory append-
age. Mystacocarids have a pair of limbs behind the first antennae that are virtually identi-
cal in form to the mandibles (Fig. 1.3C,C′), except these so-called second antennae lack the
gnathal armament at the base of the limb that occurs on the mandibles. The mystacocarid
“antennae” are locomotory limbs. Branchiurans possess broad plates in this position with
basal hooks and terminal, recurved spines—nothing sensory at all but rather serving to assist
with attachment (Fig. 1.3D). Tantulocarids lack head appendages altogether. Copepods have
well-developed limbs in this position that serve for the most part as the primary organs of
swimming (Fig. 1.3E). It is difficult to specify what this limb does in ascothoracicans, where
all head limbs are highly modified to achieve attachment to a host or to penetrate host tis-
sues (Fig. 1.3F). In cirripedes, the adults lack the antennae, but the nauplius and cypris lar-
vae have limbs in this position to assist in swimming; the second antennae disappear at the
time of attachment prior to metamorphosis to the adult cirripede. Finally, within the wide
array of Cambrian microarthropods that are considered to bear some relationships to modern
groups (see chapter 2), such as Bredocaris (Fig. 1.3G), Martinssonia , Rehbachiella , Skara , and
Walossekia , the so-called second antennae are more often than not locomotory limbs, similar
in structure to the mandibles and maxillae of these fossils.
We can conclude from this brief survey that the only character that Crustacea share at this
position, that is, the first segment posterior to the true antennae, is simply the presence of a pair
of limbs. However, this is to say nothing—the mere presence of limbs on the first postantennal
segment, or any postantennal segment for that matter, is a generalized, primitive, or plesiomor-
phic feature.
As noted above, merostomes, pycnogonids, and arachnids also have a limb in this position,
but that does not make them crustaceomorphs. In arthropods, all segments generally carry
limbs, at least on the head and thorax; it is only when limbs are particularly specialized, or even
missing, that things become more interesting and can serve to help diagnose a group. For exam-
ple, the presence of a limb on this first somite posterior to the antennae in crustaceomorphs
stands in contrast to what occurs in myriapods and insects. In these latter groups, the limb buds
on the first postantennal somite are diverted from forming a limb into producing the special
labrum seen in these groups. We know this is so because, at least for insects, developmental gene
expression studies reveal that the labrum is the “appendage” of the so-called intercalary (first
postantennal) segment (Boyan et al. 2002). This diversion of the first postantennal anlagen into
forming the upper lip rather than a set of limbs clearly is a derived feature. It is the lack of limbs
on the first postantennal segment of insects and myriapods that is a noteworthy and significant
apomorphy, not the mere presence of a limb on that segment as occurs in crustaceomorphs,
cheliceriforms, and many fossil groups such as trilobites.
Crustacea are generally said to have a five-segment head. However, many crustaceomorph
groups include at least one pair of maxillipeds and the associated “thoracic” somite into the
head, and we thus speak of a cephalothorax. Most of the time, it is clear that these maxillipeds are
obviously modified anterior thoracic limbs. Development in the many crustaceomorph groups
that have maxillipeds allows us to document successive stages wherein the maxillipeds become
specialized and their associated somites through successive molts become incorporated into
the cephalon during ontogeny. However, at least one group of crustaceomorphs, the remipedes,
does not exhibit such a transition. Koenemann et al. (2007, 2009) observed no biramous precur-
sor state to the uniramous maxilliped in the earliest larval stages—the remipede maxilliped and
its segment are part of the head in the earliest recognized ontogenetic stages. Consequently, we
could say that the remipedes, for all intents and purposes, have a six-segment head (Koenemann
et al. 2009).
In summary, this first part of the diagnosis of Crustacea (head of five somites, each bearing
a set of appendages consisting of two pairs of antennae, a pair of mandibles, and two pairs of
maxillae) is not informative.
“Body consisting of three regions: head, thorax, and ‘abdomen’”
Body tagmosis is often an important component of defining an arthropod body plan. For exam-
ple, as noted above, among the chelicerates a discrete head is lacking because the anterior seg-
ments associated with feeding and sensation are fused with the segments bearing the walking
limbs to form a solid unit, the prosoma, a very distinctive feature.
The possession of a head, thorax, and abdomen is certainly distinctive, but it is also a feature
shared with insects. Hence, while we might appear to have, with tagmosis, another argument
for seeking some kind of relationship between crustaceomorphs and insects, that is, within a
monophylum Pancrustacea or Tetraconata (Wheeler et al. 2004, Giribet et al. 2005), we do not
have an effective component for a definition that seeks to uniquely define Crustacea.
Furthermore, crustaceomorphs themselves vary considerably in this regard, as we will pur-
sue in more detail below. The number of thoracic segments can be characteristic, but only
for individual crustaceomorphs and not for Crustacea as a whole. Remipedes have a long,
homonomously developed trunk with no differentiation between anterior and posterior sec-
tors. Mystacocarids have five and branchiurans have four thoracomeres. Large-bodied bran-
chiopods often have 11 or 12 thoracomeres. Many maxillopodans and the malacostracans have
seven or eight thoracomeres: maxillopodans sensu stricto have seven, while cephalocarids and
malacostracans have eight.
Moreover, the possession of an abdomen is not a uniting feature. This variability is true
not only regarding external, gross anatomical features such as total numbers of segments and
those with and without paired limbs on the segments, but also for the underlying expression of
Hox (homeobox) family genes as well (Fig. 1.4). In connection with the latter, Abzhanov and
Kaufman (2004) and Schram and Koenemann (2004a) surveyed the available information
concerning Hox gene expression in crustaceans. There are two fundamentally different types
of posterior tagmata: the abdomen, a region without expression of the abd-A (abdominal A)
Hox gene; and the pleon, a region with the expression of abd-A . Species with the latter type,
the malacostracans, possess appendages on the segments and also display a well-differentiated
central nervous system in that body region, whereas species with the former type, which lack
abd-A expression in that body region (branchiopods and maxillopodans), lack appendages on
these segments and do not have a well-differentiated central nervous system in these segments.
It is for this reason that Schram and Koenemann (2004a) concluded that the old term pleon, as
applied to the posterior region of the trunk of malacostracans, is not just an equal and inter-
changeable alternative for the term abdomen; the use of pleon as a descriptor is an absolute neces-
sity. Hox gene expression indicates that the pleon of malacostracans and the abdomen of other
crustaceans exhibit fundamentally different developmental pathways.
Admittedly, the amount of available data is limited. As is the case with developmental work,
researchers focus on the study and manipulation of model organisms. Among malacostracans,
Porcellio scaber and Procambarus clarkii provided the model systems of preference for studies
of Hox patterning, and among entomostracans, Artemia franciscana and Mesocyclops edax have
served as the models, and the latter has been only incompletely investigated. The determina-
tion of Hox gene expression in diverse arthropods was a leading line of research in arthropod
evo-devo studies in the late 1990s and early 2000s, but such investigations have waned, at least
for now. In light of the above phylogenetic usefulness of this line of research, we should look
forward to more animals being investigated in this regard.
Nevertheless, this part of the definition of crustaceans (body consisting of three regions:
head, thorax, and “abdomen”) is not a particularly informative statement.
“Trunk appendages primitively multiramous”
This descriptor is also not very informative. The presence of bi- and/or multiramous limbs is
widely accepted to be a primitive condition in Arthropoda; most authorities would concede
that uniramy is derived. However, here, too, the devil is in the details. Schram and Koenemann
(2001) reviewed the information available concerning early development of crustacean limbs,
and Williams (see chapter 3) delves into this subject more deeply.
lap pb z2 zen Dfd Scr ftz Antp Ubx abd-A abd-B
Anostraca
Antp (Branchiopoda)
Ubx
abd-A Abd-B
lab
pb Porcellio scaber
Dfd Scr Antp
(Malacostraca)
Ubx abd-A
Abd-B Abd-B
Procambarus clarkii
Scr
Antp (Malacostraca)
Ubx
Abd-B abd-A Abd-B
Mesocyclops edax
Ubx (Maxillopoda)
abd-A Abd-B
Fig. 1.4.
Hox gene expression pattern for various crustaceans. Shaded areas denote thorax or thorax/pleon. Note
the different patterns from an abdomen (no Hox) and a pleon (with abd-A). Modified from Schram and
Koenemann (2004a).
We can summarize here, nevertheless, a few basic patterns of limb development. One,
in which the proximal pedestal of the limb carries distally a tubular, segmented telopod, is
sometimes referred to as the Drosophila model because it was first recognized and studied
in detail using the fruit f ly Drosophila (Cohen 1990). It is the most common pattern of limb
development seen in all biramous crustacean limbs that have been examined, particularly
using Mysidopsis bahia (Panganiban et al. 1995). The limb anlage becomes forked, leading
eventually to the exopodal and endopodal rami. The gene distalless (dll) is expressed at the
tips of the developing rami. A rather different pattern, however, prevails in Branchiopoda,
often referred to as the Artemia model and documented with studies on Artemia and Triops
(Williams and Mü ller 1996, Williams 1998). Rather than a uni- or biramous limb anlage,
limb development begins with a mediolaterally directed ridge upon which eight lobes sub-
sequently appear. The expression of dll occurs in varying patterns on these eight lobes,
which proceed to form the unarticulated, leaf like limb, or corm, characteristic of the bran-
chiopods. Similar gross anatomical sequences of limb development (though without the
related gene expression patterns) have been documented for Cyclestheria (Olesen 1999)
and the cladocerans (Olesen 1998). Hence, the multiramous limb of branchiopods has a
fundamentally different mode of development from that seen in the crustaceans bearing
biramous or uniramous limbs.
Thus, this part of the definition of Crustacea (trunk appendages primitively multiramous)
is not an informative statement. The statement equates all crustaceomorph limbs and ignores
widely divergent, perhaps incompatible, modes of development.
“Development consisting of a series of discrete larval and/or juvenile stages,

initiated by a stage termed a nauplius”
In examining this characteristic sequence, we possibly come upon firmer ground in seeking a
unique set of features to define Crustacea. Many living groups of arthropods exhibit epimorphic
development. The animals essentially hatch with the complete set of segments characteristic of
the adult; the individuals increase in size only with each molt.
Other groups of arthropods (some of the myriapods), although they resemble the adults
in general form, hatch with fewer segments than the adults and add segments with each
molt. Some Crustacea do this; for example, peracarids brood their young, and some of these
are expelled from the marsupium as little “juvenile” forms, called mancas , which eventually
molt and add a segment to achieve the adult condition.
Many crustaceomorphs, however, hatch as larvae, and these larvae not only possess fewer
segments than the adults but also exhibit a distinctive larval form. Successive molts then not
only add segments but also metamorphose the form. Does this constitute an apomorphy for
Crustacea? Other arthropods have larvae. Extensive larval stages are known for the trilobites,
and pycnogonids have a larva; many larvae, both nauplii and other intriguing forms, are known
from the fossil record (see Mü ller and Walossek 1986). However, there are distinctive patterns
of molting and metamorphosis that serve to absolutely unite some crustaceomorphs. Taxa
within Cirripedia are clearly united by the presence of a distinctive nauplius with frontola-
teral horns and a postnaupliar cypris larva in the life cycle. Branchiopods have a characteris-
tic nauplius with a naupliar process on the antennae. Zoeae are diagnostic larvae of decapod
malacostracans.
The nauplius stage is often said to represent a phylotypic stage through which in theory
all Crustacea passed in the course of the evolution of the group. We need to express some
caution here—not all crustaceomorphs begin independent life as a nauplius larva, that is,
exhibiting a larva characterized by possession of only three sets of limbs: the first and sec-
ond antennae and the mandibles. There are crustaceomorphs that do (or did) not begin life
as a nauplius but rather have as the initial stage a metanauplius, that is, a stage with more
than just the three sets of naupliar limbs and/or more than the three naupliar segments.
The issue is confused in the literature with the almost completely interchangeable use of
the terms nauplius and metanauplius . This interchangeability implies that it is almost irrel-
evant as to what the basic structure of the first larva is—if it is tiny, possesses only a small
number of limbs and segments, is given to swimming, and may or may not be filter feeding,
then it is a “nauplius.” We see here the differences between a structural and a functional
definition.
Which groups have an orthonauplius—a larva with only three pairs of appendages as
seen in Branchiopoda, Maxillopoda, Remipedia, and euphausiacean and dendrobranchiate
Malacostraca? Each of these orthonauplii bears a distinctive form. As noted above, branchio-
pod nauplii possess a naupliar process on the second antenna designed to facilitate feeding.
Variations occur within the Maxillopoda. Among the most distinctive of nauplii, those of
cirripedes bear anterolateral horns, frontal filaments anterior to the first antennae, and a long
caudal process. There are four to six naupliar stages, depending on the group. Copepod nauplii
exhibit a nauplius in almost its complete and pristine state, although the two orthonaupliar stages
are nonfeeding because the gut is not developed until the metanaupliar phase. Ostracodes pass
through a single nauplius stage, but the limbs are not completely developed, and in some species
the early developmental stages (nauplius and the metanauplii) are retained within the mother’s
shell until they are shed near the end of their development. The Cambrian fossil Rehbachiella
had an orthonauplius. Finally, the free nauplii of the euphausiaceans (two) and dendrobranchi-
ates (one) are very simple in form and do not feed, and even the succeeding metanauplii can be
nonfeeding, also true of remipedes. Most of the other eumalacostracans pass through a clear
egg-nauplius phase within the egg (Schram 1986).
The diversity of naupliar form and function led Scholtz (2000) to suggest that we should dis-
tinguish between primary and secondary nauplii, that is, between nauplii that are indeed primi-
tive and an original part of the life cycle, and nauplii that are secondarily reevolved. Scholtz
believes that the primitive stage for malacostracans is the embryonized egg-nauplius and that
the nonfeeding, free nauplii of euphausiaceans and dendrobranchiates actually evolved from
ontogenetic sequences without a free nauplius. One consequence of Scholtz’s observations is
that the nauplius larva would not be a phylotypic stage for all crustaceomorphs.
Other groups of crustaceomorphs exhibit a variety of first stages in their development.
Cephalocarida begin as a metanauplius, the first stage of which has five limbs and a variable
number of limbless segments. Mystacocarida hatch as metanauplii with four sets of limbs and
five additional limbless segments.
The significance of these metanaupliar stages becomes evident when we consider the lar-
val development in certain of the Cambrian Orsten microarthropods. The larval sequences for
many of the Cambrian Orsten taxa are known; Bredocaris, Martinssonia, and Phosphatocopina
all had four sets of limbs in the earliest phases, what Walossek has referred to as a “head larva”
(Walossek and Mü ller 1990). Agnostus and the other trilobites in their earliest stages also bear
four. There seems to be a basis for concluding that the naupliar stage, with its three sets of limbs,
is derived from forms with four (possibly five) sets of limbs.
Larvae are features of aquatic arthropods, but the nauplius larva is undoubtedly a derived
form. Unfortunately, not all crustaceomorphs have a nauplius, which is perhaps a problem
whose full implication remains to be determined; some groups may have lost it, but other groups
probably never had it.
At the beginning of this section I asked the question, What is Crustacea? It appears that
we cannot use an unambiguous set of apomorphic descriptors to diagnose a monophyletic
Crustacea. Developmental patterns and the nauplius larva appear to offer the best chance of
doing so. However, since we have crustaceomorphs that do not exhibit the naupliar stage, we
might conclude that the nauplius has evolved independently several times in the evolution of
crustaceomorphs or has been lost several times; otherwise, if one demands that the nauplius be
treated as diagnostic, Crustacea is not a monophyletic group.
It would appear from the above discussion that we must conclude that crustaceomorphs
are whatever is left over among the arthropods after we have assigned everything else to other
clearly defined monophyletic groups.
WHAT ARE THE CRUSTACEOMORPH BODY PLANS THAT MIGHT

BE MONOPHYLETIC?
We now have a conundrum. If we cannot define a monophyletic Crustacea with a single, consist-
ent set of derived characters, can we perhaps diagnose smaller monophyletic groups within the
current array of crustaceomorphs? I do believe that there are groups within this assemblage that
are monophyletic (Schram and Koenemann 2004a).
Short-Bodied Forms (Oligo-Crustacea)
Branchiura
Two groups of short-bodied forms at first glance would not appear to be at all alike (Fig. 1.5)
but share a similarity regarding gonopore location. The living branchiurans are parasites of
fish with highly modified mouthparts, but their gonopores open on the fourth thoracic somite.
While there appears to be an abdomen, it is not differentiated into segments and is little more
than a single or bilobed sac (Fig. 1.5A–C). Of special note is Pentastomida, the sister group of the
branchiurans. Comparative sperm ultrastructure (Wingstrand 1972) and molecular sequence
studies (Abele et al. 1989) revealed a close link of Branchiura with Pentastomida, odd wormlike
parasites of the respiratory system in higher vertebrates (Fig. 1.5E).
This pairing of branchiurans and pentastomids might appear peculiar, but it is a group
of great age; pentastomid fossils exist from the early Paleozoic Orsten faunas (Walossek and
Mü ller 1994, Walossek et al. 1994). The several species of Cambrian/Ordovician pentastomids
(Fig. 1.5D) can convincingly be compared to living pentastomids (see Walossek and Mü ller 1994,
their fig. 21), although the fossils have trunk limbs but lack the proboscis bearing the mouth.
Walossek and colleagues interpret these fossils as parasites, but there is no direct evidence of
this. These fossils could have been ordinary free-living members of the infauna. Nevertheless,
what the fossils do show without any debate is that, in combination with the sperm and sequence
data above, the ancestry of branchiurans is very ancient.
Mystacocarida
In contrast to the branchiurans, the mystacocarids are microscopic members of the beach meio-
fauna, almost wormlike in form, with a well-developed set of mouthparts, including maxilli-
peds, but with four pairs of rudimentary thoracic limbs (Fig. 1.5F). The gonopores are located
on the fourth thoracic somite. Mystacocarids, too, may be of great age because, in some respects,
they are not unlike Skaracarida, the Cambrian fossil group from the Orsten of Sweden (Mü ller
and Walossek 1985) (Fig. 1.5G).
Schram and Koenemann (2004a), using morphologic analysis tempered by Hox gene expres-
sion, found mystacocarids and branchiurans to be sister taxa. The results of molecular studies
for both of these groups are confusing because long-branch attraction has been a persistent prob-
lem in these analyses; for example, Spears and Abele (1997) encountered this phenomenon when
their results placed mystacocarids, remipedes, and cephalocarids together and in some proxim-
ity to chelicerates (a strange array), and the branchiurans emerged in a clade with podocopan
ostracodes. Giribet et al. (2005) increased both the number of taxa sampled and genes sequenced
but obtained a confusing collection of results depending on variant runs of taxa sampled (with
and without fossils): mystacocarids and branchiurans sometimes appear alongside copepods and
ostracodes; under other circumstances, branchiurans emerge elsewhere. Although the taxon
sampling of Giribet et al. (2005) is impressive for all arthropods (and especially for hexapods), it is
not particularly broad within crustaceomorphs. More recently, Regier et al. (2008) using nuclear
A
C
D
m E
mp
Fig. 1.5.
Body types of “short-bodied” crustaceans. (A–C) Diverse types of Branchiura (from Schram 1986). (A)
Argulus. Note the highly modified mouthparts for attachment. (B) Dipteropeltis, with highly reduced
body and winglike carapace. (C) Chonopeltis, displaying weak trunk and limb segmentation. (D and E)
Diagrammatic Pentastomida (modified from Walossek and Mü ller 1994, their fig. 21). (D) Diagram similar
to the Cambrian genus Heymonsicambria. Note the reduced trunk limbs (t). (E) Diagram of a general-
ized living pentastomid. m, mouth; g, gonopore; light gray, anterior trunk; dark gray, posterior trunk or
abdomen. (F) Derocheilocaris, a mystacocarid. The arrow indicates approximate location of gonopore on
fourth trunk limb. (G) Skara minuta Mü ller and Walossek, 1985, a Cambrian fossil crustacean that might
represent a mystacocarid stem form. mp, maxilliped.
A
Malacostraca
Maxillopoda
Branchiopoda
Cephalocarida
Remipedia
B
Hexapoda
Xenocarida Remipedia
Leptocarida
Malacostraca
Maxillopoda
Sensus stricto
Branchiopoda
Brachiura
Mandibulata Oligostraca Mystacocarida
Arthropoda Ostracoda
Myriapoda
Chelicerata + Pycnogonida
Onychophora
Tardigrada
Fig. 1.6.
(A) A classic understanding of crustacean phylogenetic relationships, based on morphology. (B) A sum-
mary version of one of the more recent molecular phylogenies. Modified after Regier et al. (2010).
protein coding genes also found branchiurans as a sister taxon to podocopan ostracodes. While the
breadth of their molecular sample was impressive, the taxon sample was again selective; for exam-
ple, no mystacocarid was included. To remedy the situation, Regier et al. (2010) have expanded
the taxon base and increased the number of genes sequenced; their results identified a clear clade
with Mystacocarida, Branchiura, and Pentastomida within a group they termed “Oligostraca”
(Fig. 1.6). The analysis by Koenemann et al. (2010) also placed these short-bodied groups together
these short-bodied groups. Oddly, these clades also contained Ostracoda (see below).
The shortness of the body in these orders imposes definite constraints. The lack of an
elaborated abdomen in branchiurans and pentastomids undoubtedly limits their ability to
move around. One could speculate whether this lack was a factor in both groups adapting para-
sitic lifestyles. So, too, with mystacocarids: the lack of a well-developed abdomen could have
constrained adapting a vermiform, interstitial existence where abilities to swim or otherwise
move around are minimized.
Branchiopoda
Living Branchiopoda
This large and fascinating group is almost exclusively restricted to freshwater, with a few
exceptional cladocerans that are marine. One is tempted to speculate that they might have been
marine to begin with and then shifted to fresh waters. However, the evidence for that is not
robust, and even most of the fossils, such as they are (mostly conchostracans), are preserved in
freshwater to brackish water situations.
The branchiopods do exhibit a distinctive set of features that outline a body plan for
the group. We have noted above in passing the distinctive mode of limb formation—from
horizontal ridges that subsequently become multilobed, rather than uni- or biramous limb
bud anlagen—and the nauplius larva. Consideration of the large-bodied branchiopods adds
some further depth to our knowledge of the branchiopod bauplan, of which Anostraca serves
as a model.
Traditionally (see Calman 1909, Schram 1986), anostracans were conceived as having
an 11-segment thorax and a 9-segment abdomen. The first two legless, abdominal segments
formed a fused genital complex. However, Hox gene expression studies reveal that the genes
Antennapedia (Antp), Ultrabithorax (Ubx), and abd-A all are expressed in the thorax of Artemia,
with a residual expression of Antp in the genital segments (Fig. 1.4). Abdominal B (abd-B), a
marker for “end of thorax” and the genital segments, occurs in the genital segments (Abzhanov
and Kaufman 2004, Schram and Koenemann 2004a). Hence, the genital segments are better
considered thoracic, rather than abdominal, with the gonopores being carried on the twelfth
segment of the thorax. The abdominal segments posterior to the genital complex do not exhibit
Hox gene expression.
Notostraca and the conchostracans have the gonopores opening on the eleventh or
between the eleventh and twelfth trunk segments. Notostraca (Fig. 1.7A,B) carry a well-
developed pair of limbs on each of the “thoracic” segments (the first two being somewhat
modified from that seen on the others), but posterior to this region the limbs become
increasingly smaller as one moves posterior in the sequence of somites, and there is little
correspondence between the number of limbs and the segment boundaries—there are many
more limbs than apparent segments. Regrettably, as yet no Hox gene expression studies have
been performed on notostracans.
The conchostracans are now generally divided into three monophyletic groups: Laevicaudata
(Fig. 1.7C), Spinicaudata (Fig. 1.7D), and Cyclestherida (Fig. 1.7E) (Martin and Davis 2001), but
they, too, appear to carry the gonopore in a position similar to that of Notostraca. The first
of these, the laevicaudatans, or Lynceidae, have fewer trunk segments than the other two, but
at least the female gonopore opens near the base of the eleventh, or penultimate, appendage
(Linder 1945). The location of the male pore still must be confirmed (Martin et al. 1986). The
other conchostracan groups have many more trunk segments, up to 32, with no differentiation
between segments and limbs posterior to the genital openings, which are said to occur on the
eleventh somite.
Thus, most Branchiopoda feature thin, foliaceous, unjointed limbs, with trunks divided into
an anterior section with well-developed limbs and good Hox expression, and with gonopores at
or near the eleventh or twelfth trunk somite. The four groups of Cladocera (Fig. 1.7F–I), while
they are clearly branchiopods, exhibit extreme forms of body reduction, or oligomery. All these
branchiopods bear either a well-developed carapace or a derivative thereof. Only the anostra-
cans (Fig. 1.7J) lack a carapace, and most authorities place the fairy shrimp as a sister group to all
other branchiopods (Richter et al. 2007).
The restriction of branchiopods to freshwater habitats entices one to wonder why these
groups have become so limited. The unique mode of limb development perhaps precludes the
development of anything other than thin, foliaceous, cormlike appendages. This in turn might
have engendered an overall body habitus that lacks well-sclerotized and/or calcified body
somites. Under these constraints, freshwater habitats, especially transient ones, provide satisfac-
tory refugia.
C
G
Fig. 1.7.
Body types of Branchiopoda. (A and B) Lepidurus arcticus, Notostraca (after Sars 1896): with carapace
removed (A) and with carapace intact (B). (C–E) Various conchostracans. (C) Lynceus gracilicornis,
Laevicaudata (modified from Martin et al. 1986). (D) Limnadia lenticularis, Spinicaudata (after Sars 1896).
(E) Cyclestheria hislopi, Cyclestherida (after Sars 1887). (F–I) Various infraorders of Cladocera (after
Lilljeborg 1901, Birge 1918). (F) Sida crystalline, Ctenopoda. (G) Bosmina longispina, Anomopoda. (H) Podon
intermedius, Onychopoda. (I) Leptodora kindtii, Hoplopoda. (J) Branchinecta lindahli, Anostraca (after
Lynch 1964).
Fossil Stem-Branchiopods
All authorities accept crown group Branchiopoda as a monophyletic group, based on the dis-
tinctive nauplius larva and the form and ontogeny of the trunk limbs. However, the branchio-
pods are also noteworthy in that a number of fossil forms are known that either occupy a stem
position to the branchiopod clade or in some instances actually stand within the group.
A
B
? E
Fig. 1.8.
Fossil species that might have some relationship to Branchiopoda, either near the base of that group or
as stem forms. Arrows indicate the twelfth thoracomere, the segment at or just posterior to the end of
the thoracic limb series, which might bear the gonopores. (A) Lepidocaris rhyniensis, Devonian (from
Scourfield 1926). (B) Rehbachiella kinnekulensis, Upper Cambrian (from Walossek 1993). (C–E) various
Cambrian waptiids. (C) Chuandianella ovata (from Chen and Zhou 1997). (D) Pauloterminus spinodorsalis
(from Taylor 2002). (E) Waptia fieldensis (from Briggs et al. 1994). (F) Castracollis wilsonae (from Fayers
and Trewin 2003).
The lipostracan Lepidocaris rhyniensis, a unique Devonian fossil (Fig. 1.8A), is preserved in
great detail within nodules of chert. The thoracic limbs are both multiramous (thoracopods
1 and 2) and biramous (thoracopods 3–5). However, the presence of fully developed maxillae
(Schram 1986), rather than the vestigial form characteristic of true branchiopods, indicates
possibly only a sister-group relationship with crown Branchiopoda.
Rehbachiella (Fig. 1.8B) has figured prominently in discussions of branchiopod origins

(Walossek 1993). However, Schram and Koenemann (2001) took exception with this and con-
cluded that Rehbachiella, while possibly a stem form, was not a branchiopod sensu stricto since
not only do they possess biramous thoracopods, but also these limbs arise from biramous anla-
gen and not the multilobed ridge of true branchiopods. Hence, I believe Rehbachiella, at best, is
a stem form.
Another fossil group from the Cambrian could be relevant to understanding stem evolu-
tion of branchiopods, the waptiids (Fig. 1.8C–E). The genus Waptia from the Burgess Shale of
Canada is probably the most famous. However, several genera are known (Briggs et al. 1994,
Chen, and Zhou 1997, Taylor 2002) and all appear to have a subdivided thorax with apparently
four anterior telopodous limbs and six posterior foliaceous limbs. The gonopores have yet to be
identified for waptiids, but I would venture a guess that they probably occurred on the eleventh
trunk segment.
Although the recent large-scale molecular analyses of Giribet et al. (2005) and Wheeler et al.
(2004) typically find Hexapoda as a sister group to all crustaceomorphs, there is an alterna-
tive hypothesis. Schram and Koenemann (2004b), VanHook and Patel (2008), Lartillot and
Philippe (2008), and Dell’Ampio et al. (2009) obtained trees with insects and Branchiopoda
as sister groups. These results were based on developmental gene expression patterns and mol-
ecule sequences, and these trees serve to propose alternative hypotheses concerning branchio-
pod relationships.
Finally, there are fossils such as Castracollis wilsonae (Fig. 1.8F) that exhibit body plans
that are complex but nevertheless place them within branchiopods, in this case 11 large, folia-
ceous, cormlike limbs on the anterior thorax followed by another series of similar limbs but
much reduced in size (Fayers and Trewin 2003). Castracollis might or might not have had a
carapace.
Eucrustacea
What remains of the crustaceomorph taxa after clades of short-bodied and branchiopo-
dan types are isolated is a confederation of diverse forms: Cephalocarida, Malacostraca,
Remipedia, and Maxillopoda. When viewed as a whole, these taxa are divergent in terms of
both habitus and habitat; nevertheless, all these groups bear gonopores on the sixth through
eighth thoracic somites. There are a couple of interesting exceptions to this rule, which I note
below.
Cephalocarida
This group of hermaphrodites is small both in size and in species numbers. It has a thorax of
eight segments and a limbless abdomen of 12 segments (Fig. 1.9A). The form of the maxillae is
very similar to that seen for the thoracopods. The gonopores are located on the sixth thoracom-
ere. Nothing is known of Hox gene expression in cephalocarids.
The body plan of cephalocarids might exhibit the results of the same sorts of constraints
we saw above with mystacocarids. In this case, the elongate, limbless abdomen with extended
terminal caudal rami at best probably functions like the tail on a kite: a stabilizer to mini-
mize drag and the effect of turbulence as the animals swim. The long series of thoracic limbs
developed as swimming paddles provide more locomotory abilities than that seen in the tiny
thoracopods of mystacocarids, but nonetheless, competition from larger and more mobile
forms probably forced the cephalocarids to retreat to f locculent bottom sediments in order
to make a living.
B
A
F D
Fig. 1.9.
The four major groups among the core bauplan of Crustacea, with gonopore-bearing segments indicated
by arrows. (A) A cephalocarid, Hutchinsoniella macracantha, a hermaphrodite with pores on the sixth tho-
racomere (modified from Schram 1986). (B) A hoplocarid Malacostraca, a male Squilla mantis. The male
pore (long arrow) would be on the eighth thoracomere; the female pore (short arrow) would be on the
sixth thoracomere (modified from Calman 1909). (C and D) Two types of eumalacostracan Malacostraca:
with (C) and without (D) a carapace. (C) A euphausiid, Meganyctiphanes norvegica . The male pore is on
the eighth thoracomere (long arrow); the female pore, on sixth thoracomere (sort arrow) (modified from
Mauchline and Fisher 1969). (D) The syncarid Anaspides tasmaniae. The male pore is on the eighth tho-
racomere (long arrow); the female pore, on sixth thoracomere (short arrow) (modified from Schminke
1978). (E and F) Two types of remipede, hermaphrodites with the male pore on the eighth thoracomere
(long arrow) and the female pore on the fifteenth thoracomere (short arrow). (E) Medium-length body,
Speleonectes gironensis (modified from Yager 1994). (F) Short-length body, Micropacter yagerae (modified
from Emerson and Schram 1991). (G) A typical maxillopodan, Calanus finmarchicus. Male and female
pores open on seventh thoracomere (modified from Calman 1909).
Malacostraca
This most variable of crustacean groups nevertheless has a fundamentally uniform structural
plan. The trunk is divided into an anterior thorax of eight segments and a posterior pleon of six
or seven segments, sometimes fewer. All trunk somites generally bear appendages, but note-
worthy variations can occur, such as one or more thoracopods serving as maxillipeds or pos-
terior thoracopods and/or pleopods being greatly reduced or absent. Hox genes are expressed
throughout the body (Abzhanov and Kaufman 2004, Schram and Koenemann 2004a) with Ubx
characteristic of the thorax and abd-A of the pleon (Fig. 1.4). The female gonopores occur in
association with the sixth thoracic segment, while the male pores are on the eighth.
The malacostracans are typically said to contain three groups: the small nectobenthic lepto-
stracans (not illustrated), the obligate carnivorous hoplocaridans (Fig. 1.9B), and the extremely
diverse caridoid eumalacostracans that have forms both with a carapace (Fig. 1.9C) and with-
out (Fig. 1.9D). The diversity of this group is examined in greater detail in other chapters in this
volume.
We might say that the great versatility imparted by the malacostracan body plan is respon-
sible for its success. The long series of limbs, extending through both the thorax and pleon,
allows a great degree of variation and specialization that undoubtedly has allowed the group
to radiate to the extent it has, with great numbers of species and remarkable variations in
structure.
Maxillopoda
With the problematic Mystacocarida and Branchiura removed from the maxillopodans, where
textbooks often place them, there remains a core set of taxa that appear to conform to a single
body plan. The old formula of 5–6-5 or the newer viewpoint of 5–7-4—five cephalic, seven tho-
racic, and four abdominal somites (see Newman 1987)—has great consistency throughout the
group. The old interpretation was of a thorax with six limb-bearing segments and an abdomen
of five segments always lacking limbs. An alternative interpretation of the gonopore-bearing
segment as actually part of the thorax (Newman 1987) leaves only four abdominal somites; this
interpretation makes more sense not only in terms of what we can see in other groups, for exam-
ple, the free gonopore-bearing segment of the anostracans that occurs just posterior to a set of
trunk limbs mentioned above, but also in terms of what limited information we have concerning
Hox gene expression, with Ubx and Abd-A expression in the thorax and abd-B in the genital seg-
ment (Averof and Patel 1997).
Copepoda (Fig. 1.9G) most clearly present the pattern of 5–7-4. The gonopores of both
sexes occur on the seventh thoracomere. Thecostraca conform to the basic maxillopodan pat-
tern with some variations. Ascothoracica exhibit 5–7-4. Facetotecta appear to manifest 5–7-3,
based on the anatomy of the Y-cypris. Cirripedia exhibit 5–7-0, considering the cypris larva as
a stand-in model for the highly derived adults. While male gonopores in the cirripedes appear
on the seventh thoracic segment, the female pore has shifted forward onto the first thoracic seg-
ment. Furthermore, the cirripedes lack an abdomen and coincidently also lack any expression of
Abd-A (Mouchel-Vielh et al. 1998).
The parasitic Tantulocarida present problems since these microscopic forms have an
extremely aberrant life cycle. However, recent advances in elucidating that life cycle (Huys
et al. 1993) allow us to conclude that the tantulocarids express a 5–7-2 pattern, with the
male gonopore appearing on the seventh thoracic somite and the single median female pore
occurring on the first. This latter feature clearly unites tantulocarids and thecostracans as
sister groups.
The constraints exerted by a limbless abdomen on lifestyle may explain much of what we
see in maxillopodan evolution. The maxillopodans certainly thrive under unusual conditions.
Parasitism is widespread in the group, especially among thecostracans, and those thecostracans
that are not parasites have lost the abdomen altogether and settled (literally) into the completely
sedentary, highly aberrant body plan seen in the barnacles. Only the copepods possess the kind
of biodiversity and habitat variability we associate with “successful” groups. Even so, the small
sizes of copepods could be related to the limits engendered by an abdomen lacking limbs.
Ostracoda
These animals remain the most vexing of arthropods to place phylogenetically and, if molecular
sequences are to be believed, may not be a monophyletic group. Their extreme reduction of body
plan (oligomery), complete enclosure within a calcareous shell, and specializations directed at
life carried on at a microscale have hindered attempts to link them to other crustaceomorphs.
There are contentious debates about homologies within Ostracoda (Horne et al. 2005), and
ostracodes do not appear to share obvious apomorphies with other crustaceomorphs. Most
textbooks and reference books consign ostracodes to the maxillopodans (see Schram 1986), but
that is more of a default placement.
K. Martens (personal communication, 2004) and R.A. Jenner (personal communication,
2009) expressed an informal view of at least some researchers that Ostracoda might not be a
monophyletic group. This possibility obtains some support from molecular data that some-
times finds Podocopa and Myodocopa in different parts of cladograms (see Spears and Abele
1997, Regier et al. 2008, 2010, Koenemann et al. 2010). However, most of these analyses have a
very limited taxon sample with sequences from only a handful of ostracode species.
There is much variation in form in ostracode limbs, but there is a consensus at least that both
the myodocopes and the podocopes are themselves monophyletic (Horne et al. 2005). However,
debates about the number of somites in each group are not settled. At first glance, one perceives
that only very few thoracic segments bear limbs, but Schulz (1976) presented some evidence that
indicates Cytherella pori, a podocopan, might have 11 trunk somites (a 5–7-4 pattern) and that
the penis appears to be associated with the sixth or seventh of these segments (see Schram 1986,
their fig. 33–1C). Tsukagoshi and Parker (2000) confirmed this in other species of podocopans.
No similar information is available yet for Myodocopa.
From this, it might appear that podocopan ostracodes are possibly maxillopodans. Some
authorities classified Ostracoda as a subclass of Maxillopoda (Schram 1986), but others main-
tain them as an independent class (Martin and Davis 2001). Most recently, Koenemann et al.
(2010) and Regier et al. (2010), on the basis of molecular sequences, obtained both podocopan
and myodocopan ostracodes as a sister group to a clade of mystacocarids, branchiurans, and
pentastomids. This arrangement would then unite all the short-bodied “oligostracans” into a
single clade near the base of the crustaceomorph tree (Fig. 1.6).
However, there existed Paleozoic, especially Cambrian, taxa that may have some bearing on
eventually determining ostracode affinities. Several such groups are under active study, such
as the bradoriids, Phosphatocopida (Maas et al. 2003), and perhaps even the thylacocephalans.
These groups will eventually have to be integrated into any classification of the crustaceo-
morphs, and undoubtedly they will prove very interesting in this regard.
Remipedia
This most recently discovered group of crustaceomorphs is noteworthy for several rea-
sons. The trunk is not differentiated into a thorax and abdomen/pleon. If we consider the
maxilliped-bearing segment as a modified trunk somite (even though it is completely merged

into the cephalon), then the female gonopore occurs on the eighth postmaxillary segment, and
the male gonopore, on the fifteenth. However, as noted above (Koenemann et al. 2007, 2009),
the distinctive maxillipeds, virtually identical in general form to the maxillae, display no devel-
opmental evidence that this limb is modified from a thoracopod format. In addition, the number
of trunk segments is not fixed, either within or between species (Koenemann et al. 2006), with
many long-bodied forms recognized (Fig. 1.9E)—although there appears to be at least a lower
limit of 16 trunk segments in the adults (Fig. 1.9F). The significance of all this variability remains
to be explored.
The remipede body plan ensured that these animals are excellent swimmers, on a par with
anything seen among the malacostracans. Even so, their habitat restrictions are quite profound;
they prefer anchialine cave habitats in low-oxygen conditions.
CLASSIF ICATION
The above review indicates there have to be changes in our concepts of crustaceomorph
classification, but this is not the place to present any new or radical higher taxonomy. In princi-
ple, we want our taxonomies to reflect phylogeny, but that is not always possible. There is much
conflicting evidence from molecular analyses, which along with morphological data often suf-
fers from limited taxon sampling, and the latter often ignores or minimizes input from fossils.
We still need to more effectively integrate data from gross morphology, molecular sequencing,
and paleontology into a coherent whole. Nevertheless, we should extend some effort to rec-
ognize the monophyletic groups about which we are certain (Fig. 1.10); there are patterns that
should be acknowledged.
To these ends, we can make good use of the concept of the plesion, a particular taxon that
does not fit well into another category and that eventually might be assigned to its own higher
category. I believe that, in this instance, we should begin to think of the infraphyla below
as monophyletic groups on a par with other well-established arthropod monophyla such as
Hexapoda, Chelicerata, Trilobita, and Pycnogonida. What fossils and where they will fall
within or between these monophyletic groups will be explored elsewhere. The scheme is not
complete in terms of all possible fossil plesions but does include most of those mentioned in
the text above (Table 1.4).
WHAT MIGHT THE CRUSTACEOMORPH ANCESTOR HAVE LOOKED LIKE?
At one time, there was a fair consensus as to what the ancestor of Crustacea might have looked
like. Hessler and Newman (1975) devised an ancestor with a long, homonomously segmented
body, each segment bearing a set of limbs not unlike a cephalocarid, for which Newman preferred
a form with a carapace, and Hessler one without (Fig. 1.11A). Cisne (1982) believed that crusta-
ceans arose from a trilobite-like ancestor. Schram (1982) concurred with Hessler and Newman
(1975), although he would have preferred a somewhat more foliaceous limb, intermediate between
cephalocarids and branchiopods (Fig. 1.11B). However, Schram’s 1982 paper had been written in
1978 (delayed due to a delay in the publication of the book in which it appeared), and in the inter-
vening years the remipedes had come to light. By 1983, Schram had altered his views as to the
form of an ancestor, which, while still in possession of a long homonomous body, was viewed
as equipped with biramous, paddlelike limbs (Schram 1983). Schram positioned this biramous
theory as an alternative hypothesis to the mixopodial theory of Hessler and Newman, and this
then postulated a remipede-like alternative ancestor as opposed to a cephalocarid-like forebear.
4
A
Mystacocarida
6-8
B
Maxillopoda
Malacostraca
Remipedia
Cephalocarida
12
C
Branchiopoda
Fig. 1.10.
Major crustaceomorph body plans based on gonopore position. (A) Mystacocarida, an “oligostracan.” (B)
“Eucrustaceans.” (C) Branchiopoda. From Schram and Koenemann (2004a).
The debate outlined above was based on morphology. Some information derived from
molecular sequences now suggests that hexapods could factor into this mix. One fossil that
might have facilitated a visual understanding of how this transition might have occurred is
Wingertschellicus backesi Briggs and Bartels, 2001 (= Devonohexapodus bocksbergensis Haas
et al., 2003). A recent reexamination of all available fossils of this species from the famous
Devonian Hunsr ück Shale (K ü hl and Rust 2009) synonymized the two names, but the origi-
nal reconstruction of Haas et al. (2003) presented a strange chimera—it appears to have a
dragonf ly anterior end and a very long myriapodous posterior end (Fig. 1.11C). Although the
interpretation of Haas et al. (2003) of D. bocksbergensis offered a head (of possibly four segments)
and a short three-segment thorax followed by a long abdomen, the new interpretation presents
a six- or seven-segment head, with the posteriormost three pairs of cephalic limbs as long, pos-
sibly prehensile appendages and followed by a long trunk with biramous limbs. Neither Briggs
and Bartels (2001) nor Kü hl and Rust (2009) offer a reconstruction of W. backesi, but the latter
believe that this species is neither a stem hexapod nor within crown group Malacostraca. Of
these I am not so sure, having once had the opportunity to examine D. bocksbergensis courtesy
of Dieter Walossek. Even though what this Devonian species might represent remains uncer-
tain, nevertheless, it does demonstrate that there is an abundance of long-bodied forms in the
Paleozoic that may have significance for understanding the early evolution and possible origins
of surviving groups of arthropods.
Another source of information that is relevant for understanding crustacean ancestry is
derived from the study of the Cambrian Orsten microfossils (a few of which were mentioned
Table 1.4. A classification of tetraconate arthropods with inclusion of fossil plesions.
Subphylum: Tetraconata (= Crustaceomorpha = Pancrustacea)

Infraphylum: Hexapoda
Infraphylum: unnamed (short-bodied crustaceomorphs—“Oligostraca”)
Class Branchiura
Order: Arguloida
Order: Pentastomida
Class: Mystacocarida
Plesion: Skaracarida
Plesion: Ostracoda (one possible position; includes Myodocopa and Podocopa)
Infraphylum: Branchiopoda
Class: Phyllopoda (= Calmanostraca)
Order: Laevicaudata
Order: Notostraca
Order: Spinicaudata
Order: Cyclestherida
Order: Cladocera
Class: Sarsostraca
Order: Anostraca
Plesion: Lipostraca (= Lepidocaris)
Plesion: Rehbachiellida (= Rehbachiella)
Plesion: Waptiidae
Infraphylum: Crustacea
Class: Cephalocarida
Class: Maxillopoda
Subclass: Copepoda
Subclass: Thecostraca
Infraclass: Ascothoracica
Infraclass: Cirripedia
Infraclass: Facetotecta
Infraclass: Tantulocarida
Plesion: Ostracoda (one possible position; includes Myodocopa and Podocopa)
Class: Malacostraca
Subclass: Eumalacostraca
Subclass: Hoplocarida
Subclass: Phyllocarida
Class: Remipedia
Cephalocarida and Remipedia might constitute a single class, Xenocarida, based on molecular evidence. Ostracoda could
occupy two possible positions: among oligostracans, based on molecular data, or within maxillopodans, based on some
morphological data. Hoplocarida and Eumalacostraca (sensu stricto) could be arranged as a single subclass Eumalacostraca
(sensu lato) with infraclasses Caridoida and Hoplocarida.
above), and these have raised the possibility of alternative hypotheses. Incompletely under-
stood in the 1980s, the depth of knowledge about these animals is now astounding, extend-
ing as it does to even developmental stages for many of these species (see chapter 2). The full
impact of these studies remains to be assessed within the larger framework of the anatomy of
modern forms, molecular sequences, and gene expressions, but much of this work suggests a
A B
A'
Fig. 1.11.
Crustaceomorph ancestors (see text for details). (A and A′) Without and with a carapace, according to
Hessler and Newman (1975). (B) According to Schram (1982). (C) Devonohexapodus bocksbergensis (from
Haas et al. 2003).
possible alternative hypothesis: a short-bodied ancestor rather than a long-bodied one. This
merits consideration (Schram and Koenemann 2004a), but it is not possible or appropriate to
examine here.
CONCLUSIONS
It would appear that we are little closer to understanding the origin of crustaceomorphs than
we were 30 years ago. While the larger assemblage of the crustaceomorphs (or pancrustaceans,
or tetraconatans, if you prefer) might be in some way monophyletic, just how it can (or even if
it can) be diagnosed with a single set of apomorphies is not clear at this point. There are, how-
ever, good monophyletic groups within this vast array that can be clearly defined. Furthermore,
these body plans appear to be constrained regarding biodiversity, functional morphology, and
habitats they can occupy. In addition, we have a growing array of fascinating fossil taxa scattered
within and between these monophyla, but how these are related to the monophyletic groups for
which they may serve as stem forms remains to be determined.
But take heart! It is a time not to mourn the demise of the monophylum Crustacea but to
embrace what will be a new world order and a better understanding of this whole branch of the
crustaceomorph arthropods.
ACKNOWLEDGMENTS
I am grateful for the invitation from Profs. Martin Thiel and Les Watling to write this chap-
ter. I also thank Dr. Ronald Jenner (Natural History Museum, London) for reading a draft and
offering some valuable comments and suggestions. Prof. Stefan Koenemann (Hannover) was
involved in producing some of the earlier papers from which parts of this chapter developed.
Any and all faults, however, are my own.
REFERENCES
Abele, L.G., W. Kim, and B.E. Felgenhauer. 1989. Molecular evidence for the inclusion of the phylum
Pentastomida in the Crustacea. Molecular Biology and Evolution 6:685–691.
Abzhanov, A., and T.C. Kaufman. 2004. Hox genes and tagmatization of the higher Crustacea
(Malacostraca). Crustacean Issues 15:43–74.
Averof, M., and N.H. Patel . 1997. Crustacean appendage evolution associated with changes in Hox gene
expression. Nature 388:682–686.
Birge, E.A. 1918. The water fleas (Cladocera). Pages 676–740 in H.B. Ward and G.C. Whipple, editors.
Freshwater biology. Wiley, New York.
Bouchet, P. 2006. The magnitude of marine biodiversity. Pages 33–62 in C.M. Duarte, editor. The explo-
ration of marine biodiversity: Scientific and technical challenges. Fundación BBVA, Bilbao, Spain.
Boxshall, G.A. 1983. Three new genera of misophrioid copepods, with special reference to
Benthomisophria palliata . Philosophical Transactions of the Royal Society of London Series B
297:125–181.
Boyan, G.S., J.L.D. Williams, S. Posser, and P. Bäunig. 2002. Morphological and molecular data argue
for the labrum being non-apical, articulated, and the appendage of the intercalary segment in the
locust. Arthropod Structure and Development 31:65–76.
Briggs, D.E.G., and C. Bartels . 2001. New arthropods from the Lower Devonian Hunsr ück Slate (Lower
Emsian, Rhennish Massif, Western Germany). Palaeontology 44:275–303.
Briggs, D.E.G., D.H. Erwin, and F.J. Collier. 1994 . The fossils of the Burgess Shale. Smithsonian
Institution Press, Washington, DC.
Brusca, R.C., and G.J. Brusca . 1990. Invertebrates. Sinauer, Sunderland, MA.
Brusca, R.C., and G.J. Brusca . 2003. Invertebrates, 2nd ed. Sinauer, Sunderland, MA.
Calman, W.T. 1909. Crustacea. Part VII, 3rd fasc., in E.R. Lankester, editor. A treatise on zoology, Vol. 7.
Adam and Charles Black, London.
Chen, J.-Y., and G.-Q. Zhou. 1997. Biology of the Chengjiang fauna. Bulletin of the National Museum of
Natural Sciences (Taiwan) 10:11–105.
Cisne, J.L. 1982. Origin of Crustacea. Pages 65–92 in L.G. Abele, editor. Biology of the Crustacea, Vol. 1.
Academic Press, New York .
Cohen, S.M. 1990. Specifications of limb development in the Drosophila embryo by positional cues from
segmentation genes. Nature 343:173–177.
Dell’Ampio, E., N.U. Szucsich, A. Carapelli, F. Frati, G. Steiner, A. Steinacher, and G. Pass . 2009. Testing
for misleading effects in the phylogenetic reconstruction of ancient lineages of hexapods: Influence
of character dependence and character choice in analyses of 28S rRNA sequences. Zoologica
Scripta 38:155–170.
Emerson, M.J., and F.R. Schram . 1991. Remipedia. Part 2. Proceedings of the San Diego Society of
Natural History 7:1–52.
Fayers, S.R., and N.H. Trewin. 2003. A new crustacean from the Early Devonian Rhynie chert,
Aberdeenshire, Scotland. Transactions of the Royal Society of Edinburgh, Earth and
Environmental Science 93:355–382.
Giribet, G., S. Richter, G.D. Edgecombe, and W. Wheeler. 2005 . The position of crustaceans within
Arthropoda—evidence from nine molecular loci and morphology. Crustacean Issues 16:307–352.
Groombridge, B., and M.D. Jenkins. 2000. Global diversity: Earth’s living resources in the 21st century.
World Conservation Press, Cambridge.
Grygier, M.J. 1981. Gorgonolaureus muzikae sp. nov. parasitic on a Hawaiian gorgonian, with special refer-
ence to its protandric hermaphroditism. Journal of Natural History 15:1019–1045.
Haas, F., D. Waloszek , and R. Hartenberger. 2003. Devonohexapodus bocksbergensis, a new marine
hexapod from the Lower Devonian Hunsr ück Slates, and the origin of Atelocerata and Hexapoda.
Organic Diversity and Evolution 3:39–54.
Hessler, R.R. 1969. A new species of Mystacocarida from Maine. Vie et Milieu 22:105–116.
Hessler, R.R., and W.A. Newman . 1975 . A trilobitomorph origin for the Crustacea. Fossils and Strata
4:437–459.
Horne, D.J., I. Schön, R.J. Smith, and K. Martens . 2005 . What are the Ostracoda? A cladistic analysis
of the extant superfamilies of the subclasses Myodocopa and Podocopa (Crustacea: Ostracoda).
Crustacean Issues 16:249–273.
Huys, R., G.A. Boxshall, and R.J. Lincoln. 1993. The tantulocaridan life cycle: The circle closed? Journal
of Crustacean Biology 13:432–442.
Koenemann, S., R.A. Jenner, M. Hoenemann, T. Stemme, and B.M. von Reumont. 2010. Arthropod phy-
logeny revisited, with a focus on crustacean relationships. Arthropod Structure and Development
39:88–110.
Koenemann, S., J. Olesen, F. Alwes, T.M. Iliffe, M. Hoenemann, P. Ungerer, C. Wolff, and G. Schultz.
2009. The post-embryonic development of Remipedia (Crustacea)—additional results and new
insights. Development Genes and Evolution 219:119–129.
Koenemann, S., F.R. Schram, A. Bloechl, T.M. Iliffe, M. Hoenemann, and C. Held . 2007.
Post-embryonic development of remipede crustaceans. Evolution and Development 9:117–121.
Koenemann, S., F.R. Schram, and T.M. Iliffe. 2006. Trunk segmentation patterns in Remipedia.
Crustaceana 79:607–631.
Kü hl, G., and J. Rust . 2009. Devonohexapodis bocksbergensis is a synonym of Wingertshellicus backesi
(Euarthropoda)—no evidence for marine hexapods in the Devonian Hunsr ück Sea. Organisms
Diversity and Evolution 9:215–231.
Lang , K. 1953. Apseudes hermaphroditicus, a hermaphroditic tanaid from Antarctica. Arkiv för Zoologie
(2) 9:341–350.
Lartillot, N., and H. Philippe 2008. Improvement of molecular phylogenetic inference and the phylogeny
of Bilateria. Philosophical Transactions of the Royal Society of London Series B 363:1463–1472.
Lilljeborg , W. 1901. Caldocera Suiciae. Nova Acta Regiae Societatis Scientarium Upsaliensus. Uppsala
3:1–701.
Linder, F. 1945 . Affinities within the Branchiopoda, with some notes on some dubious fossils. Arkiv för
Zoologie 37:1–28.
Lynch, J.E. 1964 . Packa’s and Pearse’s species of Branchinecta: Analysis of nomenclatural involvement.
American Midland Naturalist 71:466–488.
Maas, A., D. Waloszek , and K. Mü ller. 2003. Morphology, ontogeny, and phylogeny of the
Phosphatocopina (Crustacea) from the Upper Cambrian “Orsten” of Sweden. Fossils and Strata
49:1–238.
Martin, M.F. 1932. On the morphology and classification of Argulus. Proceedings of the Zoological
Society of London 1932:771–806.
Martin, J.W., and G.E. Davis. 2001. An updated classification of the recent Crustacea. Science Series,
Natural History Museum of Los Angeles County 39:1–124.
Martin, J.W., and G.E. Davis. 2006. Historical trends in crustacean systematics. Crustaceana
79:1347–1368.
Martin, J.W., B.E. Felgenhauer, and L.G. Abele. 1986. Redescription of the clam shrimp Lynceus gracili-
cornis (Packard) (Branchiopoda, Conchostraca, Lynceidae) from Florida, with notes on its biology.
Zoologica Scripta 15:221–232.
Mauchline, J., and L.R. Fisher. 1969. The Biology of Euphausiids. Advances in Marine Biology 7:1–454.
May, R.M. 1988. How many species are there on Earth? Science 241:1441–1449.
Meglitsch, P.A., and F.R. Schram. 1991. Invertebrate zoology, 3rd ed. Oxford University Press, New York .
Minelli, A. 1993. Biological systematics. Chapman and Hall, London .
Minelli, A., G. Fusco, and S. Sartori. 1991. Self-similarity in biological classifications. BioSystems
26:89–97.
Mouchel-Vielh, E., C. Rigolot, J.-M. Gibert, and J.S. Deutsch . 1998. Molecules and the body plan: The
Hox genes in cirripedes (Crustacea). Molecular Phylogenetics and Evolution 9:382–389.
Mü ller, K.J., and D. Walossek. 1985 . Skaracarida, a new order of Crustacea from the Upper Cambrian of
V ä stergotland, Sweden. Fossils and Strata 17:1–65.
Mü ller, K.J., and D. Walossek. 1986. Arthropod larvae from the Upper Cambrian of Sweden. Transactions
of the Royal Society of Edinburgh, Earth and Environmental Science 77:157–179.
Mü ller, K.J., and D. Walossek. 1988. External morphology and larval development of the Upper Cambrian
maxillopod Bredocaris admirabilis. Fossils and Strata 23:170.
Newman, W.A. 1987. Evolution of cirripedes and their major groups. Crustacean Issues 5:3–42.
Olesen, J. 1998. A phylogenetic analysis of the Conchostraca and Cladocera (Crustacea, Branchiopoda,
Diplostraca). Zoological Journal of the Linnean Society 122:491–536.
Olesen, J. 1999. Larval and post-larval development of the branchiopod clam shrimp Cyclestheria hislopi
(Crustacea, Branchiopoda, Conchostraca, Spinicaudata). Acta Zoologica 80:163–184.
Panganiban, G., A. Sebring , L. Nagy, and S. Caroll . 1995 . The development of crustacean limbs and the
evolution of arthropods. Science 270:1363–1366.
Regier, J.C., J.W. Shultz , A.R.D. Ganley, A. Hussey, D. Shi, B. Ball, A. Zwick, J.E. Stajich, M.P.
Cummings, J.W. Martin, and C.W. Cunningham . 2008. Resolving arthropod phylogeny: Exploring
phylogenetic signal within 41 kb of protein-coding nuclear gene sequence. Systematic Biology
57:920–938.
Regier, J.C., J.W. Shultz , A. Zwick, A. Hussey, B. Ball, R. Wetzer, J.W. Martin, and C.W. Cunningham.
2010. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding
sequences. Nature 463:1079–1083.
Richter, S., J. Olesen, and W.C. Wheeler. 2007. Phylogeny of Branchiopoda (Crustacea) based on a
combined analysis of morphological data and six molecular loci. Cladistic 23:1–36.
Ruppert, E.E., and R.D. Barnes. 1994 . Invertebrate zoology, 6th ed. Saunders College Publications, Fort
Worth, TX.
Sars, G.O. 1887. On Cyclestheria hislopi (Baird), a new generic type of bivalved phyllopod raised from
dried Australian mud. Christiania Videnskabernes Selskab Fordhandlinger 1:1–65.
Sars, G.O. 1896. Phyllocarida and Phyllopoda. Fauna Norvegiae, Vol 1. Stock, Christiania, Aschehoug.
Scholtz , G. 2000. Evolution of the nauplius stage in malacostracan crustaceans. Journal of Zoological
Systematics and Evolution Research 38:175–187.
Schminke, H.K. 1978. Die phylogenetische Stellung der Stygocarididae—unter besonderer
Berucksichtigung morphologischer Ahnlichkeiten mit Larvenformen der Eucarida. Zeitschrift f ü r
zoologische Systematik und Evolutionsfoschung 16:225–239
Schram, F.R. 1979. Crustacea. Pages 238–244 in R.W. Fairbridge and D. Jablonski, editors. The encyclo-
pedia of paleontology. Dowden, Hutchinson, and Ross, Stroudsberg, PA .
Schram, F.R. 1982. The fossil record and evolution of Crustacea. Pages 93–147 in L.G. Abele, editor. The
biology of Crustacea, Vol. 1. Academic Press, New York .
Schram, F.R. 1983. Remipedia and crustacean phylogeny. Crustacean Issues 1:23–28.
Schram, F.R. 1986. Crustacea . Oxford University Press, New York .
Schram, F.R. 2003. Our evolving understanding of biodiversity through history and its impact on the recog-
nition of higher taxa in Metazoa. Pages 359–368 in A. Legakis, editor. The new panorama of animal evo-
lution, Proceedings of the 18th International Congress of Zoology. Pensoft Publishers, Sofia, Bulgaria.
Schram, F.R., and S. Koenemann . 2001. Developmental genetics and arthropod evolution: Part I, on legs.
Evolution and Development 3:343–354
Schram, F.R., and S. Koenemann. 2004a . Developmental genetics and arthropod evolution: Part II, on
body regions of crustaceans. Crustacean Issues 15:75–92.
Schram, F.R., and S. Koenemann. 2004b. Are the crustaceans monophyletic? Pages 319–329 in J. Cracraft
and M.J. Donaghue, editors. Assembling the tree of life. Oxford University Press, New York .
Schram, F.R., J. Yager, and M.J. Emerson. 1986. Remipedia. Part 1. Systematics. San Diego Society of
Natural History Memoires 15:1–60.
Schulz , K. 1976. Das Chitinskelett der Podocopida (Ostracoda, Crustacea) und die Frage der Metamerie
dieser Gruppe. PhD dissertation, University of Hamburg.
Scourfield, D.J. 1926. On a new type of crustacean from the Old Red Sandstone—Lepidocaris rhyniensis.
Philosophical Transactions of the Royal Society of London Series B 214:153–187.
Spears, T., and L.G. Abele. 1997. Crustacean phylogeny inferred from 18S rDNA. Pages 169–186 in R.A.
Fortey and R.A. Thomas, editors. Arthropod relationships. Chapman and Hall, London .
Taylor, R.S. 2002. A new bivalved arthropod from the early Cambrian Sirius Passet fauna, North
Greenland. Palaeontology 45:97–123.
Tsukagoshi, A., and A.R. Parker. 2000. Trunk segmentation in some podocopine lineages in Ostracoda.
Hydrobiologia 419:15–30.
VanHook , A.M., and N.H. Patel. 2008. Crustaceans. Current Biology 18:R547–R550.
Walossek , D. 1993. The Upper Cambrian Rehbachiella and the phylogeny of Branchiopoda and Crustacea.
Fossils and Strata 32:1–202.
Walossek , D., and K. Mü ller. 1990. Stem-lineage crustaceans from the Upper Cambrian of Sweden and
their bearing upon the position of Agnostus. Lethaia 23:409–427.
Walossek , D., and K.J. Mü ller. 1994 . Petastomid parasites from the Lower Palaeozoic of Sweden.
Transactions of the Royal Society of Edinburgh, Earth and Environmental Science 85:1–37.
Walossek , D., J.E. Repetski, and K.J. Mü ller. 1994 . An exceptionally preserved parasitic arthro-
pod, Heymonsicambria taylori n. sp. (Arthropoda incertae sedis: Pentastomida), from
Cambrian-Ordovician boundary beds of Newfoundland, Canada. Canadian Journal of Earth
Sciences 31:1664–1671.
Wheeler, W., G. Giribet, and G.D. Edgecombe. 2004 . Arthropod systematics: the comparative study
of genomic, anatomical, and paleontological information. Pages 281–295 in J. Cracraft and M.
Donoghue, editors. Assembling the tree of life. Oxford University Press, New York .
Williams, T.A. 1998. Distalless expression in crustaceans and the patterning of branched limbs.
Development Genes and Evolution 207:427–434.
Williams, T.A., and G.B. Mü ller. 1996. Limb development in a primitive crustacean, Triops longicauda-
tus: Subdivision of the early limb bud gives rise to multibranched limbs. Development Genes and
Evolution 206:161–168.
Willis, J.C., and G.U. Yule. 1922. Some statistics of evolution and geographical distribution in plants and
animals, and their significance. Nature 109:177–179.
Wingstrand, K.G. 1972. Comparative spermatology of a pentastomid, Raiallietiella hemidactyli, and
a branchiuran crustacean, Argulus foliaceous, with a discussion of pentastomid relationships.
Biologiske Skrifter af det Kongelige Danske Videnskabernes Selskab 19(4):1–72.
Yager, J. 1994 . Speleonectes gironensis, new species (Remipedia: Speleonectidae), from anchialine caves in
Cuba, with remarks on biogeography and ecology. Journal of Crustacean Biology 14:752–762.
2
EVOLUTION OF CRUSTACEAN APPENDAGES
Joachim T. Haug, Andreas Maas, Carolin Haug,

and Dieter Waloszek
Abstract
The evolutionary history of the postantennular appendages of Crustacea is reviewed, includ-
ing information on limb development early in the evolutionary lineage of this taxon. This is
particularly well demonstrated in the exceptional three-dimensionally preserved Cambrian
fossils of the “Orsten” type (~500 million years old). Crustaceans started with serially similar
limbs obtained from euarthropod ancestors, the “euarthropodium” comprising a biramous
limb with a joint membrane and a prominent rigid stem portion, the basipod , carrying two
rami, called endopod and exopod , of different phylogenetic origin. However, as a key inno-
vation, they used the anterior three appendages (the “still” food-gathering antennulae and
two more limbs) to collaborate as a set for feeding and swimming. For this collaboration,
the two postantennular limbs had special outer lateral rami, exopods with fine annulation,
and swimming setae inwardly positioned; a setiferous “proximal endite” developed medio-
proximal to the basipod. Further changes of the appendages and the effects on the feeding and
locomotory system are followed along the evolutionary lineage of the crustaceans into the
crown group, Eucrustacea. Acknowledging these changes is crucial to understand the high
degree of variation of modern crustacean limb morphology and to overcome difficulties in
recognizing their common features in terms of homology and relationships. The high plas-
ticity of crustacean limb morphology is, in fact, not surprising since the major branchings
along the crustacean lineage had already occurred far back in the Cambrian. It also means
that there is no general “crustaceopodium”; instead, each limb must be viewed individually
in terms of its history and its fate. Moreover, restructuring affected virtually all limb parts,
including the possibility of formation of epipod(ite)s/gills (not mentioned in detail herein)
and development of numerous types of surface outgrowths (spines, setae, and subordinate
structures; discussed elsewhere in this volume) for various duties. Also, the rami underwent
34
Evolution of Crustacean Appendages 35
significant changes regarding functional adaptations. One example of this change is that the
rami became paddle shaped and/or symmetrical (of same morphology) as an adaptation to
swimming, and sometimes multiannulated or even lost. Other strategies that evolved subse-
quently in eucrustacean ingroups include the arrangement of limbs into functional units and
consequent changes in their morphologies, and the high modification of limbs for very spe-
cific purposes, for example, reproduction/copulation. Lastly, limbs are also lost repeatedly
in various taxa. Reconstructing the evolutionary history of limbs along different crustacean
lineages is still a major task for future research.
HOW DID THE CRUSTACEAN APPENDAGES EVOLVE?
Noncrustacean euarthropod taxa such as myriapods, insects, and the arachnid chelicerates have
comparatively uniform, exclusively uniramous appendages (except for appendages 2–4) that
function mainly for walking. Moreover, they are made of one long, segmented element and are
restricted, at least in arachnids and insects, to either the head region (in arachnids called pro-
soma) or the thorax. The many thousands of species of Crustacea, however, exhibit a remark-
ably large variation regarding the morphology of their appendages, particularly the initially
biramous postantennular appendages, which are the focus of this chapter. At one extreme, crus-
tacean appendages may display high multifunctionality (Swiss Army knife effect); at the other
extreme, they or parts of them may be specialized for a particular function. To highlight the
problem of comparability, limbs that are used exclusively for walking, as in several malacostra-
can taxa, appear, at first sight, strikingly similar to those of the (mostly) terrestrial euarthropod
taxa mentioned above; that is, they are made of one long, segmented element. This superficial
similarity is misleading, however, because even this design is based on a quite different origi-
nal morphology. Yet, it is fairly easy to distinguish crustacean limbs from those of noncrusta-
cean taxa, mainly because of the morphology of their proximal parts, original constitution, and
details of joint morphology—but only when we have knowledge of the morphologies in the sur-
rounding taxa and of the historical traits.
When tracing limb morphology back in time, postantennular limbs in the ground pattern
of the crown arthropods, the Euarthropoda, were indeed all “biramous.” This means that they
consisted of a rigid, large, platelike basal structure, the “basipod,” that carried one rod-shaped
ramus mediodistally, the so-called endopod, and a paddle-shaped structure on its sloping lateral
edge, the exopod (basipod = carrier of the rami; e.g., Waloszek et al. 2005, 2007).
Consequently, uniramy within euarthropods constitutes the apomorphic state.
Development of uniramy in arachnid chelicerates is readily reproducible since postcheliceral
prosomal arachnid appendages possess the basipod as a small proximal element and an elon-
gate endopod made of several articles, possibly more than eight originally. The disappear-
ance of the exopod is evidenced by the presence of this ramus on opisthosomal limbs and on
the last walking limb (called flabellum; see Boxshall 2004) of xiphosurids. Moreover, within
arachnids, the basipod even becomes fixed to the body. This results in a situation where the
endopod-basipod joint is the limb-mover joint, and the main part for walking is the endopod:
arachnids are “endopod” walkers (and head walkers). In all uniramous myriapods, insects, and
crustaceans, the main joint remains the body-limb joint, so they are “whole-limb” walkers.
Uniramy in crustaceans has apparently developed many times convergently, such as in various
taxa of malacostracan crustaceans, for example, amphipods, isopods, and different ingroups
of decapods. In these “thoracic walkers” (rather, walking on limbs of thorax I sensu Walossek
and Mü ller 1998a), the proximal limb portion is a coxa (see below for its origin), while the
(plesiomorphically retained) basipod is the second limb portion and about as small as the coxa.
This basipod then gives rise to the basically five-segmented and astonishingly uniform, elon-
gate endopod. In all cases, the original state as deducible from the related taxa is the possession
of an exopod stemming from the basipod, so there is convergence in all cases. Uniramy also
occurs in Entomostraca, such as in some ostracodes and in the predatory water fleas (onycho-
pods and haplopods). The latter do not really walk on their thoracopods, but use them for many
tasks, including grasping prey. The number of limb portions is also different from that of mala-
costracans because a coxa is lacking from the beginning. The situation is even more complex for
myriapods and insects because we cannot apply, at present, the terms coxa and basipod to the
proximal limb elements due to lack of reference structures, for example, the exopod.
The question therefore arises of how this large variety of appendage morphologies evolved
in crustaceans. Moreover, what was the original condition and morphology that crustaceans
received from their ancestors to start with? With this and a better knowledge of what the
appendages looked like in the ground pattern of Crustacea, we may understand what they were
used for, how they evolved subsequently, and what the probable driving forces were. It is, in this
context, also important to clearly homologize the different limb parts—to use an appropriate
and consistent terminology—in order to trace them from the beginning of limb formation in
arthropods to modern crustacean taxa. Clearly, the basic form was laid down much earlier, and
crustacean postantennular limbs retained (as a “historical burden”) much of the morphology
that was present even in the stem taxa of Arthropoda sensu stricto (= s. str.) and Euarthropoda,
at least initially (see below).
It seems useful, therefore, to start this review with a look at our current understanding of
postantennular limbs before Crustacea. This might help us to better understand the specific
changes in the early evolutionary lineage of crustaceans that led to the conditions developed
within the modern ingroups. This might also allow us to overcome the difficulties with mor-
phologies and terminologies people have had in the past when addressing the question of the
general morphology of crustacean appendages and their origin—particularly those attempts
made before data became available about the early to late Cambrian fossils of the Chengjiang
and “Orsten” fossil deposits (lagerstätten). Examples of such historical studies are Hansen (1925),
Størmer (1939), Heegaard (1945), Snodgrass (1958), and Kaestner (1967). Neglecting the fossil
data even after this information became available is not much better. And sometimes it appears
that there are as many different answers as there are researchers in this field—all researchers
seem to have developed their own ideas and terminologies (examples of more recent attempts:
Boxshall 2004, Williams 2004, Boxshall and Jaume 2009). Accordingly, there is still no consen-
sus in sight today.
Our review cannot cover all of the different morphologies present in Crustacea but instead
seeks to focus on some major issues, such as origin and fate of the crustacean postantennular
appendages and their major components. Also, some examples of the capabilities crustaceans
have achieved are given to demonstrate that crustaceans are the euarthropod taxon that made
the most use of its appendages—and did so very successfully.
THE “ORSTEN” PERSPECTIVE
Our overview is based on data from studies of extant larval and adult Crustacea, including our
own investigations, and particularly on the Cambrian fossil record of the Crustacea, which
is evident exclusively from Orsten crustaceans with an age of 520–495 million years. There
are multiple reasons for considering this fossil evidence. First, Orsten fossils are old, but
superbly three-dimensionally preserved, thus interpretable almost as living forms. Second,
because of their ancient age, these fossils exhibit characters or character combinations that
may not, or should no longer, exist in extant crustaceans, therefore helping to identify early
evolutionary pathways. Third, different ontogenetic stages have been uncovered from several
of the Orsten-type fossils, particularly taxa of the crustacean lineage, permitting interpreta-
tions of the sequential morphogenesis of structures. Three-dimensional Orsten preservation
in full detail, down to even submicrometer scale and in topologically correct position, also
facilitates functional-morphological interpretations, which represent another helpful tool in
understanding evolutionary pathways. Fourth, these Cambrian crustacean fossils comprise
species that have been demonstrated to represent different evolutionary levels. Accordingly,
their data can aid in sorting features in the order of evolutionary and ontogenetic appearance.
The resulting phylogenetic tree directly ref lects the appearance of particular features on cer-
tain nodes, with some species already possessing certain features that others (still) lack. This
knowledge can be readily used for reciprocal illumination sensu Hennig (1965). Fifth, these
fossils help us to progressively establish a consistent terminology for crustacean and even
arthropod appendages, including a coloration scheme for homologous parts of limbs based
on the fossil material, which can be followed up from Arthropoda s. str. (the evolutionary
level of sclerotized arthropods; see Maas et al. 2004) into the different crustacean ingroups
(e.g., Walossek 1993; see also Walossek and Mü ller 1990, 1998a, 1998b, Maas et al. 2003, 2004,
Waloszek 2003a, Waloszek et al. 2007, Zhang et al. 2007, Stein et al. 2008, Haug et al. 2009a).
Our approach permitted, for the first time, large-scale comparability between the various
crustacean and euarthropod taxa.
This helped not only to sort in new taxa, including two-dimensionally preserved forms (e.g.,
from Chengjiang and Burgess lagerstätten) but also to identify modifications of known morphol-
ogies and to correct past errors in interpretation. This allowed for various new better-known
taxa to be added to our knowledge base and significantly improved our understanding of the
evolutionary pathways of structures and structural systems in arthropods and Crustacea. It is
particularly the evidence of structures and structural systems in the early fossil record that we
consider useful for understanding phylogeny and evolution—sometimes even more than any
other data, because the once living morphologies are the proof of existing structures and are
always superior to models of any kind. Altogether, research on fossils in Orsten-type preserva-
tion and the huge character data set provided by the other sources has challenged traditional
assumptions on the early evolution of Crustacea and has significantly stimulated this subject.
The result of this is, it is hoped, a straightforward, consistent view of the evolution and phylog-
eny of the Crustacea and their appendages.
Sources for Fossilized Appendages
In studying the early radiation of arthropods in the Cambrian (first geological period for
the fossil record of animals), we made use (mainly) of four lagerstätten: the North American
Burgess Shale, the Sirius Passet in northern Greenland, the Chinese Chengjiang biota, and the
world-wide occurring Orsten. The name Orsten has been applied to limestone nodules, which
are embedded within alum shales. They were first found in Sweden in rocks dated to the mid-
dle to upper Cambrian, but they occur worldwide (North America, Europe, Siberia/Russia,
China, and Australia) from the Terreneuvian series (former lower Cambrian; ca. 520 mya) to
the Lower Ordovician (ca. 490 mya) (Maas et al. 2006). While fossils from Burgess Shale, Sirius
Passet, and Chengjiang provide us with data from the level of Arthropoda sensu lato (= s. l.)
up to Euarthropoda (unassignable taxa, chelicerates, trilobites and allied), only the Orsten has
yielded confirmed crustacean fossils from the Cambrian (besides lobopods, chelicerates, and
agnostid euarthropods).
Several Cambrian species have been claimed to be Crustacea. A few prominent examples of
so-called “crustaceans” from the Burgess Shale are Branchiocaris pretiosa Resser, 1929 (see Briggs
1976), Waptia fieldensis Walcott, 1912 (Heldt 1954), and Canadaspis perfecta Walcott, 1912 (Briggs
1978). There are further examples from the Chengjiang biota, such as Pectocaris spatiosa Hou,
1999 (Hou et al. 2004), Ercaia minuscula Chen et al., 2001 (Chen et al. 2001), and Isoxys auritus
Jiang, 1982 (Shu et al. 1995). Although all these species have been assigned to Crustacea or even
to ingroups, many if not all of them may be euarthropods or, in some cases, not even members
but stem derivatives (e.g., Dahl 1984, Maas and Waloszek 2001a, Taylor 2002, Waloszek et al.
2005, Budd 2008). Indeed, interpretations of the mentioned species as crustaceans suffered
from a rather incomplete knowledge of their morphologies, especially concerning the segmen-
tal composition of the head or the (important) proximal parts of the appendages. Likewise, the
Cambrian record of malacostracans (based on the stem euarthropod Canadaspis perfecta; see
Maas and Waloszek 2001a) and ostracodes (bradoriids and phosphatocopines misidentified as
eucrustacean ostracodes) is based simply on misinterpretations, even though it is mentioned in
modern textbooks. Until now, no unequivocal malacostracan and no ostracode had been uncov-
ered in the Cambrian (Siveter 2008).
Orsten-type preservation, by contrast, provides a rather complete view of historic (crusta-
cean) animals, because Orsten fossils are uncompressed and exhibit the finest details, such as
setae carrying minute setules, eye structures with visible facet patterns, and weakly sclerotized
membranous areas such as the arthrodial membranes of the appendages, with the smallest vis-
ible structures being only 0.2 μm (for a summary, see Maas et al. 2006). The reason for this may
be the fine impregnation of the epicuticular surface by phosphate (apatite), which conserves the
finest denticles and pores. Strangely, and for unknown reasons, the fossils do not exceed a length
of 3 mm, and the best-preserved ones are only 100–200 μm in length. Thus, a large amount of
larval and young developmental stages occurs in the material.
Given the small sizes of the preserved organisms, species from the Orsten are rarely rep-
resented by adults. If preserved, these adults are small in size, such as for the species of Skara
Mü ller, 1983 (e.g., Mü ller and Walossek 1985, Liu and Dong 2007) and Dala peilertae Mü ller,
1982 (Walossek and Mü ller 1998b), or possibly Bredocaris admirabilis Mü ller, 1983 (Mü ller and
Walossek 1988). A larger number of taxa are known only from certain early postembryonic (lar-
val) stages or sets of them (e.g., Mü ller and Walossek 1986a, Walossek and Mü ller 1989). Some
species are even represented by a larger set of ontogenetic stages that allow the reconstruc-
tion of more or less complete ontogenetic sequences. Examples are the euarthropod Agnostus
pisiformis Wahlenberg, 1818 (Mü ller and Walossek 1987) and various crustacean taxa such as
Hesslandona unisulcata Mü ller, 1982 (Maas et al. 2003; see Fig. 2.1E,F), Henningsmoenicaris scu-
tula (Walossek and Mü ller 1990) (Haug et al. 2010a), and Rehbachiella kinnekullensis Mü ller,
1983 (Walossek 1993; see Fig. 2.1I,J).
This large set of exceptionally preserved fossils also provides us with a wealth of morpho-
logical features and allows us to study the ontogeny and, particularly, the morphology and
morphogenesis of appendages in much detail. In a combined approach using data from extant
taxa, fossils, and data from ontogenies of both sources (although size limitation might cause a
slight bias), Orsten-type fossils have yielded key information for understanding early crusta-
cean evolution and might be regarded as the principal source. While Schram (1986) initially
considered them “larval f lotsam,” and Lauterbach (particularly Lauterbach 1986) tried to pro-
mote the view that Orsten fossil taxa are nothing but a bunch of stem mandibulates, intense
study of Orsten species over almost 30 years uncovered them as a set of taxa derived from very
different evolutionary levels. This differentiated view and understanding of their morpholo-
gies in the light of changes along the evolutionary lineage of Crustacea permitted the recog-
nition of the specific fate of particular appendages, their morphology, and their association
Fig. 2.1.
Examples of “stem crustaceans” and labrophorans (Phosphatocopina + Eucrustacea) in the Orsten mate-
rial (scanning electron microscopic images and reconstructions). (A and B) The cambropachycopid
Goticaris longispinosa Walossek and Mü ller, 1990. (C and D) The “stem crustacean” Martinssonia elongata
Mü ller and Walossek, 1986. (E and F) The phosphatocopine Hesslandona unisulcata Mü ller, 1982. (G and H)
The entomostracan Yicaris dianensis Zhang et al., 2007. (I and J) The branchiopod Rehbachiella kinnekul-
lensis Mü ller, 1983. In this figure and those that follow, repository numbers and museum names are given
so that the reader can locate these specimens: BM, Natural History Museum, London; MB.A, Museum
f ü r Naturkunde, Berlin, Germany; UB, University of Bonn, Germany; YKLP, Yunnan Key Laboratory for
Paleontology, Yunnan University, Kunming, China. (A) UB 98; (C) UB 752; (E) UB 1570; (G) YKLP 10841
(Zhang et al. 2007, their fig. 1a); (H) from Zhang et al. 2007, their fig. 2; (I) UB 644. All figures used with
permission of the authors.
within the series of limbs along the body. These fossils could also be used to illuminate the
early branchings of the crustacean lineage into lines with living descendants and the evolu-
tion of structural systems such as locomotory and feeding apparatus (e.g., Stein et al. 2005,
Waloszek et al. 2007).
In fact, several species from the Cambrian Orsten fossil sites could thus be assigned to the
crown group of Crustacea, Eucrustacea (Müller 1983, Müller and Walossek 1985, 1988, Walossek
1993, Zhang et al. 2007) and are even deeply nested within extant taxa. Others belong to the
Phosphatocopina, a group of small bivalved forms that could be identified as the sister group of
Eucrustacea (Phosphatocopina + Eucrustacea = Labrophora; see Maas et al. 2003, Siveter et al.
2003; see also Waloszek 2003a, 2003b, Maas and Waloszek 2005). Lastly, a set of taxa turned out
to represent derivatives of earlier branchings (see below). Until now, the Orsten is the only pale-
ontological source providing species that are derivatives of the stem lineage of Labrophora, thus
extending the view of the crustacean stem lineage further back in time phylogenetically (Walossek
and Müller 1990, Stein et al. 2005, 2008, Haug et al. 2009a, 2010a, 2010b; see Fig. 2.1A–D).
Appendage Morphologies
The Basis, 1: Appendages at the Level of Arthropoda sensu lato and sensu stricto
Before discussing the appendage morphologies of crustaceans, we need to know more about the
evolution and functional history of these limbs. This will also ensure that we understand the
respective homologies and apply appropriate terminology to these appendages. Accordingly,
we need to know about the ground pattern status of limbs before the crustacean level, that is,
the postantennular limbs in the ground pattern of Euarthropoda and, even prior to this, of the
Arthropoda s. str. and s. l. (see Maas et al. 2004, Waloszek et al. 2005). The arthropod system as
it is used throughout this chapter has been developed over a period of almost 30 years and laid
down in many of our papers. It is presented in Table 2.1 in a simplified written version, following
the notation proposed by Hennig (1965) and Ax (1995).
Table 2.1 Phylogenetic system of Arthropoda.

Arthropoda sensu lato Maas et al., 2004
(= Aiolopoda Hou and Bergström, 2006 [see Bergström et al. 2008])
Arthropoda sensu stricto Maas et al., 2004
(= Arthropoda sensu Bergström et al. 2008)
“Fuxianhuiidae” Hou and Bergström, 1997
Euarthropoda Walossek, 1999
Chelicerata Heymons, 1901
Myriapoda Latreille, 1796
Insecta Linnaeus, 1758
Crustacea sensu lato Stein et al., 2008
(= Crustacea Brünnich, 1772)
N.N. 2 = unnamed sister taxon
Labrophora Siveter, Waloszek, and Williams, 2003
Phosphatocopina K.J. Müller, 1964
Eucrustacea Kingsley, 1894 (sensu Walossek 1999)
Entomostraca O.F. Müller, 1785
Malacostraca Latreille, 1802
A B C D E
mem mem mem
basipod endopod exopod proximal endite / coxa
Fig. 2.2.
Postantennular appendages from Arthropoda sensu stricto to Eucrustacea. mem, membrane. (A)
Arthropoda sensu stricto: Fuxianhuia protensa Hou, 1987. (B and C) Euarthropoda. (B) Leanchoilia
illecebrosa Hou, 1987 (modified after Liu et al. 2007). (C) Agnostus pisiformis Wahlenberg, 1818. (D)
Crustacea sensu lato: Martinssonia elongata Müller and Walossek, 1986. (E) Eucrustacea: Skara anu-
lata Müller, 1983. Color scheme modified from Walossek (1993): black, proximal endite/coxa; light
gray, basipod; medium gray, endopod; dark gray, exopod. All figures used with permission of the
authors.
The crustacean postantennular limbs consist of four major parts, for which we have to iden-
tify the traits in earlier morphologies. The ground pattern of the soft cuticle-bearing arthro-
pods in the broad sense (Arthropoda s. l.) forms the start, because we have some knowledge
from extant onychophorans and about 10 Cambrian so-called lobopodians (Maas et al. 2007).
Legs of such forms (and autapomorphy of the taxon Arthropoda s. l.) were tubular, possibly
ending in a distal pair of claw hooks, and as soft as the body proper. Arthropods in the strict
sense (Arthropoda s. str.) have, among other features, a much more sclerotized dorsoventrally
flattened body, each segment bearing a tergitic dorsal part connected by softer membranous
cuticle (the evolutionary process is called arthrodization). This morphology is known now
from three two-dimensionally but well-preserved, several-centimeters-long lower Cambrian
taxa: Fuxianhuia protensa Hou, 1987, Chengjiangocaris longiformis Hou and Bergström, 1991, and
Shankouia zhengei Chen et al., 2005 (Waloszek et al. 2005; see also Figs. 2.2A, 2.3A), tradition-
ally combined in the taxon Fuxianhuiidae with unclear phylogenetic status. These fossils also
helped to reconstruct the appendages in the ground pattern of Arthropoda s. str.
The main portion of their limbs, or limb stem, is tubular as before, but it is apomorphically
annulated consisting of approximately 20 sclerotic rings with membranes between. The articles
of these “arthropodia” articulate against each other via two opposing so-called pivot joints, that
is, knoblet-against-depression joints (evolutionary process: arthropodization). This construc-
tion might have guaranteed flexibility as before but also provided much more stability for walk-
ing on the limbs with the body lifted up to some degree. Yet the joint angle of bending between
the articles is limited—possibly the high number of articles counterbalanced this. Another new
limb structure is a paddle-shaped structure on all postantennular limbs arising from the outer
proximal edge of the limb stem (Fig. 2.2A, 2.3A), which is missing, however, on the first append-
age, the antennula.
The new postantennular arthropodium (Fig. 2.2A) consists, therefore, of two major ele-
ments and one significant detail: the multiannulated stem (originating from the lobopodium,
but now segmented), the pivot joints (new), and the flaplike outer ramus (new). In a way, this
is a biramy induced at this level, but it is different from the next step (the Euarthropoda level)
A B
C D
E F
G H
?
I basipod
endopod
exopod
proximal endite /
coxa
Fig. 2.3.
Schematic evolution of the arthropod limb apparatus from Arthropoda sensu stricto into Eucrustacea:
ground pattern status of the limb series. (A) Arthropoda sensu stricto based on Shankouia zhenghei Chen
et al., 2005 in Waloszek et al. (2005). (B) Euarthropoda, based on different taxa; number of endopod seg-
ments and exopod morphology mainly based on Leanchoilia illecebrosa Hou, 1987 (Liu et al. 2007, used
with permission). (C) Crustacea sensu lato based on Oelandocaris oelandica Mü ller, 1983 (Stein et al. 2008).
(D) Crustacea sensu lato excluding Oelandocaris oelandica, based partly on Martinssonia elongata Mü ller and
Walossek, 1986; ? indicates that some aspects are still unclear, such as exopod morphology. (E) Labrophora
(Waloszek 2003b, Maas et al. 2003, Waloszek et al. 2007). (F) Phosphatocopina (Maas et al. 2003, Maas and
Waloszek 2005); ? indicates unclear condition of coxa-basipod border in second appendage. (G) Eucrustacea
(Maas et al. 2003, Waloszek 2003b, Waloszek et al. 2007); ? indicates that the exact ground pattern condi-
tion of maxillula is unclear. (H) Entomostraca (Waloszek 2003b). (I) Malacostraca (Waloszek 2003b). Gray
shading scheme is as described in Fig. 2.2. All figures used with permission of the authors.
because only the flap is a ramus, in the sense of subsequent evolutionary steps. The stem is
in fact the main part that may be subdivided into functional portions and not a ramus. It also
demonstrates that the two portions, stem and flap, are of different age phylogenetically and by
no means symmetrical.
It may be, as known from subdivided limb parts of living arthropods and particularly crus-
taceans, that all articles were interconnected by fine muscle strands operating as intrinsic and
extrinsic musculature, with the possible exception of the terminal article (see Waloszek et al.
2007, their fig. 4G). The flap may have served to some degree as a respiratory surface but more
likely as a locomotive aid, permitting the animal to produce some water flow around the body.
Thus, it may have initiated a swimming mode of life for arthropods in addition to their crawling
lifestyle.
It is also important to note the body parts that the early arthropodium lacks: there is, most
likely, no basal limb joint; there are only a few shorter annules; and no setae or spines (immo-
bile stronger outgrowths) developed, either on the stem or along the margin of the flap. It
seems that the limbs were exclusively used for locomotion—and were all very similar to each
other (serially similar). The only structure possibly useful for food grasping and transport to
the mouth was the uniramous 15-segmented antennula (Waloszek et al. 2005; see Fig. 2.3A), the
first head appendages associated with the deutocerebrum. And at least in Fuxianhuia protensa
it may have carried one fine spine medially on each of the articles (Hou and Bergström 1997,
Waloszek et al. 2005).
The Basis, 2: Appendages at the Level of Euarthropoda
Various species, such as Canadaspis perfecta (Briggs 1978), have the potential of helping research-
ers document the evolutionary lineage to the next level, Euarthropoda. However, our knowledge
of these species is still too incomplete for a more conclusive discussion. While the antennula
apparently has not changed morphologically or functionally (grasping, food collecting aid) in
the ground pattern of Euarthropoda, two major events toward this level had taken place—most
likely achieved by more than just one single stem species. One event is the development of a
larger head unit, including the fact that now all postantennular limbs, though remaining serially
similar, are grouped into three cephalic and a set of trunk limbs.
The other event is the development of a significantly different postantennular limb, which
in the ground pattern of Euarthropoda possesses three major elements and another important
structure (Figs. 2.2B,C, 2.3B). All postantennular limbs are anteroposteriorly compressed, there-
fore extended in mediolateral direction and not circular in cross section like the limb stem of the
arthropodium. The first is a large subrectangular to triangular basal portion. A rodlike, distally
tapering and possibly nine-segmented structure (articles interconnected by pivot joints) arises
mediodistally from this portion. Another, paddle-shaped structure, marginally adorned with
setae, inserts on the outer sloping margin of the stem portion.
Importantly, the stem portion, as we know from several Cambrian fossil arthropods, shows
more details, demonstrating the significance of this level for the evolution of arthropod and
crustacean limbs. All rigid basal portions arise from the ventral body proper like bricks placed
abaxially on their narrower edges in a regular series on the left and right sides at some distance
between the pair, leaving a median path for food transport. Another morphological detail is that
the basal portions articulate with the body in an ample folded arthrodial or joint membrane.
Such folds are even visible in two-dimensionally preserved fossils (e.g., Leanchoilia illecebrosa
Hou, 1987; see Liu et al. 2007). This joint membrane may have facilitated movability of the limb,
while the rigidity of the basal portion may have permitted attachment of stronger muscles within
the stem in order to enhance operability of the limb. The elongation of the limb in mediolateral
direction limits movability to a largely forward-backward swing, but this was even enhanced by
a second feature: anterior and posterior sides of the limb stems are of different morphology. The
anterior edge is straight proximally, while the posterior edge is excavated. This condition may
have permitted wider backward than anterior swinging (e.g., Liu et al. 2007).
The next noteworthy feature is that the elongate narrow median edge of the stem portion
carries a row of spines, or pairs of spines, from proximal to distal pointing medially into the
interlimb space or food path. It is likely that these structures aided in food transport toward
the mouth, but it is possible that they (and others mentioned here) developed earlier, as such
structures are developed in the putative stem lineage derivate Canadaspis perfecta. It should
be noted that early in the evolution of Arthropoda and Euarthropoda, it is very difficult to dif-
ferentiate between immobile spines and spinelike setae that have a joint at their base. Fossils
are not preserved well enough to verify this. In our Orsten forms, this detail can be observed
more clearly, but it seems that because of size, many more robust structures are simply lacking
a joint, although they have a socket; thus, they should be named spines. By contrast, marginal
outgrowths of exopods used as swimming aids should continue to be named setae, although
they are not necessarily mobile. Outgrowths of small entomostracan crustaceans are not eas-
ily compared with those of Malacostraca (see below). Terminological classification may not
be easily applied across larger taxa because such typification may also be phylogenetically
misleading.
We have called this basal portion of Euarthropoda basipod (e.g., Waloszek et al. 2005).
The basipod not only has a characteristic shape but also carries the two rami (see above). The
endopod arises mediodistally and in line with the spine-bearing inner edge of the basipod. It
is rodlike and roughly circular in cross section. Its portions, called podomeres, are all about
the same size and are slightly humped mediodistally, each hump bearing one or two spines or
setae, very similar to those along the median edge of the basipod. The distal smaller element
bears a tuft of one or few spines or setae. It remains unclear if there were eight, nine, or even
more endopodal podomeres originally, and it is also unclear if and how much the endopod
was proximally partly fused with the outer f lap (Liu et al. 2007, their fig. 5, Stein et al. 2008,
their fig. 7D–F).
The flap arising from the sloping outer margin of the basipod is fringed with marginal setae.
The oblique orientation of this joint permits the flap to be held more laterally, therefore facili-
tating or improving the use of this flap as a locomotory device. Subdivision of the flap into a
triangular proximal part and a distal portion might even enhance locomotory abilities (Liu et al.
2007, Stein et al. 2008, Haug et al. 2010a), though we cannot yet validate this conclusively due
to lack of more evidence. We understand this setose flap, the exopod, as homologous to the
lateral flap of the arthropodium in the ground pattern of Arthropoda s. str. It remains unclear
if the exopod was individually movable by musculature at this stage, as demonstrated in extant
paddle-shaped exopods of crustaceans (e.g., branchiopods).
The entire morphology of the “euarthropodium,” as named herein, characterizing the level
of Euarthropoda, must be understood as derived from prior morphologies. It may hence be spec-
ulated that the folds of the arthropodial membrane and the sets of spines along the inner basipod
margin are indicators of an original subdivision, possibly corresponding to annules of the limb
rod of the “arthropodium.” Consequently, the cuticle of the proximal articles may have become
softer to form the basal joint area, while a set of more distal articles should have elongated in
abaxial aspect and fused to form the brick-shaped basipod. The only intermediate situation
must have been the development of spines, possibly in the course of achievement of a feeding
function of the proximal part of the limb stem. The limbs of the Cambrian species Canadaspis
perfecta (Briggs 1978, his fig. 108) could indeed give a hint to such a pathway (Maas and Waloszek
2001a), but this has to be verified in more detail.
Continuing this line of logic, the remaining part of the original multiannulated stem of the
arthropodium may have evolved into the endopod of the euarthropodium. Again, the limb of
Canadaspis perfecta can help us understand this change, because it has spines mediodistally on all
its distal articles. A kind of functional split seems indicated, which lets us view the evolutionary
path to a complex multifunctional arthropodium, with its proximal part serving for feeding and
the distal for locomotion plus food intake. While the basipod muscles may have become some-
what concentrated, the endopod retained interior muscles running individually from podomere
to podomere, which indeed can still be observed in the endopods of extant crustaceans.
In any case, it becomes quite evident also for this euarthropodium that endopod and exopod
are very different structures in terms of origin and morphology. Likewise biramy is a problem
because the original arthropodium consisted in fact of only a stem and a single extra ramus,
while the euarthropodium has a basipod that carries two real rami (endopod and exopod). Yet,
the endopod is simply not the old stem. In fact, the stem has very likely been split into one piece
forming the membrane, one forming the basipod and one forming the endopod.
The only conservative trait in this scenario is the f lap-shaped exopod, which from its
appearance in the arthropodium did not change its shape and function in locomotion
(swimming), although, in addition, setae appear along the margin. The exopod has therefore
almost as deep phylogenetic roots as the stem, but its first appearance can be traced only to
the level of Arthropoda s. str. at present. It may, however, be possible that it had appeared ear-
lier, but informative fossils in these surroundings are still too poorly understood (e.g., Budd
1998, Liu et al. 2007). The stem, on the other hand, can be traced down to the “lobopodium”
of Arthropoda s. l.
The complex limb morphology of the euarthropodium indicates that it had developed into
a multifunctional tool, using the whole set of appendages in a simple heterochronal movement
cycle that aided in locomotion as much as in food intake and manipulation. Moreover, the two
processes were rather neatly coupled. The basipod spines could assist in food transfer to the
mouth, while the endopod aided in locomotion and, with its spines, also aided in food manip-
ulation. The distal spines might even have permitted some scratching and sorting of food.
Though everything was (still) strictly serial, it was a huge innovation for arthropods to have
such a three-part euarthropodium comprising a basipod carrying the endopod and exopod.
Indeed, it was so successful that much of it—for example, the slope for the exopod—is still
present in certain appendages particularly of early larval stages of crustaceans (e.g., cirriped
nauplii), as well as in the Orsten crustaceans (see below). This morphology, particularly the
slope, can be used as a nice reference when searching for homologies of structures in different
taxa and for testing hypotheses about limb evolution in arthropods (see also Fig. 2.3).
The morphology must have been so effective that this tripartite euarthropodium (not
two or four parts! see Fig. 2.2B) and the strict seriality of the postantennular limbs was
transferred into the various descending evolutionary lineages. Various Paleozoic repre-
sentatives of the Euarthropoda such as trilobites and allied taxa exhibit this morphology
and seriality (though some head limbs may be smaller than the rest, as in Emeraldella brocki
Walcott, 1912 or Parapeytoia yunnanensis Hou, Bergström, and Ahlberg, 1995). Parts of this
complex limb morphology may well have developed earlier. Chelicerates are another exam-
ple taxon with extant descendants that retained this morphology during their evolution,
changing little more than the grasping antennula into a short chelicera (e.g., Chen et al.
2004, esp. their fig. 5).
The morphology of the entire apparatus suggests that it was a conjointly feeding and loco-
motion system: stopping locomotion meant stopping feeding. This may have been the reason
that this strategy was not taken over completely by all successive euarthropod lineages, at least
in those reducing the food-intake possibilities of more posterior limbs, as in the modern cheli-
cerates, myriapods, and insects.
In a way, Crustacea are the ones among the taxa with living representatives that retained
most of the morphology of the euarthropodium in their ground pattern—also Agnostus pisi-
formis Wahlenber, 1818, a minute euarthropod (Mü ller and Walossek 1987) with supposed affini-
ties to crustaceans (Walossek and Mü ller 1990, Stein et al. 2005, Haug et al. 2010a). And they
made the most use of it. Initially, however, much of the seriality was retained.
Appendages at the Level of Crustacea sensu lato
The appendages of crustaceans indeed exhibit such various plesiomorphic traits. This is most
evident in several Orsten fossil crustaceans that we refer to as stem derivatives—more precisely,
derivatives of the evolutionary lineage toward the Labrophora, comprising the Phosphatocopina
and the Eucrustacea (e.g., Waloszek et al. 2007). Examples of plesiomorphies are the seriality
and the gross morphology of the postantennular limbs, with the ample joint, the basipod (pos-
teriorly more excavated) with median spines on a rather straight median edge, the mediodistal
endopod with sets of spines, and the paddle-shaped exopod with marginal setae on the sloping
edge of the basipod (Fig. 2.4A).
However, this holds true only for the more posterior limbs because all three anterior append-
ages, that is, the antennulae and the following two limbs, are more specialized in the ground
pattern of Crustacea s. l. than are the corresponding appendages in the euarthropod ground pat-
tern and therefore are more like those in modern crustaceans. Nevertheless, these fossil species
combined as stem derivatives are not stem species themselves but exhibit also autapomorphies
indicative of their own evolutionary lineage (the reason that we usually speak of stem-lineage
derivatives). The following interpretations are therefore based not on single species or speci-
mens but on more than half a dozen known species. Moreover, they apparently represent differ-
ent evolutionary levels, and several of them are preserved as a set of instar stages.
Based on this evidence, we have identified several evolutionary novelties of Crustacea in the
wider sense. Many if not most affected the morphology particularly of the appendages and are
coupled with the locomotory and feeding apparatus, apparently an important issue for this euar-
thropod group. These are, for example,
• the deviation from a strict seriality of all postantennular body limbs (state of Arthropoda
s. str. and Euarthropoda; Fig. 2.3A,B);
• changing tagmosis of the head-trunk system, for example, by incorporation of more trunk
segments into the head, and specializations of limbs;
• changes in the locomotory and feeding system, again with differentiated development in
the head and the trunk, likewise independent of the changing tagmosis;
• the development of associated features with the changes in the functional system; and
• changes in the morphology of the appendages, individually as well as in sets (further
development of tagmata).
The first significant changes of the appendages and their morphologies along the crustacean
evolutionary lineage based on the stem derivatives are interpreted as autapomorphies in the
ground pattern of Crustacea s. l.:
1. Antennulae uniramous, composed of a few tubular portions or articles, though large,

limblike, and not feelerlike, but involved in both feeding and locomotion; several long
setae along the posterior side of the appendage (originally the median side) and on the tip
(see, e.g., Haug et al. 2009a for Cambropachycopidae or Stein et al. 2008 for Oelandocaris
oelandica Mü ller, 1983).
Comments: Plesiomorphies associated with the antennula include the insertion anterola-
terally at the hypostome, and the function of the antennula possibly only for food gathering
(a similar specialization has also been found in Agnostus pisiformis, which, by contrast, has
a 15-segmented antennula with short spines). A sensorial antennula seems to have evolved
convergently in several evolutionary lineages of the Euarthropoda, for example, in mala-
costracan crustaceans and atelocerate taxa (myriapods and insects). In the evolutionary
lineage of chelicerates, the antennula changed into a highly shortened grasping element,
the chelicera (Chen et al. 2004).
2. Anterior three appendages morphologically different from each other and from the more
posterior ones.
Comments: In the ground pattern of Arthropoda s. str., only the antennula differs from
the serial biramous trunk limbs in being uniramous and the major food-raking element
Fig. 2.4.
Scanning electron microscopic images of different postantennular limbs of Orsten fossil crustaceans.
(A) Isolated trunk limb of Henningsmoenicaris scutula Walossek and Mü ller, 1990, stage 10 with paddle-shaped
exopod. No proximal endite is present at this ontogenetic stage. (B) Third appendage of Hen. scutula, stage
8, multiannulated exopod with few articles, distal part of endopod broken off. The proximal endite is still
small at this evolutionary level. (C) Second appendage of Goticaris longispinosa Walossek and Mü ller, 1990,
stage 2 with multiannulated exopod. (D) Proximal endite of a trunk limb of a very late ontogenetic stage
of Hen. scutula. At this ontogenetic stage, trunk limbs also possess proximal endites. Scale bar, 10 μm. (E)
Postmandibular appendage of the phosphatocopine Hesslandona unisulcata Mü ller, 1982, growth stage III.
Note the large proximal endite, the enditic protrusions on basipod and endopod drawn out medially, and
the exopod being paddle-shaped proximally and multiannulated distally. (F) Mandible of Hes. unisulcata
with multiannulated exopod, short endopod, small basipod, and large coxa. (G) Cephalic appendages of
Martinssonia elongata Mü ller and Walossek, 1986. Multiannulation of exopod is only weakly developed. (H)
Postmandibular appendage of growth stage V of Hes. unisulcata. The exopod is paddle-shaped proximally
and multiannulated distally as in Fig. 2.4E, but the multiannulated part is smaller in this specimen due to
later ontogenetic stage. (I) Subequal (second) antenna (right) and mandible (left) of Skara anulata Mü ller,
1983, with multiannulated exopods. Abbreviations: bas, basipod; cox, coxa; en, endopod; ex, exopod; pe,
proximal endite. Repository numbers (see Fig. 2.1 for abbreviations): (A) UB W 338; (B) UB W 335; (C) UB
W 124; (D) UB 103; (E) UB 103; (F) UB W 106; (G) UB 780; (H) UB W 156; (I) UB 692.
(Fig. 2.3A). Also in the euarthropods, all postantennal limbs are serial. The second append-
age is slightly shifted anteriorly in its position and may be smaller than the more posterior
limbs but still resembles them (Fig. 2.3B). Here in crustaceans, all three anterior append-
ages move in accord and are somewhat set off from the posterior ones with their hetero-
chronous beat (Fig. 2.3C). This points to a new type of combined locomotion and feeding
in Crustacea s. l., the so-called “sweep-net feeding” (Waloszek 2003b).
3. Exopods of the first and second postantennular limbs comprising a tubular proximal part
and a multiannulated distal part with each annulus carrying a long seta on the median
side, which is directed mediodistally against the endopod (Fig. 2.4C); the proximal socket
element may have served to raise the setae-bearing part slightly away from basipod and
endopod in order to facilitate the swing of the setae.
Comments: Plesiomorphically, the exopod is a simple flap with setae around its entire free
margin (compare Fig. 2.3B,C). In the putatively closest relative to Crustacea s. l., Agnostus
pisiformis (Stein et al. 2005), the exopods of the first and second postantennular limbs are
also multiannulated, but bear setae on their lateral = outer side (Mü ller and Walossek 1987,
their plates 18:1–5, 19:1). These two limbs are generally similar to each other, except that
because of the different position regarding the mouth, the basipod and its median enditic
armature were most likely already different.
However, the most apparent new feature of Crustacea s. l. is the following:
4. Possession of a small setiferous sclerotized humped area, the “proximal endite,” within the
body-basipod membrane of the postantennular limbs and clearly proximomedially of the
basipod (Fig. 2.2D).
Comments: This endite was termed as such by Walossek and Mü ller (1990; see also
Walossek 1993) because of its morphological similarity to median basipodal endites of
extant entomostracan eucrustaceans. Much earlier, Calman (1909, 51) had pointed to its
existence in branchiopods and remarked upon it being most likely a very old feature. In
contrast to Walossek and Mü ller (1990), who assumed its presence on all postantennular
limbs originally, recent investigations of the stem derivatives demonstrated its first appear-
ance only on the third appendage in young larvae, that appendage later called mandible
in Labrophora (e.g., Stein et al. 2005, 2008, Waloszek et al. 2007, Haug et al. 2009a, 2010a,
2010b; Fig. 2.4B).
The proximal endite is regarded as one of the key evolutionary characters of Crustacea
(Walossek and Mü ller 1990, Walossek 1993, Waloszek 2003a, 2003b), possibly appearing only
on the third appendage at first (Stein et al. 2005, 2008, Waloszek et al. 2007; but see Haug et al.
2010a). Further along the evolutionary lineage to the Eucrustacea, the proximal endite occurs
on all postantennular appendages, having become larger and more setiferous (Figs. 2.3D, 2.4D).
Its possible main purpose was food manipulation and transport, as seen still today, for example,
in cephalocarids and mystacocarids (Fig. 2.5G,H).
It is still unclear if the proximal endite was already movable at this early stage, as described,
for example, for the proximomedial endite (and the more distal ones) of Cephalocarida (see
Sanders 1963, Hessler 1964, his fig. 11). It also remains unclear if it served as a food-raking device
from the very beginning. Its functionality as an aid in food transport is, however, clear from
its later shape, position, and use in living taxa, indicative of its continuing significance in the
Fig. 2.5.
Scanning electron microscopic images of proximal and basipodal endites and appendage armatures.
(A) Mandible of an undetermined phosphatocopine. Anterior and posterior sets of setae are not yet
differentiated from each other. Numbers indicate different sets of setae: 1, anterior retention setae;
2, median set, usually developed as stronger spines; 3, posterior sieving setae. (B) Trunk limb of
Rehbachiella kinnekullensis Mü ller, 1983; numbers are as in A. While the retention setae (1) are arranged
in parallel rows, the sieving setae (3) form more or less a triangle. (C) Trunk appendage of Yicaris dian-
ensis Zhang et al., 2007 with about the same arrangement of setal sets as R. kinnekullensis; numbers are
as in A. (D) Trunk limbs of fossil R. kinnekullensis . (E) Trunk limbs of extant Cyclestheria hislopi (Baird,
1859) (Olesen 2007). Enditic arrangement very similar to that of R. kinnekullensis (see panel D). (F)
Anterior head region of the phosphatocopine Hesslandona unisulcata Mü ller, 1982. Note the enlarged
coxa of the mandible as an extreme variation of the proximal endite. (G) Postmaxillulary appendage
of the cephalocarid Lightiella monniotae Cals and Delamare-Deboutteville, 1970. (H) Maxillula of the
mystacocarid Derocheilocaris remanei Delamare-Deboutteville and Chappuis, 1951. Abbreviations: cox,
coxa; end, endite; pe, proximal endite; ste, sternum. Repository numbers (see Fig. 2.1 for abbreviations):
(A) UB W 255; (B) UB W 380; (C) Spec. 5/YKLP 10846; (D) UB W 86; (F) UB W 381. All figures used
with permission of the authors.
food-gathering apparatus of head and thorax. Its absence in other euarthropods, including
Agnostus pisiformis (Mü ller and Walossek 1987, Waloszek et al. 2007), is interpreted as primary
lack, while other general appendage features are shared between A. pisiformis and Crustacea s. l.,
that is, multiannulated exopods on appendages 2 and 3, suggestive of closer alliance.
One less obvious feature of Crustacea s. l. concerns the number of endopod podomeres. In
the ground pattern of euarthropods, there may have been 9, possibly up to 11. Not least regarding
its armament with median spines, this may point to the importance of the endopod in both food
gathering and locomotion (possibly walking). The exclusively Paleozoic trilobites had con-
stantly seven endopod podomeres, as also Agnostus pisiformis (Mü ller and Walossek 1987, also
for data on trilobite limbs). In crustaceans the maximum number observed is six (Zhang et al.
2007 for Yicaris dianensis), five or six in Cephalocarida depending on the authors (e.g., Jones
1961), or always five in Malacostraca (specializations not counted). The maximum observed in
Orsten stem derivatives was originally thought to be five, but maybe six or seven (Haug et al.
2010a). Most fossil and extant taxa have fewer endopod podomeres, at times four or even as few
as one portion (which may not be a simple single podomere, however). This may point to a rather
early initiation of different uses of endopods, likely in accordance with differences in lifestyles
of their carriers. Walkers among malacostracans, for example, have five podomeres, but these
are tubular and may have enormous lengths so that in the extreme a limb can be more than a
meter long (for a size comparison of large arthropods, see Rudkin et al. 2003, their fig. 5). We
cannot, however, follow up this interesting question in more detail at present.
Seriality of limbs is also retained in crustaceans principally in all appendages behind the
third limb (Fig. 2.3C,D, level with more proximal endites), but these limbs share the proximal
endite with the preceding two limbs, and they differ from those in that they have paddle-shaped
exopods (Fig. 2.4A). Although partly retained from the euarthropod ground pattern, this indi-
cates the tagmotic break and the different use of anterior and posterior limbs.
We must admit that reconstructing the ground pattern status of exopods at this level remains
problematic because a multiannulated state (although with inwardly pointing setae, a status not
known from other arthropods) is known from a number of Orsten stem derivatives, such as
the cambropachycopid Goticaris longispinosa Walossek and Mü ller, 1990 (Haug et al. 2009a;
Fig. 2.1A,B) and Martinssonia elongata Mü ller and Walossek, 1986 (Fig. 2.1C,D) (unclear for
Cambropachycope clarksoni Walossek and Mü ller, 1990). In M. elongata, the annulation of its
exopods is only weakly developed (Mü ller and Walossek 1986b, their fig. 2.4G; see also Haug
et al. 2010b). As mentioned earlier, a triangular plate may be set off from the exopods basally,
as in Oelandocaris oelandica and Henningsmoenicaris scutula. In both, the distal part forms the
main setae-bearing paddle (Stein et al. 2005, 2008, Haug et al. 2010a). This morphology is
remarkably similar to what has also been described for a derivative of the stem lineage toward
Euchelicerata, Leanchoilia illecebrosa from the Terreneuvian Chengjiang fauna of China (Liu
et al. 2007). Whether these two exopod articles are homologous and how they relate to sub-
divisions developed in other Cambrian euarthropods such as trilobites and naraoiids remain
unclear at present.
Two noteworthy plesiomorphies have been taken over into the crustacean ground pattern.
One is the retention of a fairly rigid basipod with a straight inner rim carrying robust medially
pointing spines. This feature is recognizable in two of the Orsten stem derivatives, Oelandocaris
oelandica and Henningsmoenicaris scutula (Fig. 2.4A,B). All others have shortened this edge
in proximodistal aspect but elongated it in mediolateral aspect to a more humplike or endite-
like shape with a central major spine and some flanking spines or setae (e.g., in Goticaris long-
ispinosa; Fig. 2.4C). It seems that this feature may be useful to discriminate within the set of early
crustacean taxa and to resolve the early evolutionary lineage of Crustacea in more detail. The
other is an often-neglected plesiomorphy retained from Euarthropoda, namely, that the head
comprises only four appendage-bearing segments (Maas et al. 2003, Waloszek 2003b)—as in
Agnostus pisiformis. When exactly this change to a larger head unit occurred, and why, remains
unclear because several of our stem derivatives exhibit this condition. Other taxa have five
appendage-bearing head segments (H. scutula and O. oelandica). This cannot be evaluated any
further at present, but other characters indicate that the longer head may have been achieved
in parallel to the evolutionary development in the remaining crustacean taxa—as much as the
number six has been achieved various times in parallel in the different eucrustacean ingroups.
The shield cannot be the reason because H. scutula has a large shield and O. oelandica a smaller
one. There is also no change in the tagmotic pattern on the ventral side.
In summary, crustaceans have retained much of the limb morphology of the euarthropo-
dium, but evolved (1) a new type of exopod that is multiannulated and bears setae along the
inner side and (2) a fourth limb element, the proximal endite, that has no counterpart in any
other arthropod taxon. Up to the next evolutionary level, the described condition remains sta-
ble, except for the occurrence of more proximal endites along the limb series. This also implies
that the fourth and fifth appendages resemble trunk appendages—regardless of whether they
are already included into the head.
Appendages at the Level of Labrophora
Major novelties along the crustacean lineage characterize the evolutionary level of Labrophora
(Maas et al. 2003, Siveter et al. 2003). As before, most if not all of them are allied with significant
changes in the locomotory and feeding apparatus, more specifically the cephalic one (Waloszek
et al. 2007). However, only few changes affected the limb morphology. Examples of innovations
(autapomorphies) not associated with the appendages include the following:
• The appearance of an enormous fleshy “labrum” with slime glands and chemoreceptors on
the posterior side of the hypostome (note that labrum and hypostome are both present and
not synonymous structures!)
• The occurrence of a “sternum” as a fusion product of the sternites of the mandibular and
first postmandibular segments (no sternite belonging to the second appendage visible)
• A pair of humps on the mandibular sternite, the “paragnaths”
• Fine hairs or denticles occurring in rows on the labral flanks and like a carpet on the
sternum and paragnaths (for details, see, e.g., in Maas et al. 2003, Waloszek et al. 2007).
It is very likely that this, again, did not happen in a single stem species, but up to now we have not
discovered more fossil species to be able to split up this set more precisely.
Regarding appendage morphology, labrophoran autapomorphies occur, as far as we could
detect them in our material, only on the anterior two postantennular limbs but in two impor-
tant ways:
• The proximal endite of the second appendage, from this level on called antenna, is enlarged to a
ring-shaped sclerotic structure on the proximal end of the limb, long ago named coxa; its original
enditic surface with setae is prolonged and points, due to the special position of the antenna
laterally, at the labrum posteromedially around the labral flanks toward the mouth; the coxa now
carries the basipod with its median enditic hump and armature, which itself carries the rami.
• The proximal endite of the third appendages, now called “mandible,” is also enlarged to a
ring-shaped sclerotic structure on the proximal end of the limb; also here this coxa is medi-
ally prolonged but points medially because of the position of the mandible lateral to the
paragnaths; different from the antenna, the surface of the coxal endite is slightly flattened
and tilted against the mouth, a morphology often called gnathobase (Figs. 2.3E, 2.5F; see
Fig. 2.6F for an extreme variation).
Fig. 2.6.
Scanning electron microscopic images and schematic drawings of malacostracan and entomostracan trunk
limbs. (A) Pereopod of euphausiid malacostracan, not to scale. In contrast to Entomostraca, the thoracic
limbs of Malacostraca do not have endites. (B–D) Postmaxillulary appendages of different entomostra-
can species. (B) Lightiella monniotae Cals and Delamare-Deboutteville, 1970 (Cephalocarida). Note the
two-parted exopod. (C) Yicaris dianensis Zhang et al., 2007. The proximal part of the basipod is concealed.
(D) Dala peilertae Mü ller, 1982. Endites are bent toward the reader. (E) Schematic cross section of thorax
I (sensu Walossek and Mü ller 1998a) at the level of the first thoracopod of the malacostracan Speonebalia
cannoni Bowman, Yager, and Iliffe, 1985, modified after Bowman et al. (1985, their fig. 2a). Each sternite
has a median keel for food manipulation (Walossek 1993). (F and G) Cross sections at the level of post-
maxillulary appendages of two entomostracan species. Note the large number of endites and the proximal
endite, all used for feeding (Walossek 1993). (F) Y. dianensis, the only entomostracan with the unequivocal
(high) number of six endopod articles. (G) The branchiopod Rehbachiella kinnekullensis Mü ller, 1983 with
the ventral food groove, autapomorph for Branchiopoda and used for feeding (Walossek 1993). Gray shad-
ing scheme is as described in Fig. 2.2. Abbreviations: bas, basipod; cox, coxa; en, endopod; ex, exopod; pe,
proximal endite. Repository numbers (see Fig. 2.1 for abbreviations): (C) YKLP 10859 (Zhang et al. 2007,
their fig. 1i–k); (D) UB W 310. All figures used with permission of the authors.
Often the coxal endite is called a gnathite and is even thought to serve for grinding or cutting.
At this early evolutionary stage, nothing of that kind is even remotely present. Equipped with
fine, setalike outgrowths distally, it is not capable of biting. This may even be a major misunder-
standing of arthropods in general when applying functional terms from other animals, such as
jawed vertebrates. An example is the molar surface of gammarid amphipods, which is made of
a large number of extremely soft, densely packed outgrowths. The molars act, for example, to
destroy the cells of diatoms or plants (Watling 1993), and they improve the ability to hold food
(Mayer et al. 2009, their fig. 3E,F; G. Mayer, personal communication). Plesiomorphically, the
antenna and mandible are very similar to each other (see Fig. 2.4I) (except for the tilted endite
surface of the mandibular coxa), and the spines and setae-bearing enditic protrusions of coxae
and basipods served to stuff food into the mouth (Labrophora are in a way “Di-Mandibulata,” as
Waloszek 2003b pointed out). Also, the distal elements are little different from the state before;
both limbs retain the multiannulated exopod for sweeping. This situation has even been retained
in all those eucrustacean taxa with a larval development that includes feeding nauplii/metan-
auplii (e.g., cephalocarids, mystacocarids, copepods, branchiopods). Slight differences between
the two appendages refer to the different positions and orientation along the body axis regard-
ing the mouth opening. While the posteromedially oriented antenna is inserting laterally to the
mouth, the mandible inserts posterolaterally, being orientated medially to anteromedially. Also,
the more posterior appendages appear to have remained largely unaltered in their gross morphol-
ogy; that is, they are serial and composed of four elements: proximal endite, basipod, endopod,
and (here) paddle-shaped exopod.
Even so, all postantennular limbs show another evolutionary novelty, clearly recognizable
in our material:
• A special arrangement of the spines and setae on the median enditic protrusions of the
proximal endite, the basipod, and likewise, all endopodal podomeres. This armature is
clearly different from that developed in all known stem derivatives and also all available
outgroups. It comprises basically one central spine and a set (crescentic row) of setae flank-
ing the spine anteriorly and posteriorly (e.g., Walossek 1993, Maas et al. 2003, Waloszek
2003b; Fig. 2.5A–C; for more details, see below).
Remarkably, at this level of Labrophora, all median structures of the appendages are rather similar
to each other, that is, the proximal endite, the basipod protrusion, and the mediodistal humps on
the endopodal podomeres. Despite these similarities, the proximal endite is often easily detect-
able. It is usually larger and better armed than the other enditic protrusions, and it is slightly ante-
riorly tilted (e.g., Walossek 1993, his plate 2–2). This tilting of the proximal endite against the axis
of the limbs can be almost 90°, as in triopsid branchiopods (Fryer 1988, his fig. 102). The enditic
origin remains visible even if the proximal endite is modified as in the mandibular coxal median
prolongation (e.g., in Figs. 2.4F, 2.5A), the so-called gnathobase—best seen in phosphatocopine
larval stages (see Maas et al. 2003, their fig. 65A for the antenna and fig. 66A for the mandible).
Another example of extreme modification is that of the maxillulae (or first maxillae) and maxil-
lae (or second maxillae) of eubranchiopods, which are nothing but the retained proximal endites
of the otherwise strongly reduced limbs (e.g., Martin and Cash-Clark 1995, their figs. 6, 11A–C,
Olesen et al. 2003, their fig. 9E).
The entire feeding apparatus of Labrophora may be regarded as a posteriorly open
food-path system, with the anterior appendages as much engaged in feeding and locomotion
as the posterior set that brought in food from the posterior along the interlimb space. The
more specialized appendages were located in the vicinity of the mouth. Here food could be
checked (chemosensed at rear of labrum; Waloszek 2003b, his fig. 3B), sorted, and directed
into the mouth by means of the strong enditic spines of antenna and mandible. As before,
the posterior feeding system works while moving, but the anterior system was decoupled
and could operate much more individually. During rotation of the limbs around their basal
joints, the limbs produced moving currents by their exopods as much as inwardly directed
food flow (even more so by the antennae and mandibles). From this, nutrients were raked off
and shoveled against the mouth. It is important to note that the basipod, at this level, possesses
only one major enditic protrusion and that the median edge was not subdivided into soft lobate
endites.
Within the Labrophora, phosphatocopines deviate from this in having significantly modi-
fied their postantennular limbs in at least two aspects (Fig. 2.3F):
• All endopods are basically three segmented (Maas et al. 2003; endopod of antennae and
mandibles may be only two segmented in ingroups); each article of the otherwise serial
postmandibular limbs is drawn out into long endites (Fig. 2.4E,H) (yet with the triplet of
setae as described above).
• Within the taxon, the endopods may be further modified from the ground pattern for spe-
cial feeding purposes as observed from isolated appendages from the middle Cambrian of
Australia. Here the endopod is involved in the formation of a kind of gnathic edge together
with the coxa and the basipod, comprising more or less a “whole-limb jaw” (Walossek et al.
1993, their fig. 3C).
• The mandibular basipod becomes progressively shorter and smaller during ontogeny until
it almost disappears, which gives the superficial impression of a coxa carrying the rami.
The fate of the basipod was documented at least for Vestrogothia spinata Mü ller, 1964 (Maas et al.
2003, their fig. 59A,C and plate 45A,B, Maas and Waloszek 2005, their fig. 2A,B). Eventually, the
basipod can no longer be recognized as a larger subtriangular unit carrying the two rami and is
nothing more than a separate setae-bearing endite below the proximal endopodal endite, while
the exopod seems to stem directly from the coxa (Fig. 2.4F; see Maas et al. 2003). This final mor-
phology is quite misleading because the basipodal endite seems very much like an endopodal
article and gives the appearance of three articles altogether, as in the endopods of all posterior
limbs and in the ground pattern of Phosphatocopina. The developmental sequence can be rec-
ognized only in intermediate (= younger) stages that possess a narrow ring around the exopo-
dal basis with connection to the median protrusion (Maas et al. 2003, their fig. 59C). Thus, it
becomes clear that coxa and basipod do not really fuse.
A number of phosphatocopine species also have multiannulated exopods on the postmandib-
ular appendages, for example, Vestrogothia spinata, Falites fala Mü ller, 1964, and Hesslandona
neocopina Mü ller, 1964 (Maas et al. 2003). In Phosphatocopina, the exopod morphology is
very special, because there are species that change during ontogeny from one morphology,
that is, multiannulated exopods on the posterior appendage series with inner setation, to the
other morphology, that is, paddle-shaped exopods with marginal setation (Maas et al. 2003 for
Hesslandona unisulcata).
Phosphatocopina are also a good model for the understanding of the ontogenetic change
of the proximal endite into a huge coxa with its median gnathic edge. Also, the armature, still
present in the earliest stages, is a nice reference for the recognition of the transition (see Fig.
2.5A). Lastly, Phosphatocopina also demonstrate the retention of the large excavation of the
proximal margin of a limb (Fig. 2.4F here referring to the coxal posterior side), as initiated in the
euarthropodium.
Appendages of the Eucrustacea
The ground pattern of Eucrustacea includes the four-element postantennular limb, with coxae
on the antenna and mandible as well as proximal endites on all posterior limbs (Figs. 2.2E,
2.3G). Some doubt remains regarding the development of the proximal endite into the coxa in
the antenna and mandible. Only a few taxa exhibit the morphogenetic change of a proximal
endite to a coxa on the mandible in very early larval stages, such as the Cambrian Rehbachiella
kinnekullensis, while the antenna clearly has a coxa from the beginning (Walossek 1993). It is
also difficult to determine the ground pattern of phosphatocopines, though it could be demon-
strated for one species from the lower Cambrian, Klausmuelleria salopensis Siveter et al., 2003
(Siveter et al. 2003, their text fig. 4). At present, we therefore favor the hypothesis that the mor-
phogenetic switch in the antenna occurred in the labrophoran ground pattern.
The only notable change concerning limb morphology in the ground pattern of Eucrustacea
seems to have affected the third postantennular or fourth cephalic limb, which from this evolu-
tionary level on is termed maxillula and may represent an autapomorphy of Eucrustacea:
• First postmandibular limb is dissimilar in morphology to the preceding and succeeding

limbs, functioning as a feeding aid.
The word seems is used to express our cautiousness, because the morphology of the maxillula
remains unclear. This is because (a) its shape differs between the two sister taxa Malacostraca
and Entomostraca (see below; examples given in Walossek and Mü ller 1998a, their fig. 12.11),
and (b) the maxillulary shape of these taxa differs significantly from that of the fourth limb of
phosphatocopines and that of “stem crustaceans.” Therefore, we cannot reconstruct a ground
pattern state for the morphology of the maxillula. We can only construct a ground pattern
state for its function because function is generally the same in all ingroup eucrustacean taxa.
What seems clear is only that the maxillula was already reduced in size compared to that of the
more posterior limbs. This situation can be seen in all known Cambrian Orsten taxa referred
to Eucrustacea, for example, Bredocaris admirabilis (Mü ller and Walossek 1988), Rehbachiella
kinnekullensis (Walossek 1993), and Yicaris dianensis (Zhang et al. 2007). (The same seems to be
the case in Dala peilertae and Walossekia quinquespinosa Mü ller, 1983, but detailed descriptions
of these are still under way.)
We also have difficulties reconstructing the morphology of the fourth postantennular or
fifth cephalic limb, traditionally called the maxilla. We can only clearly state that it was not a
“mouthpart”—a still repeated misunderstanding of crustacean morphology. It was included in
the head, and it was acting in accord with the trunk limbs, a plesiomorphic trait. So this holds
only for its feeding and locomotory duties in the ground pattern of Eucrustacea. Clearly, the
maxilla at that level did not have the morphology of previous levels, as we learned for other limbs
and for earlier nodes. And it is also not a mixture of the morphology of ingroup maxillae, but the
maxillae have adopted the specific trunk-limb morphology of one of the two sister taxa within
Eucrustacea. As discussed below, these limbs are also very differently developed, in terms of
specific changes in the locomotory and feeding apparatus and tagmotic changes, for example, in
the Malacostraca. For both maxilla and the trunk limbs, we cannot state that the malacostracan
morphology should be plesiomorphic, but we cannot state this for the entomostracan morphol-
ogy either. Likewise, it is difficult to argue that entomostracans are a paraphylum “along the evo-
lutionary lineage toward Malacostraca” because this would intimately violate the data around
limb morphology.
The retention of the maxilla within the posterior limb system appears plesiomorphic, while
the specific similarity in shape, flatness, and softness of the maxillula and maxilla in malacostra-
cans only adds to the large number of other autapomorphies validating this monophylum. The
condition that the maxilla has a trunk-limb morphology is developed in several Cambrian fos-
sil eucrustacean taxa such as Bredocaris admirabilis, Dala peilertae, Rehbachiella kinnekullensis,
Walossekia quinquespinosa, and Yicaris dianensis, and in extant cephalocarids (e.g., Sanders 1957,
1963). It may hence be likewise interpreted as a specific feature of Entomostraca and not as an
ancient trait.
All more posterior appendages remain basically unaltered in their gross morphology. They
are serially homonomous and composed of the proximal endite, the basipod, the endopod, and
the paddle-shaped exopod (= euarthropodium + proximal endite). It appears likely that epipods
on these limbs belong to the ground pattern of Eucrustacea, but their number remains uncer-
tain, being three in Entomostraca and no more than two in Malacostraca. Their exact origin
also remains unclear at the moment (Maas et al. 2009). (For a discussion of the second autapo-
morphy, the ontogeny via a short-segmented [ortho]nauplius, see Maas et al. [2003].)
Lastly, it must be stressed that coxa and proximal endite exclude each other because a coxa,
as far as we can state at present, originates from this endite below the basipod. The joint between
coxa and basipod originates from the fact that the proximal endite lies embedded within the
proximal limb joint membrane. When the coxa develops, the distal portion of the membrane is
simply retained between the final sclerotic stem portions.
Different Evolution of Limb Morphologies in Entomostraca and Malacostraca
The appendages remain more or less unchanged in the ground pattern of Eucrustacea, but
substantial further evolutionary modifications of them occurred in the evolutionary lineages
of the two sister taxa. This is fully understandable since all branchings mentioned so far, and
possibly even a few more already on the lines of the two sister taxa, had already occurred in the
Cambrian. The others had, accordingly, another 500 million years to make changes. Significant
differences in appendage morphology already in the ground patterns of Entomostraca
(Fig. 2.3H) and Malacostraca (Fig. 2.3I) indicate that, as in the maxillulae and maxillae, it is often
difficult to reconstruct well-founded ground pattern states, because the differences between the
taxa to be compared are not traceable down to a common ancestral morphology.
Up to now, only the evolution of Entomostraca has been documented (as we think) by
well-preserved Cambrian fossils in Orsten-type preservation, for example, Yicaris dianen-
sis (Zhang et al. 2007, Fig. 2.1G,H), Bredocaris admirabilis (Mü ller and Walossek 1988), and
Rehbachiella kinnekullensis (Walossek 1993; see Fig. 2.5D,E for comparison with an extant bran-
chiopod). The early phase of malacostracan evolution, in contrast, is still completely unknown.
The earliest reliable malacostracan fossils occur in the Lower Ordovician, and even the status
of these so-called phyllocarids must be considered uncertain at best: living representatives of
phyllocarids, having leaf-shaped limbs in the anterior thoracic portion (thorax I after Walossek
and Mü ller 1998a), are indeed very different from the well-sclerotized large fossil forms possibly
having rather stenopodial limbs.
This bias may have led to the impression of a “well-defined” taxon Malacostraca
(admittedly the two-section thorax region present in all living taxa is a striking feature),
while entomostracans seem to express—another misunderstanding—“morphological insta-
bility as an expression of plesiomorphy,” because their ingroup taxa exhibit very different
morphologies. In fact, this is exactly their “trick.” The high number of autapomorphies of the
Malacostraca in its ground pattern means nothing but the result of a long, though unknown,
evolutionary lineage in which these characters have been accumulated. These are assigned
now to the last common ancestor of all descendants with living representatives. The morpho-
logical conservatism of Malacostraca may then just be the retention of plesiomorphies, not
expression of evolutionary success.
The bias also results, in our opinion, in the superficial view that Entomostraca should have
retained more plesiomorphic traits than the malacostracans (the often-used terms lower and
higher crustaceans reflect this interpretation) and hence should not be monophyletic. Indeed,
some body parts retained plesiomorphic traits, such as the anterior appendages. Antennular and
antennal morphologies of malacostracans are easily identified as their evolutionary novelties,
while Entomostraca apparently retained a plesiomorphic appearance of these two append-

ages. However, all further posterior appendages underwent significant evolutionary changes in
both lineages, and in both, the morphology of these limbs deviates from the ground pattern of
Eucrustacea or Labrophora. This can even be stated for the mandibles, which lose their basipod
plus the rami during the ontogeny in entomostracans, and for the maxillulae and maxillae as
well. Accordingly, many features in the stem species of Entomostraca and Malacostraca, as far
as they can be reconstructed, can be well understood as modifications in accordance with adap-
tations to specific life habits achieved in each group separately. This makes any evolutionary
transition from the one to the other morphology unlikely; that is, in these cases, the features
represent autapomorphic states of the two taxa.
Therefore, we view the assumption of a paraphyly of Entomostraca, as commonly proposed
(see Waloszek 2003b for discussion), to be improbable and less parsimonious and uphold the
hypothesis of their monophyly. One area of evidence for this is the specific morphology of
appendages, which is detailed next.
Anterior Cephalic Appendages
The antennula of adult malacostracans comprises a prominent tubular basal part and two distal
flagella (three in some taxa) and has sensory function. Only in the nauplii of Euphausiacea and
Dendrobranchiata (the only malacostracan taxa with free-living nauplius larvae) is the anten-
nula uniramous and limblike as in their ancestors; it even bears a number of long swimming
setae on its distal end (e.g., Hirota et al. 1984a, 1984b, Kidd 1991). Thus, it appears that in these
early larvae the antennula recalls at least part of its original state. The original functions of the
antennulae, swimming and helping in sweeping in food particles, may have been abandoned
early during evolution and ontogeny. Nauplii of these groups only swim and do not feed; having
no feeding aids at all may even point to a very early loss and change to lecithotrophy. This loss
may have been in line with the modification of the other appendages taking these functions over
later during development, that is, from the protozoea onward.
Similarly, a plesiomorphy exposed in larvae is recognizable in the antenna of Euphausiacea
and Dendrobranchiata (e.g., Cockcroft 1985 for the penaeid Macropetasma africanum Balss,
1913, Maas and Waloszek 2001b for the Antarctic krill Euphausia superba Dana, 1852). The mor-
phology is very similar to that of feeding entomostracan nauplii, but those of malacostracan
taxa lack any median feeding structures because they do not feed. Later in ontogeny the anten-
nal endopod is transformed into a sensorial “feeler” with a long multiannulated flagellum, and
the exopod becomes the paddle-shaped “scaphocerite” (e.g., Maas and Waloszek 2001b for E.
superba as an example of euphausiids). Lastly, the naupliar mandible of malacostracans with
early larvae is very similar to those of early larval entomostracans, including coxa, basipod,
and two rami. The retention of the parts distal to the coxa, called palp in later stages and the
adult, may be plesiomorphic, but this uniramous palp is only remotely similar to the original
condition of the Eucrustacea. The adult palp consists of three articles interpreted as basipod
and the bipartite endopod (see, e.g., Olesen and Walossek 2000). The morphology of the palp
is remarkably similar in all known ingroup taxa and clearly represents an autapomorphy of
Malacostraca.
In Cephalocarida, Branchiopoda, and, as the ontogenetic path suggests, most likely in a
number of Orsten species, such as Yicaris dianensis, Rehbachiella kinnekullensis, and Walossekia
quinquespinosa, all parts of the mandible distal to the coxa are lost during ontogeny. This condi-
tion is considered an autapomorphy in the ground pattern of Entomostraca. We thus understand
the presence of a palpus in Maxillopoda as resulting from a pedomorphic event in their evolu-
tionary history (e.g., Newman 1983, Walossek and Mü ller 1998a, Waloszek 2003b).
The situation of the exopods of antennae and mandibles is more complicated. In entomo-
stracans, they may retain their multiannulated morphology (e.g., cephalocarids, some maxil-
lopodans), be modified (some phyllopod branchiopods), or become lost (some maxillopodans,
anostracan branchiopods). Immature stages retain the original morphology in all taxa. In
Malacostraca, the larvae—where developed—have multiannulated antennal exopods, but
in adults the exopod has at most two parts and is flattened, that is, the scalelike scaphocerite.
Furthermore, these appendages can undergo high modification or complete loss in particular
ingroups, but mostly entomostracans. Examples are the tantulocarids (all cephalic appendages),
facetotectans (antenna, mandible), and cirripedes (antenna).
Not only do the maxillulae of Malacostraca and Entomostraca differ significantly in
their morphologies, but they also differ from the equivalent limb in the Phosphatocopina
and stem derivatives. The homotope, that is, the positional homologue, of the maxillula in
Phosphatocopina is still serial to all more posterior appendages and consists of a lobate proximal
endite, a basipod with one median endite, and the rami (Maas et al. 2003). In both Malacostraca
and Entomostraca, the maxillula is developed as a further “mouthpart” and differs in morphol-
ogy from the more posterior appendages. The malacostracan maxillula is uniformly rather thin
and has a slight C-shape (concave anteriorly) and a proximal endite modified into a coxa. Both
coxa and basipod are medially drawn out into one blade-shaped enditic process with a rim of
spines or setae. Both maxillula and maxilla are similar and act as a unit behind the mandible,
closing the food chamber posteriorly. In the ground pattern, the entomostracan maxillula has
a proximal endite and three more setose endites along the median edge of the basipod (not
one as in phosphatocopines or stem derivatives). This state is realized in copepods, in mysta-
cocarids, and in cephalocarids during the larval phase. In the stem-branchiopod Rehbachiella
kinnekullensis it occurs until the latest instar stage known, and it is also developed in, for exam-
ple, the Orsten taxa Yicaris dianensis (Zhang et al. 2007), Walossekia quinquespinosa (unpub-
lished), and Bredocaris admirabilis (Mü ller and Walossek 1988). Crown-group branchiopods
(Eubranchiopoda) have reduced maxillulae and maxillae retaining only their proximal endites
(see Walossek 1993).
In summary, the maxillulae have a different fate from that of the maxillae in entomostracans
but are both fully integrated and acting together in a cephalic feeding system in malacostracans.
There they are rather similar to each other, and both have a coxal portion below the basipod.
Only in cephalocarids among the living entomostracans does the maxillula serve as a single
“mouthpart,” while the maxilla is a trunk limb. In all other taxa, the situation is different. In
the extreme, maxillula and maxilla are almost lost (eubranchiopods) or completely lost (para-
sitic tantulocarids). Remarkably, the maxillae retain a paddle-shaped exopod in all taxa where it
remains developed—and there is no exception throughout.
Postmaxillulary Appendages
In Malacostraca the maxilla is much flattened in anteroposterior aspect, in this way looking much
like the maxillula. It is also C-shaped (anteriorly concave), and its proximal endite forms a coxa.
Coxa and basipod are medially drawn out into bladelike spine- to setae-bearing protrusions, but in
contrast to the maxillula, they have a median cleft, so they appear divided in two. Both maxillulae
and maxillae have a very soft and fragile appearance and are considerably shorter than all subsequent
limbs of the trunk. These postcephalic trunk appendages of Malacostraca not only are different
from the maxillae but also cannot easily be discussed because (1) they occur in two very distinctive
sets, and (2) they are rather different in the two sister taxa Phyllocarida and Eumalacostraca. Only
the first eight thoracic limbs (of thorax I according to Walossek and Müller 1998a) have a limb stem
made of a coxal and basipod portion, but the so-called pleopods (limbs of thorax II sensu Walossek
and Müller 1998a) have neither a coxa nor a proximal endite.
The anterior eight thoracopods of phyllocarids are flattened and appear very superficially
similar to the filter appendages of Branchiopoda—though virtually all details are differ-
ent, the feeding system is a closed one, phyllocarids do not filter feed in the strict sense (see
Walossek 1993 for detailed comparisons), and they have fairly large coxae and basipods, from
which an elongate endopod and a paddle-shaped exopod arise. The first four pleopods have a
rod-shaped basal part, which carries two rami of equal size immediately on its top (e.g., Olesen
and Walossek 2000, their fig. 7b). Pleopods 5 and 6 are small and consist only of an elongated
lobe. The eight anterior thoracopods of Eumalacostraca have fairly short coxae and basipods
but likewise elongate endopods. The exopods are nowhere prominent except in euphausiids
and may be small paddles (e.g., Maas and Waloszek 2001b, their fig. 11) or multiannulated rods
stemming from a proximal peduncle piece (e.g., Neil et al. 1976, their figs. 3a, 5c, 9)—the slop-
ing articulation area of the exopod recalls the original morphology taken over from the euar-
thropodium. As in Phyllocarida, eumalacostracan pleopods lack a coxa or a proximal endite,
and also their rami rest on top of the stem portion. The variety of morphologies of the rami is,
however, large.
The maxilla in the ground pattern of Entomostraca is, on the other hand, very different
from the morphology in the maxilla or trunk limbs of malacostracans—and it matches that of
the series of posterior limbs (Fig. 2.3H). In size and morphology, it virtually equals the trunk
limbs at this stage. Its proximal endite is prominent, possibly the largest of all postmaxil-
lulary limbs, and in its setation grossly similar to that developed in Phosphatocopina. The
basipod is a large subrectangular element, longer than wide. Its mediodistal extension forms
a kind of socket for the transition to the endopod and a sloping distal outer margin from
which the exopod is articulated. Its straight median edge is drawn out into several lobate
setiferous endites (Waloszek 2003b). Their armature resembles that of the proximal endite
but is progressively less elaborate. The basipod body is fairly f leshy and little sclerotized,
with the exception of the lateral edge proximal to the exopod insertion, which is slightly
better sclerotized but interrupted by two furrows, giving this side a tripartite appearance
(Fig. 2.6F,G). For the extant cephalocarids (see Fig. 2.6B), it is clear that the proximal endite
and the endites along the inner rim of the basipod have muscles internally and can be moved
accordingly (Sanders 1963, Hessler 1964). It is possible that, as the preservation of endites in
Rehbachiella kinnekullensis and other such Orsten eucrustaceans suggests, the movability
was a particular feature of these endites already in the ground pattern of Entomostraca and
an additional autapomorphy. In those taxa where the basipod rims are more or less straight,
more rigid, and adorned with rows of setae, this would be a secondary adaptation in line with
somewhat modified food intake.
The endopod appears to be the direct continuation of the basipod. Not only do its proxi-
mal podomeres match the shape of the distal enditic protrusions of the basipod, but also the
setation pattern is continued, again being less and less developed toward the distal end. The
endopod is maximally six segmented in Eucrustacea and ends in a much smaller distal conelike
to caplike piece with a terminal tuft of setae or spines. The exopod is paddle shaped with a mar-
ginal row of long setae. This entire morphology matches that of the subsequent limbs and is
developed in this way not only in certain Orsten taxa (Yicaris dianensis, Rehbachiella kinnekul-
lensis, Dala peilertae, and Bredocaris admirabilis; see Mü ller 1983, Mü ller and Walossek 1985,
1988, Walossek 1993, Zhang et al. 2007) but also in the extant Cephalocarida (e.g., Carcupino
et al. 2006, their fig. 4A).
Although this type of appendage does not match that of any of the known stem derivatives,
phosphatocopines, or malacostracans (which have a coxa in the maxilla and anterior eight tho-
racopods), we can find here a mixture of plesiomorphies and apomorphies present on a sin-
gle structure. In terms of seriality, the maxilla in the ground pattern of entomostracans (and
ingroups!) is similar, that is, homonomous, to the more posterior limbs. In other words, it is not
included into a specific cephalic feeding and locomotory apparatus, so it can be termed maxilla
in the strict sense.
Superimposed on this plesiomorphy are other, autapomorphic features, such as a subdivi-
sion of the median edge of the basipod into several setae-bearing lobate endites (up to seven
in Yicaris dianensis; see Zhang et al. 2007). The same applies to the more posterior append-
ages, the thoracopods, in Entomostraca (up to eight basipodal endites in Yicaris dianensis; see
Zhang et al. 2007). Furthermore, the otherwise transversely inserting basipods of all post-
maxillulary appendages are elongated in proximodistal and lateral axis and are rather f leshy
and slightly C-shaped curved backward, so the posterior side is concave. In cephalocarids this
special morphology forms narrow chambers between the limbs in the row. These are opened
and closed during the moving cycle (heterochronal beat) of the limbs pressing out water or
sucking it in during opening. The system of pumping chambers is known from these and
other eucrustaceans but is studied in more detail in anostracan branchiopods, which filter
feed (Fryer 1983), a habit not applicable to cephalocarids (Walossek 1993). Suspension feeding
is widespread among the Crustacea and is not discussed here any further (for more details,
see chapter 8).
Yet, for both taxa it is known that the system has two functions: feeding and locomotion.
Moreover, it requires the open system, as noted for the Labrophora level. Maxillae forming a
chamber as in Malacostraca is, however, a very different operational system. Also, maxillae and
a so-called maxilliped operating as a closed feeding system, as in copepods, can be set off, but
since this condition occurs in ingroup entomostracans, this system is derived from the open ento-
mostracan type. A similar system with fleshy basipods has also been reconstructed for Orsten
entomostracans such as Rehbachiella kinnekullensis and Yicaris dianensis, so it may have operated
similarly. The differences in detail (setae, subsetules, endite form, etc.) not only point to differ-
ences in feeding and locomotion but also may indicate different development in different evolu-
tionary lineages.
The basipodal endites of all postantennular appendages are, as mentioned above, equipped
with setae and spines. These occur in a pattern of three different rows of spines/setae, similar
to that of Phosphatocopina (ground pattern of Labrophora). However, while the anterior and
posterior sets of setae on the enditic protrusions are still undifferentiated in Phosphatocopina
(Fig. 2.5A), in Entomostraca the setae are differentiated both in structure and arrangement into
anterior retention setae with rows of more backward oriented setulae, median stronger spines,
and posterior setae, which have rows of anteriorly pointing setulae (Fig. 2.5B,C), each set form-
ing a small basket. The specific morphology and the so-called sucking chambers between the
limbs enable the animals to feed and locomote at the same time using the entire postmaxillulary
apparatus (Walossek 1993), as seen today in cephalocarids and branchiopods. This morphology
was most likely modified again in Maxillopoda.
The tripartite set of setae develops ontogenetically through a two-part set, as exemplified
by Rehbachiella kinnekullensis (Walossek 1993). This ontogenetic change from a two-row to a
three-row system can also be observed in Yicaris dianensis (Zhang et al. 2007). The presence
of a two-row system in Maxillopoda, such as in Bredocaris admirabilis (Mü ller and Walossek
1988), can thus be understood as another effect of pedomorphosis that affected Maxillopoda
(Newman 1983, Walossek 1993).
None of these special changes of the basipods can be found in Malacostraca. There the
maxilla is indeed developed as a specialized mouthpart in the ground pattern of this taxon,
more or less an aid to close the oral chamber. The maxilla is extremely f lat, similar to the max-
illula, and the proximal endite is also enlarged to form a coxa. Coxa and basipod are medially
drawn out into two (not just one) bladelike protrusions each. In both maxillula and maxilla,
the endopods are most likely subdivided into at least three articles in the ground pattern of
Malacostraca, as exemplified by the euphausiacean Bentheuphausia amblyops G.O. Sars, 1883
(see Maas and Waloszek 2001b). These limbs differ from those of the Entomostraca also in
that they surround the mandibles like hands held over the mouth. Accordingly, this apparatus
is a closed system, whereas that of entomostracans is an open system.
Basipods of more posterior limbs in Malacostraca may carry setation but do not have lobate
endites (Fig. 2.6A,E). It has to be noted here that the appendages of the Silurian fossil phyl-
locarid Cinerocaris magnifica Briggs et al., 2004 have been interpreted as possibly possessing
endites (Briggs et al. 2004). Unfortunately, the appendages of this species have been presented
as two-dimensional line drawings (Briggs et al. 2004, their fig. 2i) and not, as usual for this pres-
ervational type, as three-dimensional reconstructions (see, e.g., Siveter et al. 2007). It is there-
fore impossible to verify the presence of any enditic subdivision of the basipods of trunk limbs
in Malacostraca. Consequently, based on the existing data, a proximodistally elongated basipod
with lobate setae-bearing enditic subdivisions of the narrow median edge is regarded here as an
autapomorphy of Entomostraca (Fig. 2.6B–D,F,G; Waloszek 2003b).
Malacostraca possess further specializations on their postmaxillary appendages, namely,
in their division into two series, eight belonging to the first part of the thorax (thorax I sensu
Walossek and Mü ller 1998a) and six so-called pleopods belonging to the second part of the tho-
rax (thorax II or pleon) in the ground pattern. Only thoracopods 1–8 appear to bear a true coxa;
that is, the proximal endite is laterally enlarged to form a complete enclosed sclerotized ring
(Waloszek 2003b). The presence or absence of a coxa or proximal endite could not be shown
with certainty in any malacostracan so far. Another evolutionary modification that cannot
be followed up here in more detail, however, is the specialization of one or even more limbs
as mouthparts, so-called maxillipeds. This feature, possibly even convergently developed, is a
gradual process and does not change the general functionality of the closed oral chamber, but
just adds the next limb—for example, as a food grasper or holder—to form a larger unit. The
trunk limbs progressively lose their ability to provide assistance in food intake, a trait that is
still recognizable in phyllocarids and at least distally in the case of the basket-feeding euphausi-
ids (Hamner 1988). It should be noted that similar strategies occur in entomostracans, where a
closed oral feeding chamber including maxillipeds exists, and the remaining thoracopods are
devoid of feeding structures and function.
Summing up regarding limb morphology, the following features are interpreted as autapo-
morphies of Malacostraca:
• Mandible with a typical tripartite palp (basipod and two endopod elements)
• Maxillula with a coxa; coxa and basipod each with a bladelike endite
• Maxilla with a coxa; coxa and basipod with two endites each
• Trunk limb series divided into two special series (thorax I and II of Walossek and Mü ller
1998a) of eight anterior and six posterior pairs of appendages; appendages of the anterior
series with coxae
Limb-related autapomorphies of Entomostraca include the following:
• Mandible loses palp late in ontogeny

• Maxillula with proximal endite and with basipod bearing three endites
• Basipod of “maxilla” (not specialized as a mouthpart) and all trunk limbs elongated in
proximodistal axis of the limb, medially equipped with a series of endites (seven to eight
originally?); basipod laterally subdivided into three major parts; setation on the endites
organized in three sets of setae specialized for sorting of food particles anteriorly and
retention setae posteriorly (orientation of subsetules different)
VARIATIONS ON A THEME: LIMB MODIF ICATIONS
The two rami of an appendage, endopod and exopod, are modified and specialized in many
ways in the various eucrustacean ingroup taxa; in the extreme, they are completely lost. In the
following we give a number of examples for different morphological variations of the two rami.
This is, however, a limited set since the morphological variation is very extensive within such a
large taxon as the Crustacea.
Endopod Variations
The crustacean endopod plesiomorphically has a simple tubelike shape with setae or spines on
mediodistal humps along the inner margin (one such hump per podomere) and a setiferous to
spine-bearing tip, possibly an adaptation for food gathering and locomotion (much retained
from the euarthropod ground pattern; see above). Alterations occur in various ways. On the one
hand, the endopod can be, very rarely, partially reduced to a simple bulbous structure within
Eubranchiopoda (Olesen et al. 2001). (Another example outside Crustacea is the endopod of
the second head appendage of Agnostus pisiformis [see Mü ller and Walossek 1987, their fig. 6B
and plates 12.5, 16.1].) Reduction in size of the endopods and/or of their segmentation in liv-
ing branchiopods led some authors to (among other errors) misidentify the basipodal endites
as endopod podomeres of the according appendage (e.g., Wehner and Gehring 1995, caused by
Preuss 1957; for correction, see Walossek 1993).
On the other hand, the endopod may become elongated by its podomeres, the number of
which stays the same. This occurs, for example, in the thoracopods 1–8 of Eumalacostraca, and
there even the whole limb may become stenopodous by parallel reduction of the coxa and basi-
pod as well as the reduction or even loss of the exopod (walking legs). This is also independent
of the numbers in toto: an endopod made of one or two portions may be as large as others with
more portions. Because of this it is extremely difficult to identify functional or evolutionary
adaptations. As hinted at before, each limb has to be viewed separately and in the context of the
other limbs.
Another specialization is that endopod tips may become subchelate or chelate in various
lineages, for example, in Stomatopoda (Morgan and Goy 1987), Peracarida (tanaidaceans or
amphipods), and Decapoda (Richter and Scholtz 2001). Also within Entomostraca, endopods
with a subchelate tip may be found, such as in the form of claspers of males to attach to the
females—examples are the first trunk limbs of certain diplostracans (e.g., Olesen et al. 1996)
or the antenna of Anostraca (e.g., Dumont and Negrea 2002, their fig. 130I). It is apparently
evolutionarily possible even to change the endopod morphology from one extreme (partially
reduced endopod) to the other (elongated stenopodous endopod), as proven by the raptorial
water fleas within Cladocera. In the ground pattern of Cladocera, the thoracic endopods are,
as in the ground pattern of Eubranchiopoda, simple undivided bulbs (Olesen 2004, 2007).
Within Onychopoda and Leptodora kindtii Focke, 1844, the whole anterior thoracic appendages
are elongated into multisegmented stenopodia to fulfill raptorial functions (Olesen et al. 2001,
2003; Fig. 2.7F). The endopod may also become a paddle-shaped structure for swimming (see
“Symmetries in the Morphology of the Rami,” below).
Although partial reduction is possible, a complete loss of the endopod is quite unusual
within eucrustaceans. Often only the loss of the entire appendage also permits the endopod
to be missing as in the pleopods of various interstitial peracarids, or the loss of the distal part
of the appendage including the basipod such as in branchiopod mandibles. Investigation of the
ontogeny of, for example, the Cambrian branchiopod Rehbachiella kinnekullensis, in which the
mandible is complete in early stages (Walossek 1993, his plate 4–1), reveals that the distal part,
Fig. 2.7.
Variations of biramous crustacean limbs. (A and B) The branchiopod Lepidocaris rhyniensis Scourfield,
1926. Images show a maximum intensity projection; that is, images of different focal planes are combined
(for details, see Haug et al. 2009b). Arrows indicate exopods of adjacent limbs. (A) Anterior postmandib-
ular appendage in anterior view. Exopod and endopod differ strongly in their morphology and in their
insertion angle and position on the basipod. (B) Posterior postmandibular appendage in posterior view.
Exopod and endopod are rather symmetric morphologically and in their insertion position and angle on
the basipod (“copepod-like”). (C) Thoracopod of Lepas sp. Linnaeus, 1758 (Cirripedia). Endopod and exo-
pod (cirri) are morphologically indistinguishable (arrows); only their position in the living animal shows
their identity. Image not to scale. (D) Tail fan of the Jurassic stomatopod Sculda pennata Mü nster, 1840.
The uropodal exopod is a simple undivided paddle. (E) Tail fan of the extant stomatopod Squilla mantis
Linnaeus, 1758. The uropodal exopod is divided into a distal paddle and a proximal article. (F) Ventral view
on a late embryo of the phyllopod Leptodora kindtii Focke, 1844. Arrows mark the second and third tho-
racopods, developed as stenopodous limbs with median setation, whereas the ground pattern of phyllopod
branchiopods is characterized by leaf-shaped limbs. (G) Second antenna of the branchiopod Macrothrix
laticornis Jurine, 1820. Exopod and endopod are symmetrically composed of three tubular elements. (H)
Thoracopod of an undetermined copepod. Endopod and exopod are symmetrically composed of three
setose anteroposteriorly flattened elements. Image not to scale. Abbreviations: bas, basipod; cox, coxa;
dex, distal paddle of exopod; en, endopod; ex, exopod; pex, proximal article of exopod. Repository num-
bers (see Fig. 2.1 for abbreviations): (A and B) BM 25698; (D) MB.A.669.
the “palp,” of the appendage becomes progressively smaller. Finally, a small round scar marks
the original insertion of the palp, but the appendage consists solely of the coxa (Walossek 1993,
his plate 17–4). One of the rare examples of complete endopod loss in Eucrustacea is the degen-
eration of the posterior two thoracopods within Euphausiacea. The gill in these two appendages
is the most prominent structure. A coxa-basipod subdivision is not identifiable; a uniramous
structure with marginal setation is identified as exopod, while an endopod is lacking (see, e.g.,
Maas and Waloszek 2001b, their fig. 13).
Exopod Variations
The exopods, often referred to as the swimming branches (e.g., Calman 1909), also exhibit
a wide variety of morphologies in the different eucrustacean taxa. As mentioned above, in
Eumalacostraca, the antennal exopod is a two-part paddle that is reduced even further to a
simple undivided paddle in Caridoida (Richter and Scholtz 2001; caridoids are the sister group
to stomatopods). While exopods are paddle shaped in the maxillulae and maxillae where
developed, they are multiannulated on the first eight thoracopods of various taxa within the
Eumalacostraca. There the exopod is highly movable and is used for locomotion—for exam-
ple, in larvae of lobsters (Neil et al. 1976) or in mysid peracaridans, where it may move at
high speed to keep the animal in position like a helicopter (the German name Schwebegarnele
refers to this). In certain entomostracan taxa, the exopod is subdivided into several articles,
often three, as in the trunk limbs of Copepoda and Remipedia (Itô 1982, 1989), but this is
unlikely to be a hint to relationships but merely a functional enforcement to achieve a more
f lexible paddle. Another example of the appearance of an additional joint in an exopod is the
uropodal exopod of some Eumalacostraca, for example, the Stomatopoda. All extant species
of Stomatopoda have a bipartite uropodal exopod (Fig. 2.7E), but a number of fossil species
demonstrate that this condition is most parsimoniously derived from a simple undivided exo-
pod (Schram 2007; Fig. 2.7D).
The exopod has become more subject to loss than the endopod, both during evolution and
during ontogeny. This is most evident in all land-living bottom-walking crustaceans, as well as
in other euarthropods such as arachnids, myriapods, and insects. But this also holds true for
limbs of benthic walkers in the marine environment such as thoracopods 4–8 of Eureptantia
among the decapod Malacostraca (not the anterior thoracopods 1–3, which are modified into
the maxillipeds, specialized limbs that support feeding) or all isopods, in both cases an autapo-
morphy of these taxa, or outside crustaceans in the pantopod Chelicerata (already observa-
ble in fossils from the Devonian; Bergström et al. 1980). Exopod loss in nonlocomotive limbs
can be recognized, for example, on the mandibles of land-based isopod peracarids among the
Malacostraca (so clearly convergent to Entomostraca) or on the maxillulae and maxillae of
Mystacocarida (species of the taxon Ctenocheilocaris Renaud-Mornant, 1976 also lack the exo-
pod on the maxilliped) and Copepoda (unclear if this hints at a close relationship).
We consider these true losses, not a lack of subdivision of exopod and endopod. The idea of the
loss of exopods through a lack of subdivision of exo- and endopod (and thus the remaining “endo-
pod” being a homologue of former endopod and exopod) has been concluded from the results of a
cell lineage investigation of an amphipod (Wolff and Scholtz 2008). It appears to be unfounded to
expand this putative mechanism, which is interpreted to exist in a highly derived ingroup malacos-
tracan taxon, to all Crustacea, or even Arthropoda. This also contradicts all data accumulated that
depict the evolutionary path from the lobopodium to the arthropodium and euarthropodium and
eventually the crustacean limbs, as we explained it here. Even though the cell lineage data may indi-
cate that the walking limbs of the pereopods are the result of “undivided” branches, the structural
similarities to the endopods of other malacostracans and the endopod origin from the distal part of
the limb stem in Arthropoda s. str. clearly reject this assumption (for discussion, see also Boxshall
and Jaume 2009). Other Crustacea also gain uniramous appendages through loss of exopods. In the
mystacocarid species of the taxon Derocheilocaris Pennak and Zinn, 1943, for example, the maxillula
and maxilla appear very similar to the maxilliped—except that the maxilliped possesses an exopod.
Therefore, it appears to be much more parsimonious to assume a simple loss of the exopod in max-
illula and maxilla than to homologize their endopods with both rami of the maxilliped.
Symmetries in the Morphology of the Rami
Despite their clearly different phylogenetic origin, the two rami, endopod and exopod, can
be almost identical or symmetrical in certain eucrustacean taxa. There they even serve the
same functions. Examples of such symmetrization of rami can be found in various taxa and
on different appendages—clearly an example of convergence. Some examples of this are the
“cirri” (endopod and exopod) of the thoracopods of adult barnacles (Fig. 2.7C) and, within the
Branchiopoda, the antennae of Diplostraca. These bear two very symmetric rami, best known
probably from Cladocera (= “branched horns”; i.e., the taxon name established by Pierre André
Latreille in 1829 even refers to this symmetrization), including one of the standard laboratory
organisms in student courses, Daphnia pulex De Geer, 1778. Both endopod and exopod comprise
three articles, with the proximal articles carrying a single median seta each and the terminal
article carrying a number of setae concentrated medially (Fig. 2.7G). All these similar-appearing
setae are long and setulose and mainly serve as swimming devices.
Another example of symmetrization of rami is Lepidocaris rhyniensis Scourfield, 1926, a
putatively branchiopod species from the famous Early Devonian Rhynie Chert lagerstätte in
Scotland (Scourfield 1926). The anterior trunk appendages exhibit clearly differing morpholo-
gies in the endopod and the exopod (Fig. 2.7A). But in the series of posterior trunk appendages,
the so-called copepod-like appendages, both rami appear very similar. They are developed as
simple paddles with seven to nine setae along their whole margins (Fig. 2.7B). Symmetrization
in this case affects not only the shape of the two rami but also their insertion at the basipod—
both rami insert distally. In the anterior trunk appendages, the exopods insert laterodistally
(Scourfield 1926). The morphology of these posterior limbs has been interpreted as an adapta-
tion to swimming.
As the terminology in Lepidocaris rhyniensis (“copepod-like” appendages) already indicates,
copepods also have symmetrical rami on the posterior trunk limbs. Unlike in L. rhyniensis, the
endopod and exopod are not simple paddles but are more elongated and comprise three arti-
cles (Fig. 2.7H). Even so, endopod and exopod have a very similar appearance. A comparable
morphology of the two rami as symmetric elongated paddles with three articles on the trunk
appendages is also found in Remipedia (Itô 1989).
Also, in various malacostracan taxa, appendages with symmetrical rami occur. The pleopods
of Eumalacostraca are one example. In Stomatopoda the endopods and exopods of the pleopods
(limbs of thorax II sensu Walossek and Mü ller 1998a) are developed as symmetrical paddles
bearing a large number of setae along the whole margin. Yet, the symmetry is partly interrupted,
as the exopod carries gills on its anterior side (Morgan and Goy 1987, Maas et al. 2009).
Seriality of the Limbs and Tagmatization
Changes to the appendage morphologies can affect single appendages or complete series and
can be coupled to tagmatization pattern changes, but need not. For example, the inclusion of
further appendages into a specialized feeding apparatus is not necessarily linked to the inclu-
sion of the corresponding segments into the head tagma. There are, on the other hand, examples
of the inclusion of segments into the head tagma with unmodified appendages, that is, append-
ages that look exactly like trunk appendages, as it is reconstructed for the eucrustacean ground
pattern and also exhibited by extant cephalocarids. Also, the reverse case can be found, where
an appendage is distinctly evolved into a specialized feeding apparatus, while the segment is
dorsally clearly set off from the head tagma. This can be seen in the Copepodoida. The autapo-
morphy of this taxon comprising, in our view, the Copepoda, the tiny interstitial Mystacocarida
and the Cambrian Skaracarida is a special cephalothoracic feeding apparatus with one maxil-
liped involved. The maxilliped segment is incorporated in the cephalothorax in copepods; that
is, its dorsal surface is included into the shield. In Skaracarida and Mystacocarida, the segment
is set off dorsally: it is movable against the head (Walossek and Mü ller 1998b).
Stomatopoda possess a feeding apparatus, which involves five postmaxillary maxillipeds.
The posterior four maxillipeds are arranged in a highly condensed area on the ventral surface.
Nevertheless, the fifth maxilliped indeed belongs to an extra segment, which is not included
into the cephalothorax and which possesses an extra tergite (e.g., Ahyong 2001). Research in
developmental genetics has supported this long known morphological phenomenon: dorsal and
ventral segmentation patterns need not necessarily be coupled (see Janssen et al. 2004).
Also, the postcephalic trunk region of labrophorans or eucrustaceans (head includes here
the maxillary = fifth appendage-bearing segment) may be further subdivided into tagmata and
with this exhibit differentiated appendage morphologies. A subdivision of the trunk into an
appendage-bearing thorax and a limbless abdomen is a possible autapomorphy supporting the
taxon Entomostraca (Walossek and Mü ller 1998a, Maas et al. 2003, Waloszek 2003b).
An autapomorphic trunk division of Malacostraca is the differentiation into two compart-
ments, called thorax and pleon or thorax I and II (see Walossek and Mü ller 1998a), both with
differently specialized appendages (Waloszek 2003b). In Eumalacostraca the pleon is further
subdivided as the sixth pair of appendages is transformed in structure and insertion to form a
tail fan together with the telson (see Fig. 2.7D,E for two stomatopod species). Functional subdi-
vision of the limb-bearing thorax is rarely known from Entomostraca, such as in the Devonian
fossil Lepidocaris rhyniensis. In this species, the anterior thoracopods have well-developed
endites and are also used for food transport, while the posterior appendages have symmetric
rami and are mainly used for swimming (Scourfield 1926).
In many Entomostraca, the last thoracopods may be specialized, often highly modified, for
copulation or as an egg carrier (e.g., Sanders 1957 for Cephalocarida; Torrentera and Dodson
1995 for Anostraca). In Malacostraca, the anterior one or two pleopods may be modified as a
sperm-transfer appendage (mostly called petasma, though likely comprising various different
morphologies; e.g., Martin and Abele 1986), or a thoracopod of the first thoracic limb series
bears an appendix for sperm transfer. In summary, many morphological changes occur in con-
junction with copulation and the transfer (in males) or the reception (in females) of sperm. The
same holds for brood care, which also led to the development or modification of specific struc-
tures associated with the thoracopods, such as oostegites in Peracarida (as possible modified
epipodites; see Maas et al. 2009) or specific setae that hold the eggs, such as in diplostracans.
Within various crustacean groups and possibly in the ground pattern character at least of
Eucrustacea, epipodites occur as rather soft outgrowths on the lateral side of the limb stems of
thoracopods. They may serve for a respiratory or osmoregulatory function (see Maas et al. 2009
for an extensive essay of these structures).
FUTURE DIRECTIONS
One important unsolved riddle is the early evolution of Malacostraca. As mentioned above,
entomostracans are well represented in the fossil record as early as the Terreneuvian, while we
simply lack malacostracan fossils for this period and even several million years later. All Paleozoic
malacostracans show clear malacostracan features, so they are not derivatives of the stem line-
age and cannot contribute much to the reconstruction of the early evolution of Malacostraca
and their appendages. Here we have to wait for new fossil discoveries, because comparison of
extant malacostracan and entomostracan species cannot tell us anything about the evolution-
ary split of these two taxa. Also, the ground pattern status of Maxillopoda needs further sta-
bilization, because this taxon represents, together with Branchiopoda and Cephalocarida, the
taxa with extant derivatives within the Entomostraca. Therefore, we are confident that a closer
look at some fossil maxillopods, for example, Dala peilertae, will contribute to the solution of
this problem.
Another problem awaiting a solution is the phylogenetic position of Insecta, respectively
Tracheata. Especially for the appendages, it is difficult to draw out a plausible evolutionary sce-
nario that would show the evolution from a crustacean ingroup taxon to Insecta/Tracheata.
Especially difficult would be the derivation via Branchiopoda, as has been suggested quite
recently (Glenner et al. 2006). Insecta or Tracheata may well be Labrophora or at least their
sister group (Zhang et al. 2007), but still an evolutionary scenario remains hard to reconstruct
with the existing data on early insect/tracheate evolution. Leaving the character “appendages”
aside for reconstructing phylogenetic trees is not helpful since the animals evolved as a whole
and not just their single character complexes. Besides studying fossil specimens, a closer look at
the development of several taxa living today will provide additional information of probable use
for this question. While many publications in the modern evo-devo field already show promis-
ing results, the classic morphological studies of arthropod ontogeny also contribute important
data (see, e.g., Liu et al. 2009). Nevertheless, many fossil and extant arthropod species need to
be studied to finally solve this section of the tree of life.
CONCLUSIONS
Postantennular appendages of Crustacea show an extremely large variety of morphologies—in

our view more than in any other taxon within Euarthropoda, and this diversity is considered the
driving force of the crustacean success. In living eucrustaceans the head appendages are specifi-
cally dissimilar to the trunk appendages. This dissimilarity is also evident in land-living euarthro-
pods such as spiders and insects. As we know now from a number of fossil species, crustacean
evolution began, however, with only three specialized head appendages, that is, three anterior
appendages differing from the remaining ones—yet more than in the euarthropod ground pat-
tern! Specialization of the two postantennular appendages occurred successively along the
crustacean evolutionary lineage, most significantly in the ground pattern of Labrophora. Any
coincidence in the morphology of head appendages between Eucrustacea and the insects refers
to rather basal features, which would be explainable only when assuming at most a derivation
from a basal node within Labrophora. Ingroup eucrustacean affinities, as suggested, for example,
by molecular studies (e.g., Regier et al. 2008) suffer from little support by any morphological
structures (e.g., one criticism is that the segments bearing the excretory glands in insects differ
from those in all eucrustacean taxa). Furthermore, a huge variety of tree suggestions may also be
explained as being founded on symplesiomorphies.
Again, tagmatization of the body into head and trunk does not correspond to a functional
tagmatization of the limb series. A head with four appendage-bearing segments in the crustacean
ground pattern has only three specialized limbs originally. The fourth head limb is functionally
a trunk appendage. A larger head including the fifth limb-bearing segment in the eucrustacean
ground pattern is in conjunction with the specialization of the fourth head limb. However, the
fifth head limb is still trunk-limb shaped. Therefore, defining what a trunk limb or thoracopod
is depends heavily on the evolutionary level. We even think that a differentiation is rather inap-
propriate, since further trunk segments become involved in the head, although their appendages
do not necessarily change their morphology.
Lastly, it is important to note that counting (at particular structures and taking the evolu-
tionary level into account) deserves a better reputation. The endopod, for example, originally
having more than eight articles in the ground pattern of Euarthropoda, shortened to comprise
seven articles at most in the sister taxon to Chelicerata (e.g., trilobites, Agnostus pisiformis). The
basal number is unclear for myriapods and hexapods (or Tracheata if monophyly is favored)
because of the unclear subdivision of the entire limb but should be six in the endopods of
Crustacea. Within this group, many taxa evolved lower numbers, individually on different
limbs and groups of limbs, but never more.
Probably most important when dealing with crustacean appendages is to recognize that
there is no special “crustaceopodium.” The morphology, ontogeny, and evolution of each
crustacean appendage need to be studied separately and in combination with the other
appendages.
ACKNOWLEDGMENTS
First, we thank Martin Thiel and Les Watling for their invitation to contribute to this volume
and for their editorial work. Thanks are also due to the Central Facility of Electron Microscopy
of the University of Ulm for their support in using their equipment. Several images were taken
during research stays in Copenhagen and London by J.T.H. and C.H., which were supported
by grants from the European Commission’s (FP 6) Integrated Infrastructure Initiative pro-
gram SYNTHESYS (DK-TAF-2171, DK-TAF-2652, GB-TAF-4733). During these visits, scan-
ning electron microscopic (SEM) images were taken on a JEOL JSM-840 and JEOL SM-31010
(Copenhagen), and light microscopy was performed on a Leica DFC 480 (London). Jørgen
Olesen, Copenhagen, kindly provided access to specimens from his collection (Figs. 2.5G,H,
2.6B, 2.7F,G). We would also like to thank several persons for their permission to use some of
their images: Zhang Xi-guang, Kunming (Figs. 2.1G, 2.5C, 2.6C), Jørgen Olesen, Copenhagen
(Fig. 2.5E), Yu Liu, Munich (Fig. 2.2B), and Verena Kutschera, Ulm (Fig. 2.7E). In Ulm, images
were taken on an SEM Zeiss DSM 962 at the Central Unit for Electron Microscopy and on a
Zeiss Axioskop with a mounted DCM 510 ocular camera. Some images had to be enhanced or
processed with various computer programs. Therefore, we express our sincere thanks to the
people that spent their time in providing open-access and open-source software programs such
as ImageJ, CombineZM, GIMP, and Inkscape. Lastly, we thank Klaus J. Mü ller, discoverer of
the Orsten, and the German Research Foundation (DFG) for its continuous funding of the
Orsten research activities, for which J.T.H. received funding under DFG WA-754/15–1.
REFERENCES
Ahyong , S.T. 2001. Revision of the Australian stomatopod Crustacea. Records of the Australian Museum,
Supplement 26:1–326.
Ax , P. 1995 . Das System der Metazoa I. Ein Lehrbuch der phylogenetischen Systematik. Gustav Fischer,
Stuttgart.
Bergström, J., X. Hou, X. Zhang , and S. Clausen . 2008. A new view of the Cambrian arthropod
Fuxianhuia. Geologiska Föreningens i Stockholm Förhandlingar 130:189–201.
Bergström, J., W. Stürmer, and G. Winter. 1980. Palaeoisopus, Palaeopantopus and Palaeothea, pycnogonid arthro-
pods from the Lower Devonian Hunsrück Slate, West Germany. Paläontologische Zeitschrift 54:7–54.
Bowman, T.E., J. Yager, and T.M. Iliffe. 1985 . Speonebalia cannoni n.gen., n.sp., from the Caicos Islands,
the first hypogean leptostracan (Nebaliacea: Nebaliidae). Proceedings of the Biological Society of
Washington 98:439–446.
Boxshall, G.A. 2004 . The evolution of arthropod limbs. Biological Reviews 79:253–300.
Boxshall, G.A., and D. Jaume. 2009. Exopodites, epipodites and gills in Crustaceans. Arthropod
Systematics and Phylogeny 67:229–254.
Briggs, D.E.G., 1976. The arthropod Branchiocaris n. gen., Middle Cambrian, Burgess Shale, British
Columbia. Geological Survey Bulletin 264:1–29.
Briggs, D.E.G., 1978. The morphology, mode of life, and affinities of Canadaspis perfecta (Crustacea,
Phyllocarida), Middle Cambrian, Burgess Shale, British Columbia. Philosophical Transactions of
the Royal Society of London 281:439–487.
Briggs, D.E.G., M.D. Sutton, David J. Siveter, and Derek J. Siveter. 2004 . A new phyllocarid (Crustacea:
Malacostraca) from the Silurian Fossil-Lagerstätte of Herefordshire, UK. Proceedings of the Royal
Society of London Series B 271:131–138.
Budd, G.E. 1998. Stem group arthropods from the Lower Cambrian Sirius Passet fauna of North
Greenland. Pages 125–138 in R.A. Fortey and R.H. Thomas, editors. Arthropod Relationships.
Systematics Association Special Volume Series, Vol. 55. Chapman and Hall, London .
Budd, G.E. 2008. Head structure in upper stem-group euarthropods. Palaeontology 51:561–573.
Calman, W.T. 1909. Part VII. Appendiculata. Pages 1–346 in Lankester, R., editor. A Treatise on Zoology.
Crustacea, Vol. 3. Adam and Charles Black , London .
Carcupino, M., A. Floris, A. Addis, A. Castelli, and M. Curini-Galletti. 2006. A new species of the genus
Lightiella: The first record of Cephalocarida (Crustacea) in Europe. Zoological Journal of the
Linnean Society 148:209–220.
Chen, J.-y., J. Vannier, and D.-y. Huang. 2001. The origin of crustaceans: New evidence from the Early
Cambrian of China. Proceedings of the Royal Society of London Series B 268:2181–2187.
Chen, J.-y., D. Waloszek , and A. Maas . 2004 . A new “great-appendage” arthropod from the Lower
Cambrian of China and homology of chelicerate chelicerae and raptorial antero-ventral append-
ages. Lethaia 37:3–20.
Cockcroft, A.C. 1985 . The larval development of Macropetasma africanum (BALSS, 1913) Decapoda,
Penaeoidea) reared in the laboratory. Crustaceana 49:52–74.
Dahl, E. 1984 . The subclass Phyllocarida (Crustacea) and the status of some early fossils: A neontologist’s
view. Videnskabelige Meddelelser fra Dansk naturhistorik Forening 145:61–76.
Dumont, H.J., and S.V. Negrea. 2002. Introduction to the class Branchiopoda. Backhuys, Leiden .
Fryer, G. 1983. Functional ontogenetic changes in Branchinecta ferox (Milne-Edwards) (Crustacea,
Anostraca). Philosophical Transactions of the Royal Society of London Series B 303:229–343.
Fryer, G. 1988. Studies on the functional morphology and biology of the Notostraca (Crustacea:
Branchiopoda). Philosophical Transactions of the Royal Society of London Series B 321:27–124.
Glenner, H., P.F. Thomsen, M.B. Hebsgaard, M.V. Sørensen, and E. Willerslev . 2006. The origin of
insects. Science 314:1883–1884.
Hamner, W.M. 1988. Biomechanics of filter feeding in the Antarctic krill Euphausia superba: Review of
past work and new observations. Journal of Crustacean Biology 8:149–163.
Hansen, H.J. 1925 . On the comparative morphology of the appendages in the Arthropoda. A. Crustacea.
Studies on Arthropoda, Vol. 2. Gyldendalske Boghandel, Kopenhagen.
Haug , J.T., C. Haug , A. Maas, S.R. Fayers, N.H. Trewin, and D. Waloszek . 2009b. Simple 3D images from
fossil and Recent micromaterial using light microscopy. Journal of Microscopy 233:93–101.
Haug , J.T., Maas, A., and D. Waloszek. 2009a . Ontogeny of two Cambrian stem crustaceans, Goticaris
longispinosa and Cambropachycope clarksoni. Palaeontographica Abteilung A 289:1–43.
Haug , J.T., Maas, A., and D. Waloszek. 2010a . Henningsmoenicaris scutula, Sandtorpia vestrogothiensis
gen. et sp. nov., and heterochronic events in early crustacean evolution. Transactions of the Royal
Society of Edinburgh, Earth and Environmental Science 100:311–350.
Haug , J.T., D. Waloszek , C. Haug , and A. Maas. 2010b. High-level phylogenetic analysis using develop-
mental sequences: The Cambrian Martinssonia elongata, Musacaris gerdgeyeri gen. et sp. nov., and
their position in early crustacean evolution. Arthropod Structure and Development 39:154–173.
Heegaard, P. 1945 . Remarks on the phylogeny of arthropods. Arkiv för Zoologi 37A:1–15.
Heldt, J.H. 1954 . Waptia fieldensis Walcott et les stades larvaires des Pénéides. Bulletin de la Societe des
Sciences Naturelles de Tunisie 6:177–180.
Hennig , W. 1965 . Phylogenetic systematics. Annual Review of Entomology 10:97–116.
Hessler, R.R. 1964 . The Cephalocarida. Comparative skeletomusculature. Memoirs of the Connecticut
Academy of Arts and Sciences 16:1–97.
Hirota, Y., T. Nemoto, and R. Marumo. 1984a . Larval development of Euphausia nana (Crustacea:
Euphausiacea). Marine Biology 81:311–322.
Hirota, Y., T. Nemoto, and R. Marumo. 1984b. Larval development of Euphausia similis (Crustacea,
Euphausiaeea) in Sagami Bay, Central Japan. Journal of the Oceanographical Society of Japan
40:57–66.
Hou, X.-G., and J. Bergström. 1997. Arthropods of the Lower Cambrian Chengjiang fauna, southwest
China. Fossils and Strata 45:1–116.
Hou, X.-G., J. Bergström, and G.-H. Xu. 2004 . The lower Cambrian crustacean Pectocaris from the
Chengjiang biota, Yunnan, China. Journal of Paleontology 78:700–708.
Itô, T. 1982. The origin of “biramous” copepod legs. Journal of Natural History 16:715–726.
Itô, T. 1989. Origin of the basis in copepod limbs, with reference to remipedian and cephalocarid limbs.
Journal of Crustacean Biology 9:85–103.
Janssen, R., N.M. Prpic , and W.G.M. Damen. 2004 . Gene expression suggests decoupled dorsal and
ventral segmentation in the millipede Glomeris marginata (Myriapoda: Diplopoda). Developmental
Biology 268:89–104.
Jones, M.L. 1961. Lightiella serendipita gen. nov., sp. nov., a cephalocarid from San Francisco Bay,
California. Crustaceana 3:31–46.
Kaestner, A. 1967. Lehrbuch der Speziellen Zoologie. Gustav Fischer, Stuttgart .
Kidd , R.J. 1991 . Development of embryonic and naupliar setae and spines and their role in hatching
in the penaeid Sicyonia ingentis: A light and electron microscopic study. Journal of Crustacean
Biology 11:40–55.
Latreille, P. A. 1829. Les crustacés, les arachnides, les insectes. Pages 1–584 in G. Cuvier, editor. Le règne
animal distribué d’après son organisation, pour servir de base à l’histoire naturelle des animaux et
d’introduction à l’anatomie comparée. Déterville, Crochard, Paris.
Lauterbach, K.E. 1986. Zum Grundplan der Crustacea. Verhandlungen des naturwissenschaftlichen
Vereins Hamburg (NF) 28:27–63.
Liu, J., and X.-P. Dong. 2007. Skara hunanensis a new species of Skaracarida (Crustacea) from Upper
Cambrian (Furongian) of Hunan, South China. Progress in Natural Science 17: 934–942.
Liu, Y., X.-G. Hou, and J. Bergström. 2007. Chengjiang arthropod Leanchoilia illecebrosa (Hou, 1987)
reconsidered. Geologiska Föreningens i Stockholm Förhandlingar 129:263–272.
Liu, Y., A. Maas, and D. Waloszek . 2009. Early development of the anterior body region of the grey
widow spider Latrodectus geometricus Koch, 1841 (Theridiidae, Araneae). Arthropod Structure and
Development 38:401–416.
Maas, A., A. Braun, X.-p. Dong , P.C.J. Donoghue, K.J. Mü ller, E. Olempska , J.E. Repetski, D.J. Siveter,
M. Stein, and D. Waloszek . 2006. The “Orsten”—more than a Cambrian Konservat-Lagerst ätte
yielding exceptional preservation. Palaeoworld 15:266–282.
Maas, A., C. Haug , J.T. Haug , J. Olesen, X. Zhang , and D. Waloszek . 2009. Early crustacean evolution and
the appearance of epipodites and gills. Arthropod Systematics and Phylogeny 67:255–273.
Maas, A., G. Mayer, R.M. Kristensen, and D. Waloszek . 2007. A Cambrian micro-lobopodian and the
evolution of arthropod locomotion and reproduction. Chinese Science Bulletin 52:3385–3392.
Maas, A., and D. Waloszek. 2001a . Cambrian derivatives of the early arthropod stem lineage,
pentastomids, tardigrades and lobopodians—an “Orsten” perspective. Zoologischer Anzeiger
240:451–459.
Maas, A., and D. Waloszek. 2001b. Larval development of Euphausia superba Dana, 1852 and a phyloge-
netic analysis of the Euphausiacea. Hydrobiologia 448:143–169.
Maas, A., and D. Waloszek . 2005 . Phosphatocopina—ostracode-like sister group of Eucrustacea.
Maas, A., D. Waloszek , J.-y. Chen, A. Braun, X.-q. Wang , and D.-y. Huang. 2004 . Phylogeny and life habits
of early arthropods—predation in the early Cambrian sea. Progress in Natural Science 14:158–166.
Maas, A., D. Waloszek , and K.J. Mü ller. 2003. Morphology, ontogeny and phylogeny of the
49:1–238.
Martin, J.W., and L.G. Abele. 1986. Notes on male pleopod morphology in the brachyuran crab family
Panopeidae Ortmann, 1893, sensu Guinot (1978) (Decapoda). Crustaceana 50:182–198.
Martin, J.W., and C.E. Cash-Clark. 1995 . The external morphology of the onychopod “cladoceran” genus
Bythotrephes (Crustacea, Branchiopoda, Onychopoda, Cercopagididae), with notes on the mor-
phology and phylogeny of the order Onychopoda. Zoologica Scripta 24:61–90.
Mayer, G., G. Maier, A. Maas, and S. Waloszek . 2009. Mouthpart morphology of Gammarus roeselii com-
pared to a successful invader, Dikerogammarus villosus (Amphipoda). Journal of Crustacean Biology
29:161–174.
Morgan, S.G., and J.W. Goy. 1987. Reproduction and larval development of the mantis shrimp
Gonodactylus bredini (Crustacea: Stomatopoda) maintained in the laboratory. Journal of
Crustacean Biology 7:595–618.
Mü ller, K.J. 1983. Crustacea with preserved soft parts from the Upper Cambrian of Sweden. Lethaia
16:93–109.
V ä stergötland, Sweden. Fossils and Strata 17:1–65.
Mü ller, K.J., and D. Walossek. 1986a . Arthropod larvae from the Upper Cambrian of Sweden.
Transactions of the Royal Society of Edinburgh, Earth and Environmental Science 77:157–179.
Mü ller, K.J., and D. Walossek. 1986b. Martinssonia elongata gen. et sp. n., a crustacean-like euarthropod
from the Upper Cambrian “Orsten” of Sweden. Zoologica Scripta 15:73–92.
Mü ller, K.J., and D. Walossek . 1987. Morphology, ontogeny and life habit of Agnostus pisiformis from the
Upper Cambrian of Sweden. Fossils and Strata 19:1–124.
Mü ller, K.J., and D. Walossek . 1988. External morphology and larval development of the Upper Cambrian
maxillopod Bredocaris admirabilis. Fossils and Strata 23:1–70.
Neil, D.M., D.L. Macmillan, R.M. Robertson, and M.S. Laverack. 1976. The structure and function of
thoracic exopodites in the larvae of the lobster Homarus gammarus (L.). Philosophical Transactions
of the Royal Society of London 274:53–68.
Newman, W.A. 1983. Origin of the Maxillopoda; urmalacostracan ontogeny and progenesis. Pages 105–
120 in F.R. Schram, editor. Crustacean phylogeny. Crustacean Issues, Vol. 1. Balkema, Rotterdam,
The Netherlands.
Olesen, J. 2004 . On the ontogeny of the Branchiopoda (Crustacea): Contribution of development to phy-
logeny and classification. Pages 217–269 in G. Scholtz , editor. Evolutionary developmental biology
of Crustacea. Crustacean Issues, Vol. 15. Balkema, Lisse, The Netherlands.
Olesen, J. 2007. Monophyly and phylogeny of Branchiopoda, with focus on morphology and homologies
of branchiopod phyllopodous limbs. Journal of Crustacean Biology 27:165–183.
Olesen, J., J.W. Martin, and E.W. Roessler 1996. External morphology of Cyclestheria hislopi (Baird,
1859) (Crustacea, Branchiopoda, Spinicaudata), with a comparison of male claspers among the
Conchostraca and Cladocera and its bearing on phylogeny of the “bivalved” Branchiopoda.
Zooogica Scripta 25:291–316.
Olesen, J., S. Richter, and G. Scholtz . 2001. The evolutionary transformation of phyllopodous to sten-
opodous limbs in the Branchiopoda (Crustacea)—is there a common mechanism for early limb
development in arthropods? International Journal of Developmental Biology 45:869–876.
Olesen, J., S. Richter, and G. Scholtz . 2003. On the ontogeny of Leptodora kindtii (Crustacea,
Branchiopoda, Cladocera), with notes on the phylogeny of the Cladocera. Journal of Morphology
256:235–259.
Olesen, J., and D. Walossek. 2000. Limb ontogeny and trunk segmentation in Nebalia species (Crustacea,
Malacostraca, Leptostraca). Zoomorphology 120:47–64.
Preuss, G. 1957. Die Muskulatur der Gliedma ßen von Phyllopoden und Anostraken. Mitteilungen des
Zoologischen Museums Berlin 33:221–256.
Regier, J.C., J.W. Shultz , A.R. Ganley, A. Hussey, D. Shi, B. Ball, A. Zwick , J.E. Stajich, M.P. Cummings,
J.W. Martin, and C.W. Cunningham . 2008. Resolving arthropod phylogeny: Exploring phylogenetic
signal within 41 kb of protein-coding nuclear gene sequence. Systematic Biology 57:920–938.
Richter, S., and G. Scholtz. 2001. Phylogenetic analysis of the Malacostraca (Crustacea). Journal of
Zoological Systematics and Evolutionary Research 39:113–136.
Rudkin, D.M., G.A. Young , R.J. Elias, and E.P. Dobrzanski. 2003. The world’s biggest trilobite—
Isotelus rex new species from the Upper Ordovician of Northern Manitoba, Canada. Journal of
Paleontology 77:99–112.
Sanders, H.L. 1957. The Cephalocarida and crustacean phylogeny. Systematic Zoology 6:112–128.
Sanders, H.L. 1963. The Cephalocarida: Functional morphology, larval development, comparative exter-
nal anatomy. Memoirs of the Connecticut Academy of Arts and Sciences 15:1–80.
Schram, F.R. 1986. Crustacea . Oxford University Press, New York .
Schram, F.R. 2007. Paleozoic proto-mantis shrimp revisited. Journal of Paleontology 81:895–916.
Scourfield, D.J. 1926. On a new type of crustacean from the Old Red Sandstone (Rhynie Chert Bed,
Aberdeenshire)—Lepidocaris rhyniensis gen. et sp. nov. Philosophical Transactions of the Royal
Society of London 214:153–187.
Shu, D., X.-L. Zhang , and G. Geyer. 1995 . Anatomy and systematic affinities of the Lower Cambrian
bivalved arthropod Isoxys auritus. Alcheringa 19:333–342.
Siveter, David J. 2008. Ostracods in the Palaeozoic? Senckenbergiana lethaea 88(1):1–9.
Siveter, David J., D. Waloszek , and M. Williams. 2003. An early Cambrian phosphatocopid crusta-
cean with three-dimensionally preserved soft parts from Shropshire, England. Special Papers in
Palaeontology 70:9–30.
Siveter, Derek J., R.A. Fortey, M.D. Sutton, D.E.G. Briggs, and David J. Siveter. 2007. A Silurian “marrel-
lomorph” arthropod. Proceedings of the Royal Society of London Series B 274:2223–2229.
Snodgrass, R.E. 1958. Evolution of arthropod mechanisms. Smithsonian Miscellaneous Collections
138:1–77.
Stein, M., D. Waloszek , and A. Maas. 2005 . Oelandocaris oelandica and its significance to resolving the
stem lineage of Crustacea. Pages 55–71 in S. Koenemann and R. Vonck , editors. Crustacea and
arthropod relationships. CRC Press, Boca Raton, FL.
Stein, M., D. Waloszek , A. Maas, J.T. Haug , and K.J. Mü ller. 2008. The stem crustacean Oelandocaris
oelandica re-visited. Acta Palaeontologica Polonica 53:461–484.
Størmer, L. 1939. Studies on trilobite morphology. Part I. The thoracic appendages and their phylogenetic
significance. Norsk Geologisk Tidsskrift 19:143–273.
Taylor, R.S. 2002. A new bivalved arthropod from the Early Cambrian Sirius Passet fauna, North
Greenland. Palaeontology 45:97–123.
Torrentera, L., and S.I. Dodson. 1995 . Morphological diversity of populations of Artemia (Branchiopoda)
in Yucatá n. Journal of Crustacean Biology 15:86–102.
Walossek , D. 1999. On the Cambrian diversity of Crustacea. Pages 3–27 in F.R. Schram and J.C.
von Vaupel Klein, editors. Crustaceans and the biodiversity crisis, Proceedings of the Fourth
International Crustacean Congress, Amsterdam, The Netherlands, July 20–24, 1998, Vol. 1. Brill
Academic Publishers, Leiden, The Netherlands.
Walossek , D., I. Hinz-Schallreuter, J.H. Shergold, and K.J. Mü ller. 1993. Three-dimensional preservation
of arthropod integument from the Middle Cambrian of Australia. Lethaia 26:7–15.
Walossek , D., and K.J. Mü ller. 1998a . Cambrian “Orsten”-type arthropods and the phylogeny of
Crustacea. Pages 67–86 in R.A. Fortey and R.H. Thomas, editors. Arthropod relationships.
Systematics Association Special Volume Series, Vol. 55. Chapman and Hall, London .
Walossek , D., and K.J. Mü ller. 1998b. Early arthropod phylogeny in light of the Cambrian “Orsten” fossils.
Pages 185–231 in G.D. Edgecombe, editor. Arthropod fossils and phylogeny. Columbia University
Press, New York.
Walossek , D., and K.J. Mü ller. 1989. A second type A-nauplius from the Upper Cambrian “Orsten” of
Sweden. Lethaia 22:301–306.
Walossek , D., and K.J. Mü ller. 1990. Upper Cambrian stem-lineage crustaceans and their bearing upon
the monophyletic origin of Crustacea and the position of Agnostus. Lethaia 23:409–427.
Waloszek , D. 2003a . The “Orsten” window—a three-dimensionally preserved Upper Cambrian meio-
fauna and its contribution to our understanding of the evolution of Arthropoda. Paleontological
Research 7:71–88.
Waloszek , D. 2003b. Cambrian “Orsten”-type preserved arthropods and the phylogeny of Crustacea.
Pages 66–84 in A. Legakis, S. Sfenthourakis, R. Polymeni, and M. Thessalou-Legaki, editors. The
new panorama of animal evolution. Pensoft Publishers, Sofia, Bulgaria .
Waloszek , D., J. Chen, A. Maas, and X. Wang. 2005 . Early Cambrian arthropods—new insights into
arthropod head and structural evolution. Arthropod Structure and Development 34:189–205.
Waloszek , D., A. Maas, J. Chen, and M. Stein . 2007. Evolution of cephalic feeding structures and the
phylogeny of Arthropoda. Palaeogeography Palaeoclimatology Palaeoecology 254:273–287.
Watling. L. 1993. Functional morphology of the amphipod mandible. Journal of Natural History
27:837–849.
Wehner, R., and W. Gehring. 1995 . Zoologie. Thieme, Stuttgart .
Williams, T.A. 2004 . The evolution and development of crustacean limbs: an analysis of limb homolo-
gies. Pages 169–193 in G. Scholtz , editor. Evolutionary developmental biology of Crustacea.
Crustacean Issues, Vol. 15. Balkema, Lisse, The Netherlands.
Wolff, C., and G. Scholtz . 2008. The clonal composition of biramous and uniramous arthropod limbs.
Proceedings of the Royal Society of London Series B 275:1023–1028.
Zhang , X.-g., D.J. Siveter, D. Waloszek , and A. Maas. 2007. An epipodite-bearing crown-group crusta-
cean from the Lower Cambrian. Nature 449:595–598.
3
MECHANISMS OF LIMB PATTERNING IN CRUSTACEANS
Terri A. Williams
© Watling, Les; Thiel, Martin, Nov 28, 2012, Functional Morphology and Diversity
Abstract
The structural diversity of crustacean limbs is enormous, and their evolution is hotly debated.
Attempts have been made to understand the developmental patterning mechanisms that gen-
erate distinct types of adult limbs by analyzing genes known to regulate limb development in
the arthropod model system, Drosophila . This has led to the discovery of deeply conserved
Oxford University Press, USA, Oxford, ISBN: 9780199875450
features of limb patterning, although it has not clarified how some of the most basic limb
structures—a biramous limb or endites or exites—are patterned. Indeed, based on available
data, one hypothesis is that endites and exites may have varied independently during evolu-
tion. Analyses of patterning during crustacean limb development are further complicated by
the fact that their larval stages can have limbs that are quite distinct from those of adults. This
means that any particular body segment may develop two or more structurally distinct limbs
during the course of the life cycle—a phenomenon yet to be captured by models of limb pat-
terning. Finally, the diversity of limbs is evident not only in their overall plan but also in the
details of setae, joints, and muscles that permit their functional specialization. Like many other
areas of study in crustacean limb development, the analysis of how these structures develop
has barely begun.
INTRODUCTION
The evolutionary radiation of arthropods was driven by limb diversity, and nowhere is this more
evident than in crustaceans. The structural diversity of adult limbs is enormous. Indeed, the
differences are so large that homologies are not fully resolved among some limbs (Williams
2004). The intricacy and functional breadth of crustacean limbs make them a natural choice
for analyzing how development might have been modified to produce such morphological vari-
ation. While we lack a systematic comparison of leg morphogenesis in crustaceans based on
Functional Morphology and Diversity. Edited by Les Watling and Martin Thiel.
74 © 2013 Oxford University Press. Published 2013 by Oxford University Press.
Mechanisms of Limb Patterning in Crustaceans 75
classical descriptive research, more specialized studies—for example, of cellular morphogen-

esis or molecular patterning—are emerging. The purpose of this chapter is to provide an over-
view of the genetic regulation of patterning in crustacean thoracic limb development. The focus
is on the morphological diversity of crustaceans, and the failure of models of comparative limb
development to explain that diversity is noted.
The first section is a brief overview of leg development in crustaceans, emphasizing that most
crustaceans have larval stages that include functional limbs. There are various degrees of meta-
morphosis between stages, and these include transformations of limb morphology. Thus, mod-
els of crustacean limb development and patterning should include not just the initial embryonic
limb but also the transformations of later developmental stages.
Currently, our understanding of which genes function to regulate patterning in crustacean
limbs derives directly from comparisons of development in the fruit fly Drosophila melanogaster.
Therefore, to summarize what is known about crustacean limb patterning, the next section is
an overview of leg patterning in Drosophila and other insects. This is followed by specific cases
where these leg-patterning genes have been examined in crustaceans. No general model of devel-
opmental patterning has emerged that explains adult limb diversity in crustaceans. However, in
this chapter it is hypothesized that limb patterning in crustaceans was controlled ancestrally by
a number of distinct regulatory networks that later became more or less interdependent in the
highly derived and specialized legs of Drosophila. One novel implication of this hypothesis is
that medial and lateral limb structures may have varied independently during evolution. This
hypothesis is followed by an exploration of the fact that crustaceans have different larval stages
with functionally different limbs. Explaining these phenomena requires explaining how radical
transformations of limb structure can precede the development of the adult limb. However, this
is not addressed in current models of limb development. That is, the question is not simply how
one limb is patterned but how a series of quite distinct limbs is patterned on one segment.
Most models of limb patterning explain only a basic coordinate system of positional infor-
mation, that is, proximal-distal, anterior-posterior, and dorsal-ventral axes, that map out a
generic limb field. In the final section of this chapter, limbs are fleshed out as structures made
of setae, muscle, and nerves. The development of these structures and the potential for inte-
grating them into current models of limb patterning are considered. Although crustaceans
provide the most diverse taxon for studies of limb development and evolution, that diversity
has just begun to be sampled and underrepresents the actual limb diversity in crustaceans.
This limits our ability to make inferences about which features of limb patterning are ancestral
and which patterning mechanisms are variable versus constrained. The emphasis throughout
this chapter is on the richness of structural limb diversity that remains virtually unexplored by
developmental analysis and yet is the basis for the functional limb diversity that is showcased
in this book.
A GENERAL DESCRIPTION OF LEG DEVELOPMENT IN CRUSTACEANS
Despite their varied life histories, crustaceans tend to develop in a progressive and sequential
manner. That is, body segments form in an anterior-to-posterior sequence regardless of whether
they develop in the embryonic or larval stage. Subsequently, limb buds develop as direct out-
pocketings of the ventral or ventral lateral body wall. In parallel with the sequential segment
development in crustaceans, limb development occurs in a progressive fashion, with limb buds
gaining complexity over time (Fig. 3.1).
Are there common cellular dynamics that accomplish outgrowth of the limb bud from the
ventral body wall? We know very little about this in crustaceans. In Drosophila, the arthropod
Fig. 3.1.
Progressive leg development in the anostracan larva Thamnocephalus platyurus. T. platyurus has a series
of similar limbs on the trunk. As they develop, limb buds show a gradual elaboration of morphological
features, from less developed posterior limbs to more developed anterior ones (inset). Scale bar, 100 μm.
model for limb development, initial specification of the limb bud differentiates a cluster of cells
that do not undergo immediate rapid growth relative to flanking cells but are instead set aside
for later proliferation. By contrast, in crustaceans, limb buds emerge directly from the surround-
ing body wall in a manner analogous to vertebrate limbs, where we know cell dynamics play
an important role. In vertebrate limbs, the sites of future limb development are detectable as
regions of cell proliferation in the lateral flank. After the emergence of the limb bud from the
flank, a ridge of stratified epithelium, the apical ectodermal ridge, extends across the distal tip
of the limb bud and functions via signaling to maintain a higher rate of cell division in the distal
limb mesenchyme (Sun et al. 2002). However, these types of cell dynamics typically remain
undescribed for direct developing arthropod limbs. In one case where the cell dynamics of ini-
tial outgrowth was examined, Freeman et al. (1992) found that a combination of cell division
and cell shape change accounts for initial outpocketing of the limb bud from the ventral body
wall in the branchiopod Artemia. Furthermore, they found that pharmacologically arresting cell
proliferation could prevent normal evagination of the limb bud. This is a potentially fruitful but
unexplored area; characterizing the cell dynamics underlying limb outgrowth in more species
might uncover common mechanisms of outgrowth, analogous to the apical ectodermal ridge in
vertebrate limbs.
Once the limb bud differentiates from the body wall, it undergoes growth, elongation, and
segmentation. Again, in vertebrate limbs, the course of this process is well described at the cel-
lular level: differentiation proceeds in a proximal-to-distal sequence, driven by a distal zone of
proliferating cells (Sun et al. 2002). By contrast, in arthropods, the basic sequence of morpholog-
ical differentiation of limb segments is not well known for most species. What is known suggests
that arthropods do not form their leg segments in a simple proximal-to-distal sequence. Instead,
they undergo a process of intercalary growth. In crickets, for example, boundaries formed by
developing joints arise sequentially, sometimes proximal or sometimes distal to the previous
boundary (Inoue et al. 2002). It would be interesting to know whether segmented walking legs in
crustaceans share a developmental sequence in segmentation that might reflect a shared under-
lying patterning mechanism. This has never been examined systematically in crustaceans, nor
have growth and elongation in nonwalking legs, for example, pleopods or phyllopods.
How does adult morphology arise? In crustaceans, there are two rather distinct routes to
generate adult limb morphology. First, adult legs may arise directly from the gradual develop-
ment and refinement of the initial limb bud that emerges from the body wall. This happens in,
for example, peracarids and anostracans (Fig. 3.2A). In these species, limb buds emerge from
the body and gradually increase in size and complexity as they form the adult limb morphol-
ogy. However, most crustacean taxa undergo varying degrees of metamorphosis during their
life cycle (Snodgrass 1956). So, for the majority of species, adult limb morphology develops from
modifications of preexisting larval limbs. In these cases, the first limb bud that emerges from
the body wall becomes a functioning larval limb. This limb may then be modified one or more
times before assuming the adult morphology. Adult limb morphology is produced only after
limbs of quite different morphology have developed on the same segment (Fig. 3.2B). Notably,
these differences can arise from one molt to the next in quite dramatic fashion without a period
of quiescence. The types of metamorphosis are too numerous to catalogue systematically but
include the following transformations of limb morphology (typically observed in a single molt):
gain or loss of the exopod, gain or loss of limb segments, gain or loss of endites or exites, com-
plete loss of limb and later redevelopment in alternate form, and extreme hypertrophy of one
feature of the limb (for examples, see Gurney 1942, Snodgrass 1956). Although not accounted
for by models of leg development, explaining these diverse routes of development are crucial for
understanding most crustaceans.
LEG PAT TERNING IN INSECTS BASED ON A DROSOPHILA MODEL OF LEG

DEVELOPMENT
Models of arthropod leg patterning are based on leg development in Drosophila melanogaster
because it has been possible in that species to dissect the function of many genes that provide
positional information to the developing leg. These genes give cells in the developing leg their
spatial fates, for example, proximal or distal and dorsal or ventral. Although a wealth of infor-
mation has been discovered about limb patterning in Drosophila, it has been challenging to
compare this information to other arthropods. In particular, Drosophila’s metamorphic devel-
opment is highly atypical among arthropods: legs do not grow directly out of the body wall, and
indeed, Drosophila has no legs until it reaches the adult stage. However, leg patterning occurs
throughout the life cycle, beginning with specification of the leg primordium in embryogenesis,
followed by elaboration of the leg positional information during the larval stages, and finally
differentiation of leg morphology in the pupal stage.
Leg development in Drosophila begins during embryogenesis when a small group of cells on
the ventral body wall are specified to become leg cells (Cohen 1990, Cohen et al. 1993). These
10–15 cells invaginate to form a saclike structure of epithelial cells lying beneath the larval
epidermis called the leg imaginal disc . Then, during the second and third larval instars, cells
within the leg disc proliferate and form a highly folded epithelium (Fristrom and Fristrom
Fig. 3.2.
(A) Progressive growth of legs on a crustacean that develops without radical metamorphosis in the notost-
racan Triops longicaudatus (successive panels represent more than a single larval molt). (B) Transformations
of a leg in a crustacean that has metamorphic development in the brachyuran Perisesarma fasciatum (after
Guerao et al. 2004); first maxilliped in first zoea, megalopa, and first crab larva.
1993). The teardrop-shaped disc contains the leg in compressed fashion, accordioned upon
itself. At metamorphosis, it everts and extends to form the adult leg (Fig. 3.3A; Fristrom and
Fristrom 1993, Taylor and Adler 2008). The constraints of metamorphosis and the consequent
highly modified leg development cause leg patterning to be analyzed in discrete phases: (1)
embryonic positioning of the primordial limb field on the body wall, (2) larval patterning of
leg axes, and (3) the late pupal transition to metamorphosis. That is, there are periods when
it is technically difficult to follow the fate of leg cells directly, for example, after invagination
but before appreciable cell proliferation and growth of the disc. This lack of simple temporal
continuity creates not only technical barriers but also conceptual difficulties when formu-
lating a general model of limb development applicable to more typical arthropods that lack
metamorphosis.
Fig. 3.3.
Establishing the proximal-distal axis in Drosophila leg development. (A) Comparison of a larval leg disc to
an adult leg showing the relative positions of proximal (P) and distal (D) leg. During eversion and elonga-
tion, the leg disc extends out of the plane of the paper to form the cylindrical structure of the adult leg (disc
after Schubiger 1971; leg traced from a wild-type adult leg). (B) Successive time points during leg develop-
ment in Drosophila showing the intercalation of additional domains of gene expression subdividing the leg
disc: Distal-less in dark gray, dachshund in medium gray, overlap of Distal-less and dachshund in light gray,
and homothorax (nuclear extradenticle) in black (after photo of expression patterns in Abu-Shaar and Mann
1998).
Early Positioning of Limb Primordia Straddles the Anterior-Posterior Boundary of

the Embryonic Segment
Leg patterning in Drosophila begins with the initial positioning and specification of the append-
age primordia on the ventral body wall of the embryo. Appendage primordia are specified rel-
ative to boundaries along the anterior-posterior (AP) and dorsal-ventral (DV) body axes. In
fact, the information used to pattern the body axes is sufficient to position the limb primordia
without other input and imparts AP positional information to the leg. This can be visualized by
boundaries of gene expression1; cells expressing the engrailed gene mark the posterior portion
of each segment and subdivide the leg disc. In Drosophila, wingless-expressing cells, which form
a stripe just anterior to the engrailed-expressing cells, activate cells along the AP boundary to
form limb primordia that are visible as a cluster of cells that express Distal-less. Mutants lacking
Distal-less develop only proximal leg structures (Cohen and Jü rgens 1989).
Comparative studies show that, while the positioning of the primordia along the AP segmen-
tal boundary appears conserved in other arthropods, the actual genes that pattern the early limb
primordia—specifically, the activation of Distal-less by wingless—are not conserved even in other
insect taxa (reviewed in Angelini and Kaufman 2005). Thus, mechanisms of primordia patterning in
Drosophila are therefore unlikely to be ancestral for insects or, by extension, for the Pancrustacea.
Establishing Proximal/Distal Positional Information in the Leg
In Drosophila, fate mapping has shown that the cells that initially express Distal-less in the
embryo assume multiple appendage fates (McKay et al. 2009)—wing, leg, or Keilin’s organs
(larval sensory structures “homologous” to larval legs). As embryogenesis proceeds, this group
of cells becomes subdivided into subsequent fates: one population of cells forms the distal limb
structures in the adult (the telopod), another population forms proximal leg structures, and a
third population produces the Keilin’s organs. Thus, one of the earliest patterning events in
the leg proper is the polarization of proximal and distal leg domains: cells that form proximal
leg structures lose the initial Distal-less expression, while cells that become distal leg maintain
Distal-less expression (albeit driven by an enhancer different from that of the initial Distal-less
expression). The leg cells at this point do not divide, and only during the larval instars will cell
division resume and the bulk of patterning that defines the proximal-distal (PD) axis occur.
Because of the small number of cells in the disc and their relatively cryptic nature early
in larval development, limb patterning in Drosophila is most frequently studied from

late-second-instar larvae through third-instar larvae to pupation. During this time, the leg
disc grows by cell proliferation and assumes its characteristic folded shape within the larva.
The initial specification of proximal and distal accomplished in the embryo becomes elabo-
rated as new domains of PD genes are established and refined (reviewed in Kojima 2004). The
elaboration of PD positional information depends on the secreted signaling molecules wing-
less and decapentaplegic (reviewed in Campbell and Tomlinson 1995, Held 1995, Brook et al.
1996, Williams and Nagy 1996, Blair 1999). wingless and decapentaplegic cooperatively activate
target genes that are expressed in discrete domains along the PD axis of the limb (Distal-less,
dachshund, and indirectly extradenticle through the gene homothorax; Lecuit and Cohen 1997).
These genes are collectively termed the leg gap genes because mutations of these genes form
truncated legs with gaps in PD leg morphology.
In the second-instar imaginal discs, a boundary is established between extradenticle expres-
sion in a proximal domain and Distal-less expression in a distal domain. In the third instar, the
Distal-less domain is subsequently subdivided into a Distal-less domain and dachshund domain
(Fig. 3.3B). The boundaries of dachshund and Distal-less expression are regulated by low and
high levels of wingless and decapentaplegic signaling, respectively, and through repression
proximally by homothorax. These three primary domains—homothorax/extradenticle, dachs-
hund, and Distal-less—are maintained by mutual repression. In addition, wingless and decap-
entaplegic regulate cell proliferation (a role particularly well studied in the wing; see Posakony
et al. 1991; reviewed in Serrano and O’Farrell 1997). Similarly, the gap genes also influence leg
growth. Loss-of-function mutants in leg gap genes cause truncations of normal leg morphology
that span several morphological leg segments.
The expression and function of the leg gap genes appear conserved in other insects. Distal-
less is found in the distal part of legs (Jockusch et al. 2000, 2004, Beermann et al. 2001, Abzhanov
and Kaufman 2000, Inoue et al. 2002, Rogers et al. 2002), with dachshund and homothorax in
intermediate and proximal domains, respectively (Prpic et al. 2001, Inoue et al. 2002, Angelini
and Kaufman 2004).
Notch Signaling Plays a Key Role in Joint Formation in the Drosophila Leg
Joints within the leg disc develop during the pupal stage. They arise by invagination of the leg
epithelium, driven at least in part by cell shape changes (Mirth and Akam 2002). The epithe-
lium that forms joints can be divided into three PD positions based on gene expression and cell
behavior: proximal, mid-distal, and distal. When the joint begins to form, cells of the distal and
mid-distal region undergo apical constriction causing indentation of the leg cylinder. Then dis-
tal cells on the anterior and posterior sides become columnar so that the mid-distal tissue bends
into the leg. Finally, proximal cells extend in a proximodistal direction forming a palisade over
the indented tissue.
The complex cellular dynamics of joint formation are regulated by Notch. Notch is a
transmembrane receptor involved with numerous developmental decisions (reviewed in
Artavanis-Tsakonas et al. 1999). Notch signaling is activated by binding to its ligands, Delta and
Serrate. In the leg, Notch signaling is localized to the joints and promotes both joint formation
and leg growth. The localization of Notch signaling is regulated by the leg gap genes, which act
in a combinatorial fashion to regulate the expression of its ligands as well as the modulator fringe
(Rauskolb 2001).
In early larval stages, Notch is expressed broadly, but by the third larval instar, it is more
concentrated at the joint regions (de Celis et al. 1998). Delta and Serrate are expressed as rings in
each leg segment in the proximal joint region and signal to the more distal cells (de Celis et al.
1998, Bishop et al. 1999, Rauskolb and Irvine 1999, Rauskolb 2001). Notch is activated at the distal
margin of the joints, and this expression correlates with the distal cells known to invaginate to
form the joint (Mirth and Akam 2002). Clones of cells produced within the pupal epithelium
mutant for either Notch or Delta and Serrate show the same phenotype: if the clones are in the
joint regions, normal joints fail to form and the leg is shorter than wild type. If expressed ectopi-
cally, Notch causes supernumerary joints and leg outgrowths (de Celis et al. 1998, Bishop et al.
1999, Rauskolb and Irvine 1999). Thus, Notch not only regulates joint formation but, like the
other PD patterning genes, also regulates leg growth.
Reports from insects other than Drosophila corroborate a role for Notch signaling in leg
segmentation. Beermann et al. (2004) showed the expression of Serrate in wild-type beetle
Tribolium legs. Tc-Serrate is expressed in a series of rings corresponding to each segment of the
leg. Similarly, in analyzing the role of fringe in grasshopper body segmentation, Dearden and
Akam (2000) also described fringe expression in the leg. fringe is expressed in rings along the leg
corresponding to regions proximal to the infolding joints.
Summary of Insect Leg Patterning Based on Drosophila
Drosophila legs are initially patterned by the same coordinate system that provides positional
values within the segments. After this positioning on the body wall, the leg axis is patterned.
However, this axial patterning does not directly regulate morphologically defined structures.
For example, genes that control different PD regions of the limb do not map to specific limb
segments or branches. Instead, the coordinate system appears to be generic: it provides cells
with positional values along PD, DV, and AP axes but does not directly specify adult morphol-
ogy. Indeed, this generic feature of many patterning networks allows them to be conserved
in evolution and to pattern a range of morphologies by modifications of downstream regula-
tion. Thus, although taxon sampling is sparse, it appears that the genes that pattern the PD
leg axis—Distal-less, dachshund, extradenticle —are conserved in other insects and used to
pattern legs from flies to beetles to grasshoppers. How far does this conservation extend in
crustaceans?
REVIEW OF PD PAT TERNING IN CRUSTACEAN LIMBS
Some features of the generic patterning network discovered in Drosophila are found in crusta-
ceans. This supports the idea that a generic limb-patterning network is used throughout the
arthropods, within which different limb morphologies can be specified. However, not all fea-
tures of the regulatory network described above are conserved and found in most taxa sampled.
The two main conserved features are the positioning of limb buds at an AP boundary within the
segment and the initiation and early subdivision of the PD axis. The crustacean data are repre-
sented in Table 3.1, which includes all the leg-patterning genes known from crustaceans.
Positioning of Limb Buds at the AP Segment Boundaries
Positioning of the limb bud along the AP boundary within a segment is found across crusta-
ceans (Fig. 3.4; reviewed in Williams and Nagy 2001). As in all arthropods, engrailed expression
marks the posterior part of each segment within crustaceans (e.g., Patel et al. 1989, Scholtz et al.
1993, 1994, Queinnec et al. 1999, Abzhanov and Kaufman 2000). In malacostracans, in which the
segmentation of the body and the early development of the limb bud can be followed via a pre-
dictable cell lineage, the cells that will produce the limb bud straddle the AP boundary within
the segment. Double labeling of Distal-less and engrailed in biramous limbs of malacostracans
shows that Distal-less is initiated just anterior to the engrailed boundary (Parhyale hawaiiensis,
Browne et al. 2005; Orchestia cavimana and Porcellio scaber pleopods, Hejnol and Scholtz 2004;
Thamnocephalus platyurus, T.A. Williams, unpublished observation). The signaling genes wing-
less and decapentaplegic are virtually unsampled in crustaceans. In the one case that wingless
has been examined, the phyllopodous limbs of the branchiopod Triops longicaudatus, it appears,
just like in insects, to be positioned just anterior to engrailed expression (L.M. Nagy, personal
communication).
The Initiation and Early Subdivision of the PD Axis
The most extensively sampled leg-patterning genes in crustaceans are the leg gap genes. Of
those, Distal-less has been most widely sampled (Table 3.1) and has been examined in repre-
sentative crustacean limbs of quite distinct structure: uniramous, biramous, and phyllopo-
dous. In uniramous limbs of peracarids, Distal-less is expressed on the body wall in a relatively
small cluster of cells that eventually form the tip of the outgrowing limb bud (thoracic limbs of
Porcellio scaber, Abzhanov and Kaufman 2000, Hejnol and Scholtz 2004; Orchestia cavimana,
Hejnol and Scholtz 2004). In biramous thoracic limbs, the cluster of Distal-less expressing cells
is proportionately somewhat larger but also forms an unbroken zone of expression on the body
wall. This cluster will eventually subdivide to form the endopod and exopod (Mysidopsis bahia,
Panganiban et al. 1995). This also occurs in biramous abdominal limbs: in two other peracarids,
the amphipod Orchestia cavimana and the isopod Porcellio scaber, biramous abdominal pleopods
initially develop Distal-less-expressing limb buds that subsequently subdivide to form endopod
and exopod. That is, both branches are part of the distal leg domain (Hejnol and Scholtz 2004).
Interestingly, this pattern is also found in phyllopodous limbs both in branchiopods (Williams
1998, 2008, Williams et al. 2002) and in phyllocarids (Williams 1998). In both groups, an initial
Table 3.1 Overview of limb-patterning genes examined within crustaceans.
Class/species Signaling Leg “gap” genes Leg segmentation genes “Wing” genes “Trachea” genes Body segmen-
genes tation gene
engrailed
wg dpp Dll exd hth dac N Dl nub vvl
Branchiopoda
Artemia franciscana ✓1, 2 ✓2 ✓3 ✓ 4, 5 ✓6

Thamnocephalus ✓7, 8 ✓7
platyurus
Triops longicaudatus ✓9 ✓7, 10 ✓7 ✓11 ✓11 Preliminary
Cyclestheria hislopi ✓12
Leptodora kindtii ✓12
Daphnia magna ✓13
Maxillopoda
Sacculina carcini ✓14 ✓
Malacostraca
Nebalia pugettensis ✓10
Mysdopsis bahia ✓1
Porcellio scaber ✓15, 16 ✓15 ✓15 ✓15 ✓15 ✓16
Orchestia cavimana ✓16 ✓16
Parhyale hawaiensis ✓18 ✓17 ✓17 ✓18
Pacifastacus l ✓3, 5, 19
eniusculus
Gene symbols: wg , wingless; dpp, decapentaplegic; Dll , Distal-less; exd , extradenticle; hth , homothorax; dac , dachshund; N, Notch; Dl , Delta; nub, nubbin; vvl , ventral veinless.
References: 1Panganiban et al. 1995; 2Gonzalez-Crespo and Morata 1996; 3Averof and Cohen 1997; 4Mitchell and Crews 2002; 5Franch-Marro et al. 2005 6Manzanares et al. 1996; 7 Williams et al. 2002; 8Williams
2008; 9Nulsen and Nagy 1999; 10Williams 1998; 11Sewell et al. 2008; 12Olesen et al. 2001; 13Shiga et al. 2002; 14Mouchel-Vielh et al. 1998; 15Abzhanov and Kaufman 2000; 16Hejnol and Scholtz 2004; 17 Prpic and
Telford 2008; 18Browne et al. 2005; 19Damen et al. 2002.
Fig. 3.4.
The size of the limb primordia is highly variable in crustaceans: schematic views of ventral segments in
different crustaceans illustrating the relative amount of ventral segment fated to become limbs. In all
cases, primordia retain their anterior-posterior positioning regardless of size (see text for examples).
domain of Distal-less expression forms on the ventrolateral body wall. Like the biramous domain,
it eventually subdivides to form the endopod and exopod. (However, subsequent Distal-less
expression is more widely distributed; see below.) Thus, throughout crustaceans—as through-
out all arthropods sampled—Distal-less expression is consistent with the role of patterning the
distal region of the leg and promoting PD outgrowth.
For the other leg gap genes, extradenticle and dachshund, published data exist only for
uniramous and phyllopodous limbs. Where they have been examined in crustaceans, extraden-
ticle is expressed in a proximal domain complementing and exclusive of the Distal-less domain,
indicating a conserved role for the early stages of limb patterning.2 In uniramous limbs, extraden-
ticle is expressed in the first two limb segments (Porcellio scaber, Abzhanov and Kaufman 2000).
In early phyllopodous limb bud, extradenticle is expressed in the limb bud outside the Distal-
less domain, but later, when Distal-less is expressed more proximally, extradenticle expression is
maintained so that the two are coexpressed (Triops longicaudatus and Thamnocephalus platyurus,
Williams et al. 2002). Like extradenticle, dachshund expression in uniramous crustacean limbs
is similar to that in Drosophila. It arises between the distal Distal-less and proximal extradenticle
domain (Porcellio scaber, Abzhanov and Kaufman 2000). In phyllopodous limbs, one domain
of initial dachshund expression is just proximal to the initial Distal-less expression, as might be
expected (Sewell et al. 2008). However, the expression is dynamic and becomes more complex
as the limbs develop (see below). Taken as a whole, the patterns of expression in leg gap genes in
crustaceans are similar to Drosophila: initially, proximal and distal domains are established, and
subsequently, new domains are intercalated that can provide more precise PD information.
Notch in Crustaceans
Although there are no published reports of expression of Notch pathway genes in crustaceans,
there are preliminary data that Notch protein is expressed in reiterated stripes in developing
endites in branchiopods and functions in proper endite formation (T.A. Williams, unpub-
lished observation). Notch is expressed differentially in the limb, in the medially repeated lobes
(endites) but not the lateral lobes. DAPT, a gamma secretase inhibitor that blocks Notch sign-
aling, can block formation of endites in branchiopod legs. In the most extreme phenotype, all
endites (except the most proximal one) fuse to form a single unbranched lobe. Again, the effect
within the limb is not uniform, fusing medial lobes (endites) but not lateral lobes.
Summary
All crustacean limbs currently sampled show conservation in AP limb bud positioning and
initial PD patterning. In a sense, it is remarkable that a generic PD coordinate system is used
throughout arthropods given their limb diversity. At the same time, the conservation of pattern-
ing mechanisms in the face of great morphological diversity makes PD patterning genes surpris-
ingly unhelpful in explaining how limb morphology may have evolved; known mechanisms do
not specify whether the limbs will be fundamentally uni- or biramous, for example, nor do they
pattern the medial and lateral lobes. In short, patterning genes known from Drosophila cannot
as yet explain any of the differences so prevalent in crustacean limbs. In particular, the fact that
crustaceans have legs quite distinct from uniramous walking legs gives rise to questions about
how biramous or phyllopodous legs are patterned.
How Are the Two Primary Limb Branches Patterned?
Patterning the primary limb branches is a fundamental and yet unanswered question in crus-
taceans. Everything we have learned to date points to a single PD patterning axis with a single
domain of Distal-less from which both the endopod and exopod arise. That is, there is no evi-
dence to indicate that the formation of the endopod and exopod within the distal domain is
controlled by genes known from Drosophila leg patterning. More generally, outgrowths from
the limbs are not patterned as new PD growth axes (reviewed in Williams 1998, Nagy and
Williams 2001, Williams and Nagy 2001). However, patterning of branches from the main axis
is particularly important regarding the formation of the endopod and exopod because biramous
limbs are both ancestral and widespread among crustaceans. While loss of Distal-less function
in crustaceans should produce loss of both the endopod and exopod, we do not know which
genes would prevent splitting while permitting outgrowth. In addition, although we know that
limb branches are not patterned as simply reiterated PD growth axes, we do not know to what
degree the bifurcation of the endopod and exopod is distinct from the regulatory mechanisms
that form other limb outgrowths (exites and endites).
Phenomenologically, the formation of the two branches can vary among species. Fig. 3.5
shows some scenarios for morphogenesis in biramous limbs: both limb branches might arise
simultaneously from the body wall, or limb branches might form from a subdivision of an already
elongating limb bud, or a second branch might arise late in morphogenesis as an outgrowth from
the main branch. There is some evidence that all three modes are used in crustaceans.
Fig. 3.5.
Schematic of possible types of limb morphogenesis leading to biramous limbs. (A) The limb bud arises
from the body wall bilobed and continues to extend both branches. (B) The limb bud arises unbranched
from the body wall and only after some growth subdivides and forms two branches. (C) The limb bud
arises unbranched from the body wall, grows, and then forms a small bud that subsequently grows as the
second branch.
What controls patterning in biramous crustacean limbs is unknown, and there are no
cross-species comparisons of the development of biramous limbs. However, there have been
comparisons within peracarid species of the development of biramous abdominal limbs to their
uniramous thoracic counterparts. These comparisons depend on the fact that peracarids estab-
lish their segments (and early limb buds) via a repeatable cell lineage. Therefore, it is straight-
forward to compare the fates of cells that formed the exopod in the biramous abdominal limbs
to the same cells on the thorax. In the amphipod Orchestia cavimani, Hejnol and Scholtz (2004)
found the cells that are homologous to abdominal exopod cells indeed express Distal-less early
on but then subsequently lose Distal-less expression. This suggests that these cells still have an
early specification to form an exopod—or at least distal leg structures—but that that specifica-
tion is lost during subsequent development. By contrast, in the isopod Porcellio scaber, cells in
the thorax that are homologous to abdominal exopod cells never express Distal-less (Hejnol and
Scholtz 2004). This suggests that these cells never acquire a distal limb fate at all. Thus, in taxa
that independently evolved uniramous from biramous limbs, the mechanisms controlling sup-
pression of the exopod in the thorax appear distinct.
In related studies, Wolff and Scholtz (2008) marked cells in the early uniramous thoracic
limb bud and the biramous abdominal limb bud in the amphipod Orchestia cavimani, in order
to follow the subsequent fate of those cells as the embryos grew. Before limb outgrowth, body
segments contain rows of aligned cells approximately 10 cells wide. In the abdomen, 6 of 10 cells
contribute to the limb bud and do so without much change of register; for example, the medial
cells form the endopod, and the lateral cells form the exopod. In the thorax, cells also grow out
in register, although fewer cells of the row form the leg. Notably, the cells that form the exopod
in pleopods form the lateral part of the walking thoracic leg. This suggests that, in these amphi-
pods, the formation of an unbranched limb evolved from the suppression of the mechanism that
would split the initial domain into endopod and exopod.
These data are very interesting and, in the absence of genetic manipulation, allow some spec-
ulation on how a single axis forms two axes. Of course, in these cases, one of two branches is lost
during evolution, leaving unanswered the original question—how two branches are patterned
from a single PD domain. It is also unclear how much these results can be generalized. The line-
age results that lead to the conclusion that there is a suppression of the split into a biramous limb
are derived from Orchestia cavimani (Wolff and Scholtz 2008). However, the earlier comparison
of Distal-less expression within Orchestia cavimani and Porcellio scaber suggests that, even within
the peracarids, exopod loss occurs via different mechanisms (Hejnol and Scholtz 2004). Also,
malacostracans are unique in having teloblastic growth and cell-lineage-based formation of the
germband and limb buds. Whether their mechanisms of limb patterning are similarly derived
remains to be seen.
Common Aspects of Patterning in Phyllopodous Limbs of Branchiopods
Phyllopodous limbs are even more distinct than biramous ones from the kind of uniramous
walking leg represented in most models of arthropod limb patterning. Despite the previously
mentioned conservation of some aspects of limb patterning, phyllopodous limb buds have com-
plicated temporal and spatial expression of the PD leg-patterning genes. In addition, both bran-
chiopods and phyllocarids have large thoracic limb buds that occupy virtually the entire ventral
to ventrolateral body wall. For example, in Artemia the limb bud occupies six of the eight precur-
sor rows that form the AP segmental anlage, whereas the interleg region is only two of eight rows
(Freeman et al. 1992). This contrasts with peracarids, where the initial limb buds occupy less
than half the segment (e.g., Dohle and Scholtz 1988, Scholtz 1990). These differences in relative
size of the limb anlagen, as well as differences in the geometry of the developing limbs, argue
against hypotheses of straightforward conservation of limb patterning since such differences
would certainly influence the action of, for example, short-range signaling molecules.
Additional arguments arise simply from the complex patterns of gene expression found in
phyllopodous limbs. As mentioned above, expression of the leg signaling gene wingless has been
examined in the branchiopod Triops longicaudatus and is expressed initially in segmental stripes
along the body anterior to the engrailed stripes. However, as the limbs develop on the segments,
each wingless stripe breaks up, eventually coming to occupy only a portion of each lobe of the
phyllopod (Nulsen and Nagy 1999). The wingless expression varies by lobe: on the most medial
lobe (the gnathobase), expression is on the lateral margin; on the other endites as well as the
endopod and exopod, the expression is on the medial margin; and on the epipod, the expression
outlines the entire lobe. Similarly, expression of Distal-less and extradenticle in branchiopods is
initially comparable to Drosophila: Distal-less is expressed in the distal limb, in both the devel-
oping endopod and exopod, exclusive of and surrounded by extradenticle expression. However,
wingless
dachshund
Distal-less
epi
gn
exo E2
E3
endo
E5 E4
Fig. 3.6.
Schematic of gene expression in the early limb bud of the branchiopod Triops longicaudatus. With the
exception of the gnathobase, the endites show identical patterns of expression. All other lobes are unique.
Abbreviations: E2–E5, endites 2–5; endo, endopod; epi, epipod; exo, exopod; gn, gnathobase.
as development proceeds, Distal-less expression spreads into the more proximal lobes—with
particularly extensive expression in the endites—and this later expression of Distal-less overlaps
with extradenticle. When this later Distal-less expression is traced through limb development, it
coincides exactly with seta-forming cells of the limb (Williams 2008). Early expression of dachs-
hund in the Triops limb bud is consistent with an intermediate dachshund region between the
Distal-less- only expression domain and the extradenticle domain of the proximal leg. However,
expression occupies only a small region of cells in a large limb bud, and the topology that
would correspond to a uniramous limb can be only roughly inferred. In addition, dachshund is
expressed in a proximal stripe and, later, in a series of medially reiterated stripes in each endite
(Sewell et al. 2008). Indeed, one striking feature of many limb-patterning genes in phyllopodous
limbs is that they show reiterated domains of expression in the endites. In Triops, the branchio-
pod that has been examined most extensively, the endites between the gnathobase and endopod
show identical expression patterns for wingless, Distal-less, extradenticle, dachshund, and Notch
(Fig. 3.6). This is true in another branchiopod, Thamnocephalus platyurus, although the dachs-
hund and Notch data are preliminary. Below I argue that a medial patterning system controls
medially reiterated structures in crustacean limbs.
Summary
In Drosophila a generic coordinate system provides positional information for developing limbs,
and aspects of this generic system appear conserved even in limbs of highly different morphol-
ogy, that is, initial PD patterning in phyllopodous limbs. However, this fact alone highlights how
little these positional coordinates inform us about morphology later in development: phyllopo-
dous limbs are so structurally different from uniramous limbs that sharing the same axial PD
patterning must relegate that patterning to only the most indirect control of adult morphology.
Within this context, I propose a modified view of limb patterning in crustaceans and describe
how that view accounts for some patterns of diversity.
LIMITS OF PD PAT TERNING MODEL IN EXPLAINING THE DIVERSIT Y OF LIMB

MORPHOLOGIES AND AN ALTERNATIVE VIEW OF LIMB PAT TERNING
One point emerges clearly from the analysis of Drosophila leg-patterning genes in crustaceans:
interactions of those genes alone cannot provide a satisfactory model to explain the diversity of
adult limb morphologies in crustaceans. One particular point is worth reiterating since it is cen-
tral to crustacean limb morphology. We do not know how the two main branches of a biramous
limb are patterned. This is important because the biramous limb is most likely ancestral (see
chapter 2). Beyond that, biramous thoracic limbs are very common among crustaceans, although
they happen not to occur in the few crustaceans typically used for studies of limb patterning.
Beyond the question of biramous limbs, crustaceans have a variety of endites and exites not
accounted for by the model based on patterning in Drosophila. For example, Boxshall (2004)
distinguishes as many as 9–10 distinct nonhomologous exites among crustaceans. In addition,
on medial limb margins, most anterior feeding thoracic limbs have well-developed endites used
for sorting and breaking up food. In branchiopods, the phyllopodous limbs are defined by their
well-developed endites and exites. These patterns among crustacean limbs lead to an alternative
view of crustacean limb patterning based on certain contrasts between Drosophila and crusta-
ceans (Fig. 3.7).
Model for Ancestral Limb Patterning
First, the amount of ventral and ventrolateral body wall devoted to the limb bud and the timing
of adult limb development vary. In Drosophila, the leg develops from a very small set of cells
patterned in the embryo that then invaginate and develop segregated from the larval epidermis
(see above). Through further proliferation and patterning, these cells produce the adult leg mor-
phology. By contrast, no crustaceans set aside part of the body wall epidermis for limb forma-
tion. Limbs develop directly from the body wall in coordination with adjacent tissue. In some
cases the amount of body wall devoted to the adult limb is relatively small, but in some cases it
is not. In branchiopods, virtually the entire ventrolateral body wall becomes limb. This is likely
to represent the ancestral case for pancrustaceans since stem lineage larval forms appear to have
developing limbs that are large relative to the body wall. In parallel with these differences in the
timing and extent of ventral body wall involvement in leg development, crustaceans show an
enormous variety of limb morphologies compared to the single unbranched leg in Drosophila.
Laterally, exite morphology is highly variable. Medial limb morphology is diverse as well but
often is organized around a series of medially reiterated structures: endites, leg segments, or
some combination of those.
These considerations lead me to develop a hypothetical model for how limb-patterning
genes were deployed ancestrally in Pancrustacea and modified in extant taxa (Fig. 3.7).
I hypothesize that, ancestrally, the limb-patterning field was broad and occupied a large area
of the ventral to lateral body wall. Within that patterning field, a number of patterning net-
works operated but were only loosely coupled with one another. An overall PD patterning axis
promoted limb outgrowth and controlled the formation of both the endopod and exopod. This
is supported by the fact that all crustaceans have limb buds with a region of exclusive Distal-
less expression that gives rise to the exopod and endopod. In concert, a medial patterning
Drosophila crustaceans
field of limb patterining

on body wall
segregation early in development continuous functional integrity
from the rest of the ventral of the ventral body wall
body wall
adult limb morphology unbranched leg high diversity of morphologies,

e.g., biramous, phyllopodous
HYPOTHESIS
P
L P N L N
limb pattering D
systems D
PD and N patterning are strictly Patterning axes are only loosely
superimposed; lateral genes (used coupled. PD patterns main axis of leg
to specify the wing) maintain the (1 or 2 branches); N patterns medially
same topological relationship but reiterated structures (lobes or
are not in the limb field. segments); L patterns lateral limb lobes.
Fits rapid life cycle highly Flexibility of patterning permits high

specialized for ecological niche limb diversity
consequences
DV homologies are comparable Medial/lateral homologies can vary

along PD axis independently along PD axis
Fig. 3.7.
Comparison of a number of features of Drosophila leg development and crustacean leg development illus-
trating the hypothesis that patterning systems now coupled in Drosophila may have been only loosely
coupled ancestrally. The rectangles represent a half segment, for example, from the midline outward. Gray
shading represents the size of the early limb primordia relative to that half segment. N, L, and PD repre-
sent gene patterning networks: Notch, lateral, and proximodistal, respectively. DV, dorsal-ventral axis.
system based on Notch signaling produced repeated structures. Those structures could be
either endites or segments. This is supported by preliminary data of Notch expression and
function in branchiopods. Laterally, another set of genes (nubbin, apterous) operated to pro-
duce exites (Averof and Cohen 1997). These sets of loosely coupled patterning networks would
have high f lexibility to produce the various limbs found in extant groups. In Drosophila , those
loosely coupled networks are now tightly coupled: the PD and Notch networks are linked, and
the lateral genes are expressed in cells that undergo an early migration away from the rest of
the limb anlagen. In uniramous limbs, Notch regulates leg segments; in the ancestral case, it
regulated any medially repeated structures. In the derived, uniramous limb of Drosophila ,
Notch and PD patterning are linked, the limb bud is a reduced part of the body wall, and much
more of the limb bud is restricted to the initial distal region demarcated by the PD patterning
system. This contrasts with the much more extensive limb buds found in branchiopods and
in stem group crustaceans.
Consequences and Predictions
This hypothesis suggests a rethinking of how development of limbs may have evolved and forces
a somewhat atypical view of the developmental basis of limb homologies. In particular, it pre-
dicts that homologs can vary independently on the medial versus lateral margins along the PD
axis; that is, exite morphology varies independently from endite morphology. This is consistent
with the fact that lateral limb branches are highly variable (Boxshall 2004). This hypothesis
implies that any particular slice along the PD leg axis cannot be considered as an integrated
homolog the way we conceive of a PD series of limb elements in the vertebrate limb. It also
implies that Notch regulates all medially repeated structures, that within any limb medial struc-
tures are serial homologs, and that between limbs certain dissimilar medial structures, lobes,
and segments are direct homologs. (Despite these elements being direct homologs, it may not be
possible to draw one-to-one homologies between elements, a common problem with reiterated
serial homologs [Bateson 1894, Wagner 1989, Van Valen 1993].) This hypothesis also leads to
specific predictions in taxa outside of crustaceans. For example, in insects, the gnathal append-
ages have repeated medial lobes (endites). I predict that these lobes will be regulated by Notch
signaling as are leg joints. This has not been examined in Drosophila because of their highly
reduced mouthparts.
THE IMPACT OF DIVERSE LARVAL STAGES ON MODEL S OF LIMB DEVELOPMENT

In the preceding sections, the focus was on adult thoracic limb diversity from a standard per-
spective in evolutionary developmental biology: how is development modified to produce one
adult leg morphology versus another? Although this is normally how comparisons between
species are framed, this narrow focus is justified only in the case of crustaceans that develop
their adult limbs directly. However, the majority of crustacean taxa undergo some metamor-
phosis. In these cases, a particular thoracic segment can, for example, produce a series of limbs
with distinct morphologies during successive molts. As described above, adult limb morphol-
ogy may be achieved only after limbs of quite different morphology have developed on the
same segment.
Why is this significant? Consider the differences in limb development in direct versus indi-
rect developers that are illustrated schematically in Fig. 3.8A. For direct developers, each species
produces its own particular adult morphology in a single developmental pathway from primor-
dium to adult limb. This type of life history lends itself to the question commonly posed by cur-
rent research: How do different morphologies develop? By contrast, crustaceans with distinct
larval stages develop the adult limb morphology via a sequence of potentially distinct develop-
mental pathways. In these cases, patterning of the adult limb is built upon prior functional limbs
that are transformed in a variety of ways. For example, development to the adult limb may occur
gradually or as a marked modification of a preexisting larval limb, or even as a wholesale replace-
ment after a larval limb is lost.
Fig. 3.8.
Conceptual differences in modeling limb development in direct developers versus those with multiple
functional larval stages, as are found in many crustaceans. (A) For direct developers, rows represent a
single thoracic segment in each of three different species. The adult thoracic limb morphology is differ-
ent in each species (as represented by different shading patterns). The typical question posed by current
research is how these different morphologies develop. However, in crustaceans with functional larvae, the
three rows of different species have more complex pathways to reach the adult thoracic limb morphology.
Larval stages are represented in which limbs may be only slightly different from the adult (row 1), quite
distinct from the adult (row 2), and even be lost (no color) and regained (row 3). (B) The impact of multiple
functional larval stages is similar for considerations of patterning segment identity along the body axis. For
direct developers, rows 1–3 represent three different species with different patterns of functional clusters
of limbs (represented by different shading patterns along a series of segments). The typical question posed
by current research is how these different patterns of segment identity develop. However, in crustaceans
with functional larvae, the developmental pathway leading to the adult pattern is more complex since func-
tional larvae can have distinct clusters of limb identities. In both cases, these changes in morphology over
time need to be accounted for in models of limb development.
The series of regulatory control mechanisms that might pattern such diverse routes to
adult limb morphology is wholly unaccounted for in models of limb patterning. At the least,
analysis of adult limb patterning should include every larval stage and the expression and
function of genes in each stage. As yet, patterning of different limb morphologies found in a
complex larval sequence remains unexplored. An important and related question is whether,
on any one particular segment, the diversity in limb structure is somehow constrained during
development. That is, are only some morphological transformations possible from one molt
to the next?
These differences between direct and indirect developers also influence our models of
how segment identity develops. Comparative data exist for the patterning of segment identi-
ties that define body tagmata (reviewed in Deutsch and Mouchel-Vielh 2003). Genetic regula-
tion of different body regions is provided by homeotic (Hox) genes, which show differential
expression and control segment identity along the AP body axis. Hox genes are found in all
the major crustacean taxa, and differences in their expression control the fate of anterior tho-
racic segments, for example, determining what segments bear maxillipeds (Averof and Patel
1997, Pavlopoulos et al. 2009). However, the same phenomena that complicate the patterning of
adult limb morphology on any one segment can obviously take place anywhere along the body
axis. Therefore, the patterns of segment identity within tagmata can change during develop-
ment (schematized in Fig. 3.8B). Whereas the standard question is to ask how the tagmata in
species A are patterned differently from the tagmata in species B, for most crustaceans larval
stages with different groupings of limb morphologies present a more complex sequence of tag-
mata that presumably would require differential regulation at each stage. The presence of larval
forms implies that groupings of similar segments seen in the adult may not have been stable
throughout the life cycle. In larval forms, patterns of segment identity are much more complex
since larval limbs can be structurally distinct from adults. I do not suggest that the underlying
tagmata are not stable, merely that the clustering of similar limbs—that is, the apparent seg-
ment identity—can change during development thus complicating our models of how segment
identity is specified.
Despite the absence of patterning data that bear on these questions, I discuss and illustrate
them at length because the sheer variability in limb morphology and life history patterns within
crustaceans is generally not incorporated into models of arthropod limb patterning. This diver-
sity is key to understanding the radiation of crustaceans, but our models do not account for it.
ANALYZING THE DEVELOPMENT AND DIFFERENTIATION OF LIMB STRUCTURES

Models of limb patterning mainly explain how spatial pattern arises during development,
typically through the formation of Cartesian axes: proximal-distal, anterior-posterior, and
dorsal-ventral. In these models, actual limb structures are a proxy for position; for example,
claws at the limb tip become most distal positional values. Although this has been a very use-
ful perspective in illuminating how certain generic regulatory pathways can be used in differ-
ent situations, it tends to obscure morphological structures. After all, it is specific structures
that function in the particular habits and life history of each species. Considered in their own
right, the structures that compose the leg display a number of intriguing developmental fea-
tures. For example, some setae show regularities in positioning that transcend species, such
as their position adjacent to joints. Also, many of the genes that provide axial positional infor-
mation in the leg also participate directly in patterning morphological structures. It seems
quite plausible that patterning of leg axes and morphological structures is more integrated
than expected; we are slightly misled by Drosophila , where the timing of patterning and dif-
ferentiation is atypical. In most crustaceans, patterning and differentiation are, at least phe-
nomenologically, quite closely integrated—giving rise to the question of whether they are
mechanistically integrated as well. If this is accurate, understanding the development of limb
structures could elucidate novel morphological subunits within limbs. For example, fields of
setae or setal joint complexes that are linked developmentally would constrain the possibili-
ties of limb evolution.
In addition to exploring this hypothesis of novel morphological subunits, a more straight-

forward and pragmatic reason exists for studying descriptive limb morphogenesis. To interpret
patterns of gene expression or phenotypes produced by perturbations of gene function, we must
know the details of tissue morphogenesis. As the model system, Drosophila has had much of
the descriptive groundwork done: the timing of differentiation is known, and cell types are
often well characterized. By contrast, that groundwork is lacking in crustaceans. However, to
correctly interpret details of gene expression and function, we need to know what tissues these
differentiating cells will become. This is particularly important because many patterning genes
have multiple functions, and dissecting out those functions requires knowing the fate of cells
expressing the gene.
To consider whether developmentally novel subunits exist in crustaceans, I discuss devel-
opment and patterning of muscles and setae within crustacean limbs. I again use Drosophila
as a point of reference, although it is important to note that the presence of the pupal stage has
obscured analysis that might integrate aspects of limb patterning with setal and muscle develop-
ment in that species. Various aspects of limb development in Drosophila have been compressed
to fit the demands of radical metamorphosis. In particular, the timing of differentiation into
the adult relative to patterning of the leg is not characteristic of most crustaceans. This is best
grasped schematically, as in Fig. 3.9, where, if we compare events along a normalized timeline,
it is obvious that the lack of larval limbs and the radical metamorphosis in Drosophila create
an atypical distribution of the timing of patterning versus differentiation compared to most
crustaceans—indeed, most arthropods. Cell differentiation occurs along with ongoing posi-
tional patterning in crustaceans, as illustrated by the development of the limbs in branchiopod
crustaceans. In branchiopods, the earliest differentiation of the limb bud from the body wall
is followed by differentiation of both setae and muscles (Williams and Muller 1996, Williams
2007a). The possible integration of patterning and differentiation remains an open question in
crustaceans.
LIMB DEVELOPMENT
Drosophila embryo larva pupa adult
PATTERNING
DIFFERENTIATION
crustacean embryo larva larva juvenile adult
PATTERNING
DIFFERENTIATION
Fig. 3.9.
A schematic timeline of limb development showing the relative timing of patterning and differentiation in
Drosophila and crustaceans. In crustaceans, as is likely ancestral, patterning and differentiation are highly
overlapping during development. In Drosophila, the constraints of a radical metamorphosis segregate the
two events to a marked degree.
Development of Muscle in Crustacean Limbs
Muscle in Drosophila and other insects arise from precursor cells that differentiate into
muscle founders. These founder cells act as positional templates, attracting other myotubes
to fuse with them to form functional muscle. However, in Drosophila , a radical metamor-
phosis divides muscle formation into two phases: larval and adult. Larval muscles develop
directly during embryogenesis. Some adult muscle precursors are specified during embryo-
genesis, but they become fully developed only during the pupal metamorphosis (Roy and
VijayRaghavan 1999).
In Drosophila legs, muscles originate from a population of precursors (5–10 myoblasts)
associated with the embryonic leg disc primordia. These cells proliferate during the larval
period to form about 500 myoblasts associated with the disc epithelium. During late larval
and early pupal development, some of these myoblasts begin expressing dumbfounded , an
immunoglobulin that attracts other myotubes to fuse with the founder cells and thus serves
as a marker of founders. As pupation proceeds, internal tendons form closely associated with
founder cells, myotubes fuse with the founders, and attachment sites form on the leg epithe-
lium (Soler et al. 2004).
How do crustacean muscles develop? This question is largely unexplored, although one
recent paper offers the first evidence that founder cells are present in crustaceans as well as
insects. Kreissl et al. (2008) generated a monoclonal antibody against heavy-chain myosin in
isopod crustaceans and then traced myosin-expressing cells during development. They found
that muscle development proceeded in a fashion similar to that in insects. Initially, only single
cells expressed the antigen, and these were arranged in a pattern that was a precursor to the adult
pattern. Subsequently, these cells became multinucleate syncytia, although it was not possible
to distinguish whether this occurred via fusion (Kreissl et al. 2008).
Development of Setae in Crustacean Limbs

Crustacean setae are enormously diverse (as described in chapter 6). If external morphology,
accessible through light and scanning electron microscopy studies, remains underdescribed,
the internal morphology and development of setae are even less explored. Although setae are
assumed to be homologous among arthropods, we have no general model for noninsect setae
for comparison. In insects, sensilla that form bristles (setae) and other sense organs develop
through a well-described lineage mechanism from a single precursor epidermal cell (reviewed
in Hartenstein 2005). Stereotyped divisions of the precursor cell produce both sensory neurons
and accessory cells that ensheath the neuron or form cuticular outgrowths. Modifications of
this lineage via apoptosis and/or repeated divisions in certain lineages can produce all the sen-
silla types found in insects (Lai and Orgogozo 2004), including setae without sensory function
(via apoptosis of the lineage leading to the neuron). Furthermore, whereas insect sensilla can
be grouped into two or three main categories based on adult morphology (Hartenstein 2005),
crustacean sensilla appear to have a much broader range of underlying cell numbers (Hallberg
and Hansson 1999).
How do crustacean setae develop? To my knowledge, only two studies describe events of the
cellular morphogenesis of crustacean setae. Based on transmission electron microscopy, Guse
(1983) described the development of the aesthetascs, tubular sensory setae, on the antennule of
the mysid Neomysis integer. The aesthetascs have 60–80 sensory cells and eight accessory cells
that ensheath the neurons. Sensory cells are differentiated before the molt, during which the
shaft is formed. The shaft begins to develop during apolysis with a retraction of the epidermis
from the old cuticle. The shaft develops by forming a cylindrical invagination of the epidermis
with the midpoint of the shaft being the deepest part of the invagination. The eight ensheathing
cells that secrete the shaft cuticle are arranged in a telescoping manner from proximal to distal
such that the cuticle of the distal shaft is laid down by one ensheathing cells. with more proximal
ensheathing cells laying down more proximal cuticle.
In the second study, setal morphogenesis was described for the anostracan Thamnocephalus
platyurus using light microscopy: differentiating setal cells could be seen within the develop-
ing thoracic limb bud (Williams 2007b). The thoracic limbs in T. platyurus are highly setose,
although almost none of the setae are sensory. The only sensory setae present are mechanore-
ceptors on each endite. In parallel to the anamorphic development of the larva in anostracans,
limb buds and setae on the limb buds develop gradually. Even small limb buds just emerging
from the body wall form the lobes of the adult limb and begin to develop setae with very small
shafts. The cellular composition of the nonsensory setae is uniform: all have six accessory cells,
discernable as three pairs whose size and positions are distinct. These cells are clearly identified
in the developing limb bud by the hypertrophy and alignment of their nuclei. Although the pairs
of accessory cells have distinct nuclei and positions relative to the setae, their functions remain
unknown.
Even these two studies show that very different numbers of cells are involved in setal produc-
tion. Neither illuminate the lineage of setal forming cells. Indeed, there are no lineage-tracing
studies of cells that generate crustacean setae, and we do not know whether a lineage-based
development comparable to insects occurs. Comparisons of setal development within crusta-
ceans would be very useful in their own right, and they would help address some of the bigger
questions of the evolution of setae in arthropods. For example, although nonsensory bristles in
insects can be derived from sensory ones by apoptosis of the neuronal lineage, is there reason to
suppose that sensory setae actually evolved first? That is, might not there have been a selective
pressure for structural setae just as there was for sensory accessory cells? In general, the origins
of arthropod setae remain unexplored.
Genes Important in Limb Patterning Also Pattern Setae

Another reason to consider the development of crustacean setae is that a number of leg-patterning
genes contribute to patterning bristles or sense organs. This is not surprising since many pat-
terning genes have multiple functions. Nonetheless, it is interesting to consider whether dual
patterning might be a consequence, at least ancestrally, of coordination within the leg of axial
patterning and setae. For example, two of the main leg “gap” genes in Drosophila—Distal-less
and dachshund—additionally play a role of regulating sensory structures. Distal-less plays a
role in the development of certain sensory structures in Drosophila. Distal-less-negative clones
induced late in development during the third larval period in Drosophila are often associated
with anomalous bristle morphology (although it is not reported that cells specifically express
Distal-less; Campbell and Tomlinson 1998). Distal-less is required in cells that form bracts, which
are cuticular elaborations adjacent to the mechanosensory bristles of the leg (Held 2002). In
addition, Distal-less specifies Keilin’s organs, the larval leg sense organs that consist of three
bristlelike external sensilla (Cohen and Jü rgens 1989). Indeed, the earliest ideas of the multi-
functionality of Distal-less involved co-opting an ancestral function in the nervous system for
use in body wall extensions (Panganiban et al. 1997, Panganiban 2000, Mittmann and Scholtz
2001, Williams et al. 2002).
Mutations in dachshund, another leg “gap” gene, are known to cause fusions of leg seg-
ments. However, they also change the number and distribution of bristles (Mardon et al. 1994).
Similarly, Notch signaling, which helps position joints along the PD leg axis, is also used in the
early dete mination of sense organs (reviewed in Hartenstein 2005). In addition, pox-neuro
and BarH, two genes that play a role in forming tarsal joints, can also transform sense organs
(Awasaki and Kimura 2001). Thus, numerous genes that play a role in limb patterning also play
a role in forming sensory structures.
Are Evolutionarily Relevant Substructures within Limbs Formed by

Developmentally Integrating Multiple Morphological Elements?
Given this kind of dual function in genes that pattern leg axes and sensory structures, it seems
possible that these two types of patterning were more closely linked ancestrally than they are in
Drosophila, with its highly specialized metamorphic development. Such linkage might be found
in arthropods like crustaceans that develop limbs directly. Certain patterns in crustacean leg
morphology could support this idea. For example, one notable regularity within limbs is the
position of setae at the distal margin of the limb podomere. There is a strong functional reason
for this position given that such setae can transmit information about the relative position of the
two limb joints. This function might be ancestral and would provide an apt selective scenario
for joints and sensory structures to be developmentally linked. Another morphological regular-
ity often found in crustacean limbs is the one-to-one correspondence between the annulation
and projecting setae in limbs that are multiannulate. Given that mutations in genes that regulate
joint formation can also change setal patterns, it seems plausible that the regulation of joints
and adjacent setae is mechanistically linked. Robust models of setal patterning in crustaceans
are a first step toward evaluating this hypothesis. Although the examples of structural linkage
I describe are hypothetical, they point to the fact that understanding such developmental link-
ages could provide new insights into homologies within crustacean legs, as well as the pathways
of limb diversification.
FUTURE DIRECTIONS
Comparative limb development is a wide open field in crustacean evolutionary morphology.

As shown at many points in this chapter, crustacean limbs are highly diverse both in their
basic morphology and in the transformations they undergo during the life cycle. This diversity
distinguishes them from most other arthropod groups and is part of what makes their study
so fascinating. Our developmental models still cannot explain variation among limbs of differ-
ent species. This is critical because crustacean limbs have diversified by varying their branches
and lobes, including the biramous branching of endopod and exopod and the medial and lat-
eral lobes that serve to specialize and differentiate limbs functionally. While it is remarkable
that crustacean (and arthropod) limbs have a conserved PD patterning module, we still need
to understand how the branches and lobes of limbs are patterned. We will be aided in this pur-
suit by techniques that are becoming easier to use in nonmodel organisms, for example, gene
sequencing and RNA interference. In addition, the search for other genes, not used in pattern-
ing Drosophila legs, is facilitated by the prevalence of genomic techniques. These advances will
allow both functional studies and much broader taxon sampling. Beyond the question of how
different limbs are patterned remains the question of how series of limbs are patterned, par-
ticularly since the metamorphic lifestyle of so many crustaceans means that a given segment
can develop morphologically diverse limbs during ontogeny. None of our models address such
metamorphic change, and yet this ability has permitted the specialization of larval lifestyles
radically distinct from the adult.
Finally, the field of comparative limb patterning has mainly focused on the generic Cartesian
axes used to pattern an outgrowth from the body wall. While this has shown some surprising
conservation, we have not yet begun linking that patterning to the details of the morphology
that make up the limbs. Indeed, for crustaceans, we lack even basic models as to how fundamen-
tal limb structures, such as muscles and setae, develop. Furthermore, exploring this interface
between patterning limb axes and patterning limb morphology may uncover functional links,
revealing biologically relevant units of development. If so, these developmentally operational
units in the limb could help resolve some of still tangled issues of homology between highly
divergent limbs.
ACKNOWLEDGMENTS
My thanks to M. Thiel and L. Watling for their comments and editing of this chapter and to
L. Nagy and K. Dunlap for critical readings. Ívan Hinojosa generously made the final Fig. 3.8
from my color original.
NOTES
1 Typical nomenclature is to write gene names and their abbreviations in italics and to write the protein
product of a gene in all capitals. However, to simplify the presentation, I have avoided abbreviations and
distinguishing between RNA and protein expression.
2 The function of extradenticle depends on its being transported to the nucleus. This occurs in the presence
of homothorax. Strictly speaking, when I refer to extradenticle, I am referring to this nuclear extradenticle,
in contrast to other extradenticle expression that may be present but is nonnuclear.
REFERENCES
Abu-Shaar, M., and R.S. Mann. 1998. Generation of multiple antagonistic domains along the proximodis-
tal axis during Drosophila leg development. Development 125:3821–3830.
Abzhanov, A., and T.C. Kaufman. 2000. Homologs of Drosophila appendage genes in the patterning of
arthropod limbs. Developmental Biology 227:673–689.

Angelini, D.R., and T.C. Kaufman. 2004 . Functional analyses in the hemipteran Oncopeltus fasciatus
reveal conserved and derived aspects of appendage patterning in insects. Developmental Biology
271:306–321.
Angelini, D.R., and T.C. Kaufman. 2005 . Insect appendages and comparative ontogenetics.
Developmental Biology 286:57–77.
Artavanis-Tsakonas, S., M.D. Rand, and R.J. Lake. 1999. Notch signaling: Cell fate control and signal
integration in development. Science 284:770–776.
Averof, M., and S. Cohen. 1997. Evolutionary origin of insect wings from ancestral gills. Nature
385:627–630.
Averof, M., and N.H. Patel. 1997. Crustacean appendage evolution associated with changes in Hox gene
expression. Nature 388:682–686.
Awasaki, T., and K. Kimura. 2001. Multiple function of poxn gene in larval PNS development and in adult
appendage formation of Drosophila. Development Genes and Evolution 211:20–29
Bateson, W. 1894 . Materials for the study of variation. Macmillan, London .
Beermann, A., M. Aranda, and R. Schroder. 2004 . The Sp8 zinc-finger transcription factor is involved in
allometric growth of the limbs in the beetle Tribolium castaneum. Development 131:733–742.
Beermann, A., D.G. Jay, R.W. Beeman, M. Hulskamp, D. Tautz , and G. Jurgens. 2001. The Short antennae
gene of Tribolium is required for limb development and encodes the orthologue of the Drosophila
Distal-less protein. Development 128:287–297.
Bishop, S.A., T. Klein, A.M. Arias, and J.P. Couso. 1999. Composite signaling from Serrate and Delta
establishes leg segments in Drosophila through Notch. Development 126:2993–3003.
Blair, S.S. 1999. Drosophila imaginal disc development: Patterning the adult fly. in V. E.A. Russo, D.
Cove, L. Edgar, R. Jaenisch, and F. Salamini, editors. Development, genetics, epigenetics and envi-
ronmental regulation. Springer, Heidelberg.
Boxshall, G. A. 2004 . The evolution of arthropod limbs. Biological Reviews 79:253–300.
Brook , W.J., F.J. Diza-Benjumea, and S.M. Cohen. 1996. Organizing spatial pattern in limb development.
Annual Review of Cell and Developmental Biology 12:161–180.
Browne, W.E., A.L. Price, M. Gerberding , and N.H. Patel. 2005 . Stages of embryonic development in the
amphipod crustacean, Parhyale hawaiensis. Genesis 42:124–149.
Campbell, G., and A. Tomlinson. 1995 . Initiation of proximodistal axis in insect legs. Development
121:619–628.
Campbell, G., and A. Tomlinson. 1998. The roles of the homeobox genes aristaless and Distal-less in pat-
terning the legs and wings of Drosophila. Development 125:4483–4493.
Cohen, B., A.A. Simcox , and S.M. Cohen. 1993. Allocation of the imaginal primordia in the Drosophila
embryo. Development 117:597–608.
Cohen, S.M. 1990. Specification of limb development in the Drosophila embryo by positional cues from
the segmentation genes. Nature 343:173–177.
Cohen, S. M., and G. Jü rgens. 1989. Proximal-distal pattern formation in Drosophila: Graded require-
ment for Distal-less gene activity during limb development. Roux’s Archive for Developmental
Biology 198:157–169.
Damen, W.G., T. Saridaki, and M. Averof. 2002. Diverse adaptations of an ancestral gill: A common evo-
lutionary origin for wings, breathing organs, and spinnerets. Current Biology 12:1711–1716.
Dearden, P., and M. Akam. 2000. A role for Fringe in segment morphogenesis but not segment formation
in the grasshopper, Schistocerca gregaria. Development Genes and Evolution 210:329–336.
de Celis, J.F., D.M. Tyler, J. de Celis, and S.J. Bray. 1998. Notch signaling mediates segmentation of the
Drosophila leg. Development 125:4617–4626.
Dohle, W., and G. Scholtz. 1988. Clonal analysis of the Crustacean segment—the discordance between
genealogical and segmental borders. Development 104:147–160.
Deutsch, J.S., and E. Mouchel-Vielh. 2003. Hox genes and the crustacean body plan. BioEssays 25:878–887.
Franch-Marro, X., N. Mart í n, M. Averof, and J. Casanova. 2005 . Association of tracheal placodes with
leg primordia in Drosophila and implications for the origin of insect tracheal systems. Development
133:785–790.
Freeman, J.A., L.B. Cheshire, and T.H. MacRae. 1992. Epithelial morphogenesis in developing Artemia: The
role of cell replication, cell shape change, and the cytoskeleton. Developmental Biology 152:279–292.
Fristrom, D., and J.W. Fristrom. 1993. The metamorphic development of the adult epidermis. Pages
843–897 in M. Bate and A. Mart ı nez-Arias, editors. The development of Drosophila melanogaster.
Cold Spring Harbor Laboratory Press, New York .
Gonzalez-Crespo, S., and G. Morata. 1996. Genetic evidence for the subdivision of the arthropod limb
into coxopodite and telopodite. Development 122:3921–3928.
Guerao, G., K. Anger, U. Nettelmann, and C.D. Schubart. 2004 . Complete larval and early juvenile
development of the mangrove crab Perisesarma fasciatum (Crustacea: Brachyura: Sesarmidae)
from Singapore, with a larval comparison of Parasesarma and Perisesarma . Journal of Plankton
Research 26:1389–1408.
Gurney, R. 1942. Larvae of decapod Crustacea. Ray Society, London .
Guse. G.W. 1983. Ultrastructure, development, and moulting of the aesthetascs of Neomysis integer and
Idotea baltica (Crustacea, Malacostraca). Zoomorphology 103:121–133.
Hallberg , E., and B.S. Hansson. 1999. Arthropod sensilla: Morphology and phylogenetic considerations.
Microscopy Research and Technique 47:428–439.
Hartenstein, V. 2005 . Development of insect sensilla. Pages 379–419 in L. Gilbert, K. Iatrou, and S. Gill,
editors. Comprehensive molecular insect science, Vol. 1, Reproduction and development. Elsevier,
Oxford .
Hejnol, A., and G. Scholtz. 2004 . Clonal analysis of Distal-less and engrailed expression patterns dur-
ing early morphogenesis of uniramous and biramous crustacean limbs. Development Genes and
Held, L.I. 1995 . Axes, boundaries and coordinates: The ABCs of fly leg development. BioEssays
17:721–732.
Held, L.I. 2002. Bristles induce bracts via the EGFR pathway on Drosophila legs. Mechanisms of
Inoue, Y., T. Mito, K. Miyawaki, K. Matsushima, Y. Shinmyo, T.A. Heanue, G. Mardon, H. Ohuchi, and
S. Noji. 2002. Correlation of expression patterns of homothorax, dachshund, and Distal-less with the
proximodistal segmentation of the cricket leg bud. Mechanisms of Development 113:141–148.
Jockusch, E.L., C. Nulsen, S.J. Newfeld, and L.M. Nagy. 2000. Leg development in flies versus grasshop-
pers: Differences in dpp expression do not lead to differences in the expression of downstream
components of the leg patterning pathway. Development 127:1617–1626.
Jockusch, E.L., T.A. Williams, and L.M. Nagy. 2004 . The evolution of patterning of serially homologous
appendages in insects. Development Genes and Evolution 214:324–338.
Kojima, T. 2004 . The mechanism of Drosophila leg development along the proximodistal axis.
Development Growth and Differentiation 46:115–129.
Kreissl, S., A. Uber, and S. Harzsch. 2008. Muscle precursor cells in the developing limbs of two isopods
(Crustacea, Peracarida): An immunohistochemical study using a novel monoclonal antibody
against myosin heavy chain. Development Genes and Evolution 218:253–265.
Lai, E.C., and V. Orgogozo. 2004 . A hidden program in Drosophila peripheral neurogenesis revealed:
Fundamental principles underlying sensory organ diversity. Developmental Biology 269:1–17.
Lecuit, T., and S.M. Cohen. 1997. Proximal-distal axis formation in the Drosophila leg. Nature
388:139–145.
Manzanares, M., T.A. Williams, R. Marco, and R. Garesse. 1996. Segmentation in the crustacean
Artemia as revealed by engrailed protein distribution. Roux’s Archive for Developmental Biology
205:424–431.
Mardon, G., N.M. Solomon, and G.M. Rubin. 1994 . dachshund encodes a nuclear protein required for
normal eye and leg development in Drosophila. Development 120:3473–3486.

McKay, D.J., C. Estella, and R.S. Mann. 2009. The origins of the Drosophila leg revealed by the
cis-regulatory architecture of the Distalless gene. Development 136:61–71.
Mirth, C., and M. Akam. 2002. Joint development in the Drosophila leg: Cell movements and cell popula-
tions. Developmental Biology 246:391–406.
Mitchell, B., and S.T. Crews. 2002. Expression of the Artemia trachealess gene in the salt gland and epi-
pod. Evolution and Development 4:344–353.

Mittmann, B., and G. Scholtz. 2001. Distal-less expression in embryos of Limulus polyphemus Chelicerata,
Xiphosura and Lepisma saccharina Insecta, Zygentoma suggests a role in the development of mech-
anoreceptors, chemoreceptors, and the CNS. Development Genes and Evolution 211:232–243.
Mouchel-Vielh, E., C. Rigolot, J. Gibert, and J.S. Deutsch. 1998. Molecules and the body plan: The Hox
genes of cirripedes Crustacea. Molecular Phylogenetics and Evolution 9:382–389.
Nagy, L.M., and T.A. Williams. 2001. Comparative limb development as a tool for understanding the
evolutionary diversification of limbs in arthropods: Challenging the modularity paradigm . Pages in
G.P. Wagner, editor. The character concept in evolutionary biology. Academic Press, New York.
Nulsen, C., and L.M. Nagy. 1999. The role of wingless in the development of multi-branched crustacean
limbs. Development Genes and Evolution 209:340–348.
Olesen, J., S. Richter, and G. Scholtz. 2001. The evolutionary transformation of phyllopodous to stenopo-
dous limbs in the Branchiopoda Crustacea—is there a common mechanism for early limb develop-
ment in arthropods? International Journal of Developmental Biology 45:869 –876.
Panganiban, G. 2000. Distal-less function during Drosophila appendage and sense organ development.
Developmental Dynamics 218:554–562.
Panganiban, G., S.M. Irvine, C. Lowe, H. Roehl, L.S. Corley, B. Sherbon, J.K. Grenier, J.F. Fallon, J.
Kimble, M. Walker, G.A. Wray, B.J. Swalla, M.Q. Martindale, and S.B. Carroll. 1997. The origin
and evolution of animal appendages. Proceedings of the National Academy of Sciences of the USA
94:5162–5166.
Panganiban, G., A. Sebring , L. Nagy, and S. Carroll. 1995 . The development of crustacean limbs and the
evolution of arthropods. Science 270:1363–1366.
Patel, N.H., T.B. Kornberg, and C.S. Goodman. 1989. Expression of engrailed during segmentation in
grasshopper and crayfish. Development 107:2 01–212.
Pavlopoulos, A., Z. Kontarakis, D.M. Liubicich, J.M. Serano, M. Akam, N.H. Patel, and M. Averof. 2009.
Probing the evolution of appendage specialization by Hox gene misexpression in an emerging
model crustacean. Proceedings of the National Academy of Sciences of the USA 106:13897–13902.
Posakony, L.G., L.A. Raftery, and W.M. Gelbart. 1991. Wing formation in Drosophila melanogaster
requires decapentaplegic gene function along the anterior–posterior compartment boundary.
Mechanisms of Development 33:69 –82.
Prpic , N.-M., and M.J. Telford. 2008. Expression of homothorax and in the legs of the crustacean Parhyale
evidence for a reversal of gene in the pancrustacean lineage. Development Genes and Evolution
218:333–339.
Prpic , N.-M., B. Wigand, W.G.M. Damen, and M. Klinger. 2001. Expression of dachshund in wild-type
and Distal-less mutant Tribolium corroborates serial homologies in insect appendages. Development
Genes and Evolution 211:467–477.
Queinnec , E., E. Mouchel-Vielh, M. Guimonneau, J.-M. Gibert, Y. Turquier, and J.S. Deutsch. 1999.
Cloning and expression of the engrailed.a gene of the barnacle Sacculina carcini. Development Genes
and Evolution 209:180–205.
Rauskolb, C. 2001. The establishment of segmentation in the Drosophila leg. Development 128:4511–4521.
Rauskolb, C., and K.D. Irvine. 1999. Notch-mediated segmentation and growth control of the Drosophila
leg. Developmental Biology 210:339 –350.
Rogers, B.T., M.D. Peterson, and T.C. Kaufman. 2002. The development and evolution of insect mouth-
parts as revealed by the expression patterns of gnathocephalic genes. Evolution and Development
4:96 –110.
Roy, S., and K. VijayRaghavan. 1999. Muscle pattern diversification in Drosophila: The story of imaginal
myogenesis. BioEssays 21:486 –498.
Scholtz , G. 1990. The formation, differentiation and segmentation of the post-naupliar germ band of the
amphipod Gammarus pulex L. (Crustacea, Malacostraca, Peracarida). Proceedings of the Royal
Scholtz , G., W. Dohle, R.E. Sandeman, and S. Richter. 1993. Expression of engrailed can be lost and
regained in cells of one clone in crustacean embryos. International Journal of Developmental
Biology 37:299 –304.
Scholtz , G., N.H. Patel, and W. Dohle. 1994 . Serially homologous engrailed stripes are generated via
different cell lineages in the germ band of amphipod crustaceans (Malacostraca, Peracarida).
International Journal of Developmental Biology 38:471–478.
Schubiger, G. 1971. Regeneration, duplication, and transdetermination in fragments of the leg disc of
Drosophila melanogaster. Developmental Biology 26:277–295.
Serrano, N., and P.H. O’Farrell. 1997 Limb morphogenesis: Connections between patterning and
growth. Current Biology 7:R186–R195.
Sewell, W., T.A. Williams, J. Cooley, M. Terry, R. Ho, and L.M. Nagy. 2008. Evidence for a novel role for
dachshund in patterning the proximal leg. Development Genes and Evolution 218:293–305.
Shiga, Y., R. Yasumoto, H. Yamagata, and S. Hayashi. 2002. Evolving role of Antennapedia protein in
arthropod limb patterning. Development 129:3555–3561.
Soler, C., M. Daczewska, J.P. Da Ponte, B. Dastugue, and K. Jagla. 2004 . Coordinated development of
muscles and tendons of the Drosophila leg. Development 131:6041–6051.
Snodgrass, R.E. 1956. Crustacean metamorphoses. Smithsonian Miscellaneous Collections 131:1–78.
Sun, X., F.V. Mariani, and G.R. Martin. 2002. Functions of FGF signaling from the apical ectodermal
ridge in limb development. Nature 418:501–508
Taylor, J., and P.N. Adler. 2008. Cell rearrangement and cell division during the tissue level morphogen-
esis of evaginating Drosophila imaginal discs. Developmental Biology 313:739 –751.
Van Valen, L.M. 1993. Serial homology: The crests and cusps of mammalian teeth. Acta Palaeontologica
Polonica 38:145–158.
Wagner, G.P. 1989. The origin of morphological characters and the biological basis of homology.
Evolution 43:1157–1171.
Williams, T.A. 1998. Distalless expression in crustaceans and the patterning of branched limbs.
Development Genes and Evolution 207:427–434.
Williams, T.A. 2004 . The evolution and development of crustacean limbs: An analysis of limb homolo-
gies. Pages 169–193 in G. Scholtz , editor. Evolutionary developmental biology of Crustacea.
Crustacean Issues, Vol. 15. Balkema, Lisse, The Netherlands.
Williams, T.A. 2007a . Limb morphogenesis in the branchiopod crustacean, Thamnocephalus platyurus,
and the evolution of proximal limb lobes within Anostraca. Journal of Zoological Systematics and
Evolutionary Research 45:191–201.
Williams, T.A. 2007b. Development of setal cells in the crustacean, Thamnocephalus platyurus.
Arthropod Structure and Development 36:63–76.
Williams, T.A. 2008. Early Distal-less expression in a developing crustacean limb bud becomes restricted
to setal forming cells. Evolution and Development 10:114–120.
Williams, T.A., and G.B. Muller. 1996. Limb development in a primitive crustacean, Triops longicauda-
tus: Subdivision of the early limb bud gives rise to multibranched limbs. Development Genes and
Williams, T.A., and L.M. Nagy. 1996. Comparative limb development in insects and crustaceans.
Seminars in Cell and Developmental Biology 7:615–628.
Williams, T.A., and L.M. Nagy. 2001. Developmental modularity and the evolutionary diversification
of arthropod limbs. Journal of Experimental Zoology, Molecular and Developmental Evolution
291:241–257.
Williams, T.A., C. Nulsen, and L.M. Nagy. 2002. A complex role for Distal-less in crustacean appendage
development. Developmental Biology 241:302–312.
Wolff, C., and G. Scholtz. 2008. The clonal composition of biramous and uniramous arthropod limbs.
4
THE CRUSTACEAN CARAPACE: MORPHOLOGY, FUNCTION,
DEVELOPMENT, AND PHYLOGENETIC HISTORY
Jørgen Olesen
Abstract
A carapace (a shield extending from the head region and enveloping a smaller or larger part
of the body) is a characteristic feature of many crustaceans. This chapter reviews functional,
ontogenetic, and evolutionary aspects of the crustacean carapace. Carapace morphology in
Crustacea shows much variation, which is reflected in the many functions present in the vari-
ous subgroups. Among the more widespread functions of carapaces are that in many taxa, they
provide hydrodynamic advantages, offer protection, or form a feeding chamber, a respira-
tion chamber, or a brooding chamber. Special attention is devoted to the Branchiopoda and
Malacostraca, which both show a large variation in carapace morphology and ontogeny. The
influential textbook by Calman (1909) on crustacean morphology and systematics suggested
that a carapace was present primitively in both Malacostraca and Crustacea. This assumption
was long unchallenged, but a few decades ago attempts were made to invalidate/reject Calman’s
carapace hypothesis. Here it is argued that the best starting point may still be to assume homol-
ogy, at least within Malacostraca. Whether a carapace is homologous between major crustacean
taxa is more uncertain due to a general large morphological disparity, but most major taxa have
members with a “classical Calman type” of carapace extending from the rear of the head region
either as adults or as larvae. The information from the Cambrian “Orsten” crustaceans is ambig-
uous on this question. Some taxa, such as Rehbachiella and Walossekia, have a classical type of
carapace, while others, such as Skara and the even older Yicaris, lack a carapace entirely.
INTRODUCTION
A carapace, broadly defined as a shield extending from the head region and enveloping a
smaller or larger part of the body, is a characteristic feature of many crustaceans, for example,
103
B D
1) 2) 3)
Fig. 4.1.
Examples of carapace-bearing nonmalacostracan Crustacea. (A) Triops cancriformis (Branchiopoda:
Notostraca) (from Gruner 1993). (B) Cyzicus sp. (Branchiopoda: Spinicaudata) mating (from Gravier
and Mathias 1930). (C) Bythotrephes longimanus (Branchiopoda: Cladocera) (from Lilljeborg 1901). (D)
Chonopeltis inermis (Branchiura) (from Fryer 1956). (E) Euphilomedes aspera (Ostracoda) (from Müller
1894). (A–E all taken from Gruner 1993, with permission from Gustav Fischer Verlag). (F) Metamorphosis
of Lepas (Cirripedia): 1, cypris larva; 2, attached larva; 3, young Lepas still surrounded by loosened cyprid
carapace (modified from Korschelt and Heider 1890). Arrowheads indicate the carapace.
branchiopods, ostracods, and decapods (Figs. 4.1, 4.2). The term carapace is traditionally used
for various types of shields or outgrowths covering the body of many crustaceans, but its use is
not restricted to crustaceans. The word is also used for the shields of a variety of noncrustacean
arthropod fossils and even for the dorsum of the fused head and thorax in spiders or horseshoe
crabs, as well as the well-known shell of a turtle.
Crustacea is a large taxon (>60,000 species; see Martin and Davis 2006) with an almost
unchallenged variation in morphological appearance spanning from the cave-dwelling, worm-
like remipedians to the large claw-bearing lobsters. An equal variation is seen in the ways
Crustacea have developed shields (carapaces) to cover the body. Sometimes the shield is fused
with the body, as in crabs and lobsters (Fig. 4.2); in other species it is a free shield attached
only anteriorly, as in leptostracans (Fig. 4.2A) or clam shrimps (Spinicaudata, Laevicaudata)
(Fig. 4.1B); in others it is modified to a dorsal brood pouch, as in raptorial cladocerans
(Fig. 4.1C). The large variation in carapace morphology in Crustacea is reflected in the many
known (or assumed) functions of carapaces in the various crustacean subgroups. Among the
most important functions, not all of which apply to all taxa, are protection, respiration cham-
ber, filtration chamber, brood chamber, and hydrodynamic streamlining.
The Crustacean Carapace 105
A
B
C D
E F G
Fig. 4.2.
Examples of carapace-bearing malacostracans. (A) Nebalia geoffroyi (Leptostraca) (from Claus
1888). (B) Squilla mantis (Stomatopoda) (from Giesbrecht 1916). (C) Spelaeogriphus lepidops
(Spelaeogriphacea) (from Gordon 1960). (D) Euphausia superba (Euphausiacea) (from Gruner 1993).
(E) Mysis relicta (Mysida) (Tattersal and Tattersal 1951). (F) Callinectes sapidus (Brachyura) (from Rathbun
1930). (G) Nannastacus unguiculatus (Cumacea) (from Gruner 1993). (H) Penaeus setiferus (Penaeidae)
(from Pérez Farfante 1988). (B-H all taken from Gruner 1993, with permission from Gustav Fischer
Verlag). Arrowheads indicate the carapace.
Calman (1909), in his classical and influential treatment of crustacean morphology and
systematics, suggested that the carapace is a primitive character in Crustacea. In the 1980s
and 1990s, the homologies and evolution of the carapace were discussed intensively for vari-
ous crustacean groups (Dahl 1983, 1991, Newman and Knight 1984, Walossek 1993, Fryer 1996,
Watling 1999), but since then this subject has rarely been touched. Considering the variation in
morphology, function, and development of carapace structures within Crustacea, it is not sur-
prising that the evolution of this structure has generated much discussion. One of the key ques-
tions in the earlier arguments by Dahl (1991) and Newman and Knight (1984) was whether all
crustacean carapaces are homologous or, phrased differently, whether a carapace is ancestral in
Crustacea. This question is still difficult to answer, but at least the discovery of well-preserved,
fossil microcrustaceans from the Cambrian, some of which have classical Calman-type cara-
paces extending from the rear of the cephalic region (e.g., Mü ller and Walossek 1988, Walossek
1993), provides some hints of early evolution of the carapace.
The wide occurrence of carapace structures in representatives of nearly all higher crusta-
cean taxa (see Figs. 4.1, 4.2), and the fact that so many different functions can be attributed
to the carapace in different taxa (Table 4.1) suggests that a carapace has been important in
Table 4.1. Overview of carapace morphology and function in recent Crustacea.
General morphology in adults Important functions in adults

Branchiopoda Much variation. Notostraca: carapace dorsal shield continu- General protection of body and limbs (most taxa); streamlining
(Figs. 4.1A–C, ous with head; Spinicaudata, Laevicaudata, and Cyclestherida: during swimming (some cladocerans and Notostraca); facilitates
4.4, 4.5A, 4.7A–E, carapace bivalved, capable of enclosing entire body (or most); burrowing (Notostraca); part of respiration/feeding current sys-
4.8–4.14) Cladocera: most taxa with bivalve carapace covering body but not tem (“Conchostraca” and Cladocera); protection of eggs/embryos
head; raptorial cladocerans (Onychopoda, Haplopoda): carapace (Notostraca) or as dorsal brood chamber (“Conchostraca” and
as dorsal brood pouch without free valves covering body. Cladocera); housing long, curled tubules of maxillary glands.
Branchiura All branchiurans with flat, shieldlike carapace (e.g., Møller Smooth, flattened carapace together with generally low pro-
(Fig. 4.1D) 2009) with head integrated into anterior part and with free pos- file of all branchiurans reduces frictional drag when attached
terior lobes overhanging varying parts of body; carapace evenly to hosts; general protection of body and limbs; houses widely
rounded anteriorly in some taxa (Dolops and some Argulus) and branched digestive system; carapace lobes ventral surface with
in other taxa divided into lobes (Chonopeltis). so-called respiratory areas involved in osmoregulation (Haase
1975, Boxshall and Jaume 2009); houses spermatophore glands in
Dolops (Fryer 1960).
Thecostraca Carapace of head shield type in cyprid or cypridiform stages of Hydrodynamics (e.g., Crisp 1955, Walker and Lester 2000, Walker
(Fig. 4.1F) all thecostracans (e.g., Høeg et al. 2004); Facetotecta: carapace 2004); general protection of body and limbs; surface with sensory
more or less maintains naupliar shape (not bivalved) overhanging organs such as “lattice organs” (Jensen et al. 1994, Rybakov et al.
body (Høeg et al. 2004); Ascothoracida and Cirripedia: carapace 2003).
bivalved with dorsal hinge line (Høeg et al. 2009); adult cirri-
pedes (barnacles, etc.): no carapace, but carapace valves of cyprid
larvae are ontogenetic precursors to fleshy mantle with calcified
shell plates (e.g., Calman 1909, Glenner and Høeg 1993).
Ostracoda Carapace most often calciferous and bivalved with valves held General protection of limbs and body; respiration (e.g., Abe and
(Figs. 4.1E, 4.7F) together dorsally by ligament, often also by hinge (Maddocks Vannier 1995); spaces between internal lamellae of carapace valves
1992); a few recent taxa (Swanson 1989) have a univalved are continuations of body cavity and may house organs related to
carapace. reproduction, digestion, nervous system (Maddocks 1992).
Leptostraca Large, bivalved, but with no dorsal hinge; dorsum of carapace General protection of body and limbs; form sides of filtra-
(Figs. 4.2A, 4.16A,B) continues anteriorly into small articulated rostral plate; in most tion chamber (see Cannon 1927); respiration chamber, but gas
taxa carapace covers phyllopodous thoracopods laterally (e.g., exchange over inner surface uncertain (see chapter 14 in this vol-
Nebalia), but in some taxa (e.g., Paranebalia and Nebaliopsis) tho- ume); hydrodynamics; rostral plate acts as ram during burrowing
racopods extend between valves ventrally. (Vannier et al. 1997); embryos carried ventrally by thoracopods
between carapace valves.
Euphausiacea Carapace fused with thorax dorsally so that cephalon and thorax Hydrodynamics; inner side possesses very thin cuticle so proba-
(Fig. 4.2D) form one piece (cephalothorax); a short spine extends in the mid- bly respiratory (Zimmer and Gruner 1956) (see chapter 14); carry-
line anteriorly; laterally carapace folds relatively short not covering compound organs dorsally (function unknown) (Mauchline
ing gills of thoracopods. and Nemoto 1977).
Decapoda Carapace fused with thorax dorsally so that cephalon and thorax General protection due to heavy calcification; hydrodynamics;
(Figs. 4.2F,H, 4.3, form one piece (cephalothorax); lateral folds of carapace form provides robust attachment sites for limb musculature; more
4.5B–D, 4.15C, gill chambers; much taxon-specific variation in general carapace room for internal organs; carapace fused with thorax (cephalot-
4.16E,F) morphology. horax) may facilitate backward swimming as performed during
“escape reaction”; sides of carapace (branchiostegites) form gill
chambers closed to varying degree in various taxa; branchioste-
gites involved in respiration known only for few species (see chap-
ter 14); sound production (Henninger and Watson 2005).
Stomatopoda Carapace of cephalothorax type incorporating head and one or Sound production by carapace vibration (Patek and Caldwell
(Figs. 4.2B, 4.15B, two thorax segments (number uncertain since this body region is 2006); general protection of mouth parts and bases of maxilli-
4.16C,D) compressed); cephalothorax has free lateral margins; anteriorly is peds; female carapace grabbed by male during copulation (e.g.,
median rostral plate articulated to cephalothorax; some taxa with Dingle and Caldwell 1972); carapace length shorter than bur-
distinct longitudinal keel in the midline of the cephalothorax and row width (probably to enable possibility of turning around)
with additional longitudinal lateral ridges. (Atkinson et al. 1997).
Mysidacea Carapace typically large and with free folds posteriorly and ven- Mysida: carapace forms a respiratory chamber with gas exchange
(Figs. 4.2E, 4.6A,B) trally covering most of thorax and the basal parts of the thoraco- taking place on the inner surface (Mayrat et al. 2006, Wirkner and
pods; carapace in Mysida dorsally fused with first three thoracic Richter 2007); respiratory current is produced by lamellar epipod
segments (in Stygiomysis with first four) (Gruner 1993). of first thoracopod (Cannon and Manton 1927); Lophogastrida:
carapace previously considered nonrespiratory (but see Wirkner
and Richter 2007).
(Continued)
General morphology in adults Important functions in adults

Cumacea Carapace of cephalothorax type incorporating dorsally anterior Respiration/feeding chambers; water current enters ventrally
(Figs. 4.2G, 4.6D–F) three or four thoracic segments (sometimes also segments 5 and and leaves anteriorly in Diastylis (but see text) generated by mov-
6). The lateral lobes of carapace form chambers closed posteriorly able and ventilatory epipod of maxilliped (Calman 1909, Oelze
(comparable to gill chambers in brachyurans) (Zimmer 1941). 1931, Zimmer 1932; Dennell 1937).
Tanaidacea Carapace of cephalothorax type incorporating dorsally two Respiration chambers with inner side being involved in gas
(Fig. 4.6G,H) (rarely three) thoracic segments; lateral carapace folds cover exchange (e.g., Tanais cavolinii) (Lauterbach 1970, Johnson and
mouth appendages laterally, forming semiclosed lateral respira- Attramadal 1982).
tory chambers; posteriorly with a pair of respiratory pores at edge
of carapace.
Thermosbaenacea In Thermosbaena mirabilis short carapace extends from head to Respiratory chamber; inner side of carapace with epithelium
(Figs. 4.6C, 4.7G) posterior border of fourth thoracic segment; dorsally fused with containing system of vascular lacunae connected to perivisceral
first thoracic segment (Barker 1962); lateral folds of carapace and pericardial sinuses (Siewing 1958); epipodite of the maxilli-
extend anteriorly and cover lateral bases of mouth parts and first ped beat within branchial chambers to draw inhalant respiratory
and second antennae. current (Barker 1962); ovigerous females carry embryos under
enlarged carapace.
Speleogriphacea In Spelaeogriphus lepidops short carapace, which extends from At inside is “oval patch” that may be respiratory (Gordon 1957,
(Fig. 4.2C) head posteriorly, consists of pair of lateral lobes overhanging Grindley and Hessler 1971).
anterior somites.
Mictacea Carapace not developed posteriorly but small lateral carapace Lateral carapace lobes thought to be respiratory but maxillipedal
folds cover bases of maxillae mx1, mx2, and mxp (head fused to epipod associated with respiratory function, as in other taxa, lack-
first thoracic somite) (Bowman et al. 1985). ing carapace (Bowman et al. 1985).
crustacean evolution. The evolutionary success of crustaceans (or arthropods in general) is

probably very much linked to the plasticity of segmented limbs and the possibilities this has
given (e.g., Walossek 1993, Boxshall 2004; see also chapters 2 and 7 in this volume), but the car-
apace, with all the functional possibilities such a structure gives, seems to have been equally
important.
This chapter highlights the evolutionary significance of carapace structures within
Crustacea, both from a functional perspective and from a comparative morphological per-
spective. The following aspects are reviewed: (1) morphology and function of the carapace
in selected crustaceans; (2) case studies on the ontogeny of the carapace in two crustacean
key taxa, Branchiopoda and Malacostraca, both of which exhibit much variation in carapace
morphology and function of both larvae and adults, and both of which played a central role
when Calman formulated his crustacean carapace hypothesis; (3) critical summary of recent
discussions of Calman’s (1909) inf luential carapace hypothesis; and (4) Cambrian (“Orsten”)
evidence of carapace structures.
MORPHOLOGY AND FUNCTION OF THE CRUSTACEAN CARAPACE
The following is a brief overview of some of the main functions of the crustacean carapace, but
there are other functions not mentioned below (but see Table 4.1). The literature is vast, so this
summary is by no means exhaustive.
Hydrodynamics
Carapace morphology and hydrodynamics are linked in many ways in Crustacea. Most obvi-
ously, a carapace often provides general streamlining of the body surface and reduces drag
since it covers limbs and other projecting body parts. The carapace in Cambrian crustaceans
such as Rehbachiella (see Fig. 4.8, below) and Bredocaris probably had such a streamlining
function, since in these taxa the carapace is a simple posterior extension of the naupliar shield.
Indeed, hydrodynamic advantages may have been driving early carapace evolution (but were
probably also coupled with feeding advantages). Multiple other functions have evolved (feed-
ing, respiration, brooding), but hydrodynamic aspects remain important in many taxa.
Streamlining (reduction of drag) is important in two ways: (1) it allows for association
(attached or moving) with the substratum without being pulled off by water currents, and (2) it
increases swimming speed or makes it less costly. Here I present a few examples of crustacean
carapaces where hydrodynamic properties clearly play a significant role.
In the parasitic Branchiura (carp lice), streamlining as an adaptation to ectoparasitism on
fish has been taken to an extreme (Fig. 4.1D). The flattened carapace and the generally low body
profile effectively reduce drag when attached to the fish host. A general flattening of the body is
seen in many other crustacean taxa as a modification to their parasitic lifestyle (e.g., Copepoda,
Isopoda, Amphipoda) but without involving a carapace. Another example of a carapace with
clear hydrodynamic advantages is that of the cyprid larvae in cirripede crustaceans. The cyprid
is a larval type found only in cirripedes. It is a nonfeeding larva with a suite of specializations for
the purpose of locating a suitable substratum before irreversibly settling and molting to a juve-
nile cirripede (barnacles, gooseneck barnacles, or parasitic barnacles) (e.g., Høeg et al. 2004,
Høeg and Møller 2006) (Fig. 4.1F). Among the specializations of the cyprid larva is a bivalved
carapace capable of enclosing the body almost entirely between the valves. The hydrodynamic
advantages of this carapace shape for swimming cyprid larvae were explored by Walker (2004),
who found that cyprids of Heterosaccus lunatus were significantly faster than the naupliar
stages earlier in development, which reflects the efficiency of the fusiform shape of the cyprid.
In general, cyprid larvae swim faster than other similarly sized invertebrate larvae (Walker
et al. 1987). During the phase where the cyprid explores the substratum and where eventually
attachment takes place, a streamlined carapace is clearly important since it reduces drag from
strong currents and tides and allows the cyprids to rapidly scan multiple sites. Also in bran-
chiopods, such as notostracans, where the relatively flattened carapace forms one piece with the
head, streamlining during swimming is important (Fig. 4.1A), but this morphology may also be
related to its occasional burrowing behavior (Fryer 1988).
A well-known locomotory adaptation in malacostracan crustaceans is the “escape reaction,”
which involves repeated tail-flips performed by the often heavily muscularized pleon. In some
taxa a tail-flip results in a 180° turn along the body axis (e.g., stomatopods or thermosbaen-
aceans; see Olesen et al. 2006), while in heavily calcified decapods such as crayfish, a series
of repeated flips results in backward swimming. Jacklyn and Ritz (1986) compared the swim-
ming of scyllarid lobsters with that of a panulirid lobster with respect to how much the shape
of the carapace contributes to maneuverability during backward swimming. They found that
the flattened carapace in scyllarid lobsters, in contrast to panulirid lobsters, is formed in such
a way that it produces a hydrodynamic lift when the large flattened scales of the antennae are
lowered (Fig. 4.3). They also saw that the independent movement of the right and left antennal
scales, which are at the rear during backward swimming, may alter the water flow and change
the distribution of the lift and thereby control rolling or “pitching” during swimming. In the
panulirid lobster also examined by Jacklyn and Ritz (1986), the tail-flips were used only to travel
in straight lines and over a short distance during the escape response, which they explained as
the result of the production of a negligible amount of lift during each tail-flip and by the lack of
antennae shaped or positioned to control lift.
Another type of swimming among decapods is that found in portunid crabs, which
use their fifth pair of pereopods as swimming paddles (Fig. 4.2F). Portunids can swim in
all directions, slowly when going backward or forward but rapidly when moving sideways
(Lockhead 1961). Blake (1985) examined the hydrodynamic properties of the carapace of
Callinectes sapidus. He found that f luid resistance (drag) was least when the side of the cara-
pace was oriented at right angles to the f low, which was interpreted as an adaptation to side-
ways high-speed swimming. Blake (1985) also found that the carapace of Callinectes in general
is adapted for minimum resistance and to generate hydrodynamic lift at low speeds during
forward swimming.
Feeding
In a number of well-known examples among crustaceans, the carapace plays a direct role in the
feeding process. In branchiopods (except some raptorial cladocerans), the beating of the trunk
limbs sets up a powerful current of water that is drawn in medially between the limbs and then
expelled laterally, a current that is an important part of the feeding process and sometimes also
in locomotion (e.g., Anostraca and Notostraca). In diplostracan branchiopods, where a large and
often bivalved carapace is present, this current is mostly used for feeding only. In laevicauda-
tan branchiopods, which have a large and globular carapace (see Figs. 4.7A, 4.12C, below), the
carapace plays a role in setting up the feeding current. The exopods of the trunk limbs fit neatly
against the inner wall of the carapace, thereby sealing the interlimb spaces laterally and creating
a vacuum in these spaces, with the result that water is drawn medially into the food groove when
the limbs are beating metachronically (Fryer and Boxshall 2009). Laevicaudatan branchiopods
are not true filtrators, but the basic principles of how the feeding current is set up are the same as
in most other branchiopods. In cladocerans such as Daphnia, a feeding current is generated in a
largely similar way (see Fryer 1991), and also here the carapace plays a role in guiding the currents
1)
2)
3)
B L-
L+
Fig. 4.3.
Hydrodynamics of the scyllarid Ibacus peronii. (A) Three different types of backward swimming (1–3).
The propulsion is generated with repeated tail-flips. The carapace and the antennal scales together form
an effective aerofoil profile resulting in lift. The swimming direction is controlled by changing the angles
of the antennal scales. (B) By changing the articulation angle of the flattened antennal scales, the distri-
bution of the lift can be altered so that pitching and rolling movements are created. L– and L+ indicate a
downward- and upward-directed lift, respectively, when one antennae (right) is raised and the other (left)
is lowered; d indicates the perpendicular distance from rolling axis to the point of application of the result-
ant lift forces. From Jacklyn and Ritz (1986), with permission from Elsevier.
(Fig. 4.4A,B). A number of cladoceran branchiopods have exploited niches where carapace spe-
cializations and function go hand in hand. For example, the daphniid genera Scapholeberis and
Megafenestra have a modified ventral carapace in such a way that they are capable of suspending
themselves in an inverted position from the surface film of water (e.g., Fryer 1991) (Fig. 4.4C,D).
In general, modifications of the ventral carapace margins have been important within Cladocera
C
A
D
water entering
carapace chamber
G
Exhalant current
F H
E
Fig. 4.4.
The carapace as a feeding chamber and modifications of ventral carapace margins in cladoceran
Branchiopoda. (A and B) Daphnia galeata (Daphniidae), with carapace drawn transparent to show feeding
appendages (A) and schematic drawing showing where feeding/respiration currents enter and leave the
carapace chamber (B). (C and D) Scapholeberis mucronata (Daphniidae) using modifications of ventral
carapace margins to suspend itself in an inverted position from the surface film of water (C) and showing
ventral carapace modifications (D). (E and F) Peracantha truncata (Chydoridae) crawling over the sur-
face when balancing on the ventral margins. (G and H) Graptoleberis testudinaria (Chydoridae) seen from
below (G) and behind (H) as it glides over a surface. Note the row of long setae on the ventral carapace
margins, which seals the carapace chamber when gliding. A–D from Fryer (1991), and E–H from Fryer
(1968), with permission from the Royal Society of London.
(e.g., Fryer 1968, 1991, Smirnov and Kotov 2009), but especially within Chydoridae this has been
an evolutionary trend. Fryer (1968) described a number of cases where the morphology of the
ventral carapace margins are important for crawling while food is collected in various ways from
the substratum by the trunk limbs (e.g., Fig. 4.4E–H). In the least specialized forms, such as
Alonopsis elongata, the setae on the ventral carapace margin are in contact with the substratum
on which it balances when it crawls forward by means of the first trunk limbs. Specializations
for crawling have been further exploited by Alonella exigua, which has more ventral modifica-
tions (e.g., more ventral setae, wider ventral flange). It is capable of largely sealing the carapace
chamber and then pumping water from it, which maintains a pressure difference between the
water inside and outside, enabling it to cling to and crawl over surfaces like a fly on a ceiling
(Fryer 1968). Graptoleberis testudinaria has established an almost entirely water-tight seal with a
very wide ventral flange and specialized setae (Fryer 1968) (Fig. 4.4G,H), enabling it to slide over
surfaces like a gastropod mollusc by setting up a pressure difference between the water inside and
outside the carapace chamber.
Species from the genus Nebalia (Leptostraca) spend much of their life burrowed in mud.
They have a large, bivalved carapace that constitutes the lateral sides of a large filtration cham-
ber. Cannon (1927) reported that the phyllopodous trunk limbs produce a water current, which
enters the filtration chamber anteriorly and leaves it posteroventrally, from which particles
are being filtered out by the setae on the limbs. According to Cannon (1927), the anterior free-
moving part of the carapace, the rostrum, can be depressed and thereby appears to control the
current entering the filtration chamber. Vannier et al. (1997) suggested that the rostrum acts as
a ram during burrowing, preventing large particles from entering the filtration chamber from
anterior (see Fig. 10.1D in chapter 10 in this volume).
Respiration
In a number of examples within the Crustacea, the carapace forms a respiration chamber in
which gas exchange takes place, commonly over gills situated within the chamber (decapods),
but sometimes directly over the inner side of the carapace (branchiopods, ostracods, peracarid
malacostracans). There are even cases where the carapace chamber functions partially as a lung,
as it contains air, which is used for respiration while the animal is on land (e.g., grapsid or ocy-
podid crabs).
For branchiopods, it was previously assumed that lateral, saclike limb structures, the epipods
(or “gills”), were the main organs for respiration (e.g., Gicklhorn 1925), but later studies of the
epithelia (e.g., Kikuchi 1983) have shown that osmoregulation seems to be the main function of
the epipods (see Maas et al. 2009). It remains open to discussion whether branchiopod epipods
also have a respiratory function (see chapter 14 in this volume). Instead, the inner side of the
carapace is important for gas exchange. For Daphnia magna, recent studies show that the feed-
ing current is important for uptake of oxygen from the ambient medium and that gas exchange
occurs mainly within the filtering chamber (Pirow et al. 1999a) (Fig. 4.5A). A follow-up study by
the same authors showed that the inner wall of the carapace is the major site of respiratory gas
exchange (Pirow et al. 1999b). In contrast to earlier studies, where assumptions about respiratory
functions were mainly based on studies of tissue composition, Pirow et al. (1999b) developed an
elegant method to directly image hemoglobin oxygen saturation in transparent animals, which
allowed them to localize the specific areas on the body surface where oxygen uptake and release
take place. In Daphnia magna the highest values of hemoglobin oxygen saturation occurred near
the posterior margin of the carapace and in the rostral part of the head (which is outside the cara-
pace), suggesting that these areas are the most important for oxygen uptake (Pirow et al. 1999b).
In small animals living in the range of low Reynolds numbers, where viscous forces are domi-
nant (Koehl and Strickler 1981), the boundary layer is an obstacle for diffusive gas transport.
The thickness of the boundary layer depends on the velocity of the surrounding water relative
to the surface of the organism, and Pirow et al. (1999b) pointed out that reduced boundary layers
should occur inside the filtering chamber, where water is being pumped by the beating phyllopo-
dous limbs. They found that the enlarged carapace valves not only form the lateral boundaries of
the filtering chamber but are also employed for oxygen uptake due to the thin nature of the inner
wall of the carapace. In Daphnia magna, oxygen uptake does not only occur through the inner
wall of the carapace—the rostral part of the head had high oxygen values, which may provide
additional oxygen for sensory and central nervous system structures located in the head. This
additional respiratory surface may be of advantage during hypoxia if the carapace-based respira-
tory system fails to supply enough oxygen to the head regions (Pirow et al. 1999b).
In ostracods, as with many other smaller crustaceans, it is generally assumed that gas exchange
takes place over the general surface of the body. But notable exceptions are found in larger ostra-
cods, for example, in Vargula hilgendorfii, where oxygen uptake is assumed to occur preferen-
tially through the inner (posterior) surface of the carapace where the hemolymph sinuses are
best developed and are in direct contact with seawater (Abe and Vannier 1995). In Branchiura,
the so-called respiratory areas on the ventral sides of the carapace lobes have traditionally been
B Midgut
A Heart Pericarical sinus
gland
Carapace
Carapace
Gills
Gill
chamber
Artery to leg Ventral nerve cord
C D
–∼ 60˚
AIR
AIR
5 4 3
2
1
Fig. 4.5.
The carapace as a feeding and respiration chamber in various Crustacea. (A) Respiratory function of cara-
pace in Daphnia magna (Cladocera). Arrows left of specimen show feeding/respiratory current. Arrows
inside specimen show main routes of blood flow. Fluorescence microscopy has revealed that the main sites
of gas exchange are at the inner wall of the carapace near the posterior margin and at the rostrum (from
Pirow et al. 1999b, with permission from the Company of Biologists, Ltd.). (B) Cross section of general-
ized decapod showing position of gill chambers, which are formed by lateral flanges of the carapace (gill
covers). Drawing combined from various sources. (C) Procambarus clarkii (Astacidea) with the gill covers
removed showing outer layer of gills. 1–5 represent pereopods 1–5 (from Bauer 1998, with permission from
Wiley and Sons). (D) Branchial chambers modified for air breathing and water circulation in the sema-
phore crab Heloecius cordiformis (Ocypodidae). The chambers are divided in an upper part containing air
and a lower part containing water (where the gills are). Forward tilting allows water to be tipped forward
and pumped out of the branchial chambers anteriorly and air simultaneously to be sucked in posteriorly
(from Maitland 1990b, with permission from Springer).
assumed to be involved in gas exchange, but physiological/anatomical experiments by Haase

(1975) suggested that these areas have an osmoregulatory function.
Among malacostracans, there are multiple examples of the carapace forming a respiratory
chamber, often with water being actively pulled into it by beating limbs specialized for this
purpose. The respiratory system of decapod crustaceans is well known—the lateral lobes of
the carapace (branchiostegites) form a chamber on each side of the body, housing gills of vary-
ing morphology attached to the thoracopods basally or to the body laterally (see Hong 1988 for
details and overview) (Fig. 4.5B,C). A specialized part of maxilla 2, the scaphognathite or gill
bailer, beats and performs rapid movements independent from the movements of the remaining
part of the limb, thereby dragging a ventilatory water current through the carapace chamber.
The gills are normally irrigated with a posterior-anterior flow, and the water is expelled from
the gill chambers through openings near the mouth. The precise site where water enters the
chambers varies among taxa, but in brachyurans it is generally through discrete openings near
the bases of the pereopods, while in other taxa it may enter at varying positions along the ventral
carapace margin (e.g., Dyer and Uglow 1978, Batang and Suzuki 1999). Reversal of flow direc-
tion within the gill chambers has been recognized as a gill-cleaning strategy in certain decapods
(Bauer 1989, 1998) and may be particularly important for removing sediment from the gills in
burrowing species. In one example, Metapenaeus macleayi, the respiratory current enters a tube
in the sediment formed by the antennal scales and the antennules before it flows into the gill
chambers (Ruello 1973).
It is well known that many terrestrial or semiterrestrial brachyuran decapods retain water
in the branchial chambers of their carapace while active on land and, at the same time, have a
part of the chamber modified as a lung, relying on oxygen uptake directly from the air (Farrelly
and Greenaway 1994). Aspects of water retaining behavior are particularly well studied in the
semaphore crab, Heloecius cordiformis (Ocypodidae). A series of papers by Maitland (1990a,
1990b, 1992a, 1992b) showed that the water-retaining capacity of the carapace is intimately linked
to both respiration and feeding (Fig. 4.5D). One of the key findings is that H. cordiformis is an
obligate air breather while active on land. Air-based gas exchange takes place above the gills in
air-filled cavities lined with a vascular epithelium that function as lungs. While active on land,
the gill chambers are still partly filled with water thus irrigating the gills, but in experiments
where the branchial water has been removed, activity levels and oxygen percentages were unaf-
fected, suggesting that gill respiration is of less importance (for more details, see Maitland 1990a,
1990b, 1992a, 1992b). While on land, H. cordiformis sequentially depresses and elevates its cara-
pace in a pumplike manner (as in many other terrestrial brachyurans). The specific function of
this behavior is complicated, but Maitland (1992a) suggests that the carapace pump may enable
Heloecius to functionally partition lung ventilation from water circulation, thereby alleviating
the potential conflict between air breathing and water circulation. Another important func-
tion of the branchial water in H. cordiformis is for feeding. Water from the branchial chambers is
pumped out onto the mouthparts and is used in the separation of edible material from mud and
sand (Maitland 1990b).
The carapace also serves as a respiratory chamber in some peracarids. One example is the
Mysida, where no epipods acting as gills are present, but respiration takes place over the inner
wall of a relatively long carapace (e.g., Mayrat et al. 2006, Wirkner and Richter 2007). Cannon
and Manton (1927) studied the feeding and swimming of Hemimysis lamornae and found
that alongside with feeding and swimming currents, a special respiratory current is drawn in
under the posterior edge of the carapace and pushed out anteriorly at the sides of the maxillae
by the beating, lamellar epipods of the first thoracic limbs (see also Laverack et al. 1977) (Fig.
4.6A). Lophogastrids, which are sometimes grouped with Mysida in Mysidacea (e.g., Richter
and Scholtz 2001), are in many ways similar to mysids, but the carapace has been considered
nonrespiratory (e.g., by Dahl 1991). This notion has recently been challenged by Wirkner and
Richter (2007). As in mysids, a respiration current inside the carapace is generated by a beat-
ing epipodite of the first pair of thoracopods and apparently also by the exopods of the second
maxillae (Childress 1971), but in contrast to mysids, gills (epipods) are present on thoracopods
2–7 (see Boxshall and Jaume 2009), which probably takes care of most of the gas exchange
(Fig. 4.6B).
In the Thermosbaenacea, Tanaidacea, Cumacea, and Speleogriphacea, a short carapace
forms a small respiratory chamber (Grindley and Hessler 1971), inside of which a branchial/
ventilatory first thoracopod (maxilliped) epipod generates a water current. The thermosbaen-
acean Thermosbaena mirabilis was studied in detail by Barker (1962), and notes were also made
on the respiratory system based on the study of living specimens. As in mysids, a respiratory
current is drawn through the posterior opening of the short carapace (Fig. 4.6C) by the beat-
ing of the maxilliped epipod. Barker (1962) suggested that the epipod functions as a gill since it
Inhalant
respiratory MYSIDA LOPHOGASTRIDA
Carapace Carapace
current B SCAPHOGNATHITE # 2
A
LATERAL
GILL
LEG
BASE SCAPHOGNATHITE # 1
VENTRAL GILL
Carapace
THERMOSBAENACEA
Inhalant D Carapace CUMACEA Carapace
respiratory E
C current
Exhalant th 2 th 3 th 4 th 5
respiratory mxp
ep
current Exhalant
II III IV current
Antennule endopod
Mandible Inhalant current

F epipod
Maxilliped
Inhalant
G TANAIDACEA respiratory
Respiratory H
current
pores
Fig. 4.6.
Respiratory carapaces and ventilation currents in peracarid malacostracans. (A) Lateral view of thorax
of Hemimysis lamornae (Mysida) showing the course of the respiratory currents (arrows). The current
is drawn in under the hind edge of the carapace, the inner wall of which is respiratory (no gills) (from
Cannon and Manton 1927, with permission from the Royal Society of Edinburgh). (B) Schematic lateral
view of Gnathophausia ingens (Lophogastrida) showing the course of the respiratory current under the
carapace, where gills take care of gas exchange. The respiratory current is generated by two different
“scaphognathites”: one is the exopod of the second maxilla; the other is the epipod of the first trunk limb
(from Childress 1971, with permission from the Biological Bulletin/Marine Biological Laboratory, Woods
Hole, MA). (C) Respiratory carapace in Thermosbaena mirabilis (Thermosbaenacea), carapace partly
removed (outline indicated by dashed line). Arrows show direction of respiration current (from Barker
1962, with permission from the Company of Biologists, Ltd.). (D) Diastylis species (Cumacea) buried in
sand, showing the inhalant and exhalant feeding and respiratory/feeding currents (arrows) in buried ani-
mals (from Dennell 1937, based on Zimmer, with permission from the Royal Society of Edinburgh). (E)
Anterior part of body of Diastylis from lateral showing carapace with large right respiratory maxillipedal
epipods inside. Water current enters ventrally (from Oelze 1931). (F) Maxilliped of Diastylis with respira-
tory epipod (from Calman 1909). (G and H) Tanais cavolinii (Tanaidacea) (from Johnson and Attramadal
1982, with permission from Taylor and Francis, Ltd.). (G) Schematic drawing showing water flow around
the body (arrows). Respiratory water enters through dorsal respiratory pores into respiratory carapace.
(H) Dorsal view of carapace showing position of respiratory pores (arrows).
contains vascular lacunae and offers a relatively large surface. However, the main site of respira-
tory exchange is the inner side of the carapace wall, where the cuticle covers a system of vascular
lacunae in the carapace epithelium (Siewing 1958, Barker 1962).
In the Cumacea, the epipods of the first maxilliped generate a respiratory current as in the
other mentioned taxa, but by contrast, this current also serves as a feeding/filtration current.
Zimmer (1932) found, in nonburied specimens of Diastylis rathkei , that the inhalant current
enters the respiratory chambers between the bases of the third maxillipeds, which seem in
accordance with Oelze (1931) (Fig. 4.6E). In buried specimens, which had been undisturbed
for a period of time, Zimmer (1932) found that the inhalant current forms a small funnel in
the sediment between the bases of the third maxillipeds and the body. The exhalant current
leaves anterior to the site of intake, guided by the pseudorostrum (Zimmer 1932). Dennell
(1937), based on Zimmer (1932), provided an illustration of a buried specimen of Diastylis spe-
cies with arrows close to the anterior margin of the carapace indicating the respiratory cur-
rents (Fig. 4.6D). This illustration has since been reproduced in many text books. However,
the anterior position of the inhalant current indicated by Dennell is rather different from
that shown in a figure by Oelze (1931), where the current was found to enter more ventrally
through small slits (compare Fig. 4.6D,E). Possibly the two different representations can
be reconciled. The ventral current entrance shown by Oelze (1931) (Fig. 4.6E) may be the
anatomically true one, while the entrance shown in the overview figure by Dennell (1937)
shows where the inhalant current approximately enters when the animal is buried and the
ventral side is covered by sediment. The ventilatory epipod of the first maxilliped in Diastylis
is rather large and has a region that is folded into branchial lamellae (Calman 1909, Oelze 1931)
(Fig. 4.6E,F), which must function in gas exchange. The inner side of the carapace must be
involved in gas exchange, as in a number of other peracarids, since both valves are filled with
hemolymph channels (Oelze 1931, Siewing 1952).
In Tanaidacea the carapace forms a respiratory chamber on each side of the body as well.
Calman (1909) reported that the respiratory system of Apseudidae resembled that of cumaceans,
for example, with respect to the presence of a ventilatory maxillipedal epipod. Calman (1909)
also mentioned that the lateral folds of the carapace in tanaidaceans are traversed by a net-
work of blood channels and suggested that these form the chief organs of respiration, possibly
assisted by the epipodites of the maxillipeds, all of which was later confirmed by Lauterbach
(1970) for Tanais cavolinii. Johnson and Attramadal (1982) made detailed observations on the
mechanics of the carapace-based respiratory system in T. cavolinii. The tube-building lifestyle
of T. cavolinii prevents simple observation of its behavior, so to overcome this problem, the
animals were offered capillary glass tubes of varying diameters, which were readily accepted
(Fig. 4.6G). Observations showed that the basics of the respiratory system of T. cavolinii is
comparable to that of thermosbaenaceans and cumaceans (see above) but that certain char-
acteristics can be explained as adaptations to tube-dwelling behavior. According to Johnson
and Attramadal (1982), the ventilatory epipods of the maxillipeds, under normal conditions,
generate a respiratory current in each branchial chamber, which enters the chamber through
two respiratory pores at the posterior edge of the carapace valves (see Fig. 4.6H) and leaves
through ventral pores close to the base of the maxillipeds. Occasionally, the respiration current
is reversed (linked with reversal of pleopod pumping) so that the water enters the branchial
chamber ventrally and is expelled through the dorsal pores. Johnson and Attramadal (1982)
assume that this is to protect the dorsal respiratory pores and the branchial chamber from being
clogged by foreign particles in the suspension.
Spelaeogriphus lepidops, the first discovered species of the Spelaeogriphacea (Gordon 1957)
(Fig. 4.2C), has a respiratory carapace, but the respiratory chamber is less closed than that of
tanaidaceans and cumaceans and consists basically of lateral carapace lobes overhanging the
anterior somites. Based on Gordon (1957, 1960) and Grindley and Hessler (1971), who contrary
to Gordon had the opportunity to study live material, it can be concluded that S. lepidops appar-
ently has two different respiratory systems, which is unusual for Crustacea: one based on the
thoracopodal exopods (which will not be treated here) and one involving the carapace. Both
Gordon (1957) and Grindley and Hessler (1971) assumed that the cup-shaped maxillipedal epi-
pod probably is respiratory and that the “oval patch” (Gordon 1957) on the inside of the carapace
might well be a respiratory surface, but unfortunately it was not possible for Grindley and
Hessler (1971) to observe the specific functioning of the epipodal gill of the maxilliped in the
living specimens studied by them.
Within Mictacea, which is another small peracarid order with only few species and which
show much resemblance to thermosbaenaceans and spelaeogriphaceans, it has been reported
that Mictocaris halope has an inflated, thin-walled elliptical area dorsal to the carapace fold
apparently functioning in respiratory exchange, but no respiratory maxillipedal epipod is
present (Bowman et al. 1985).
Brooding Chamber
A variety of crustaceans have brood care, and in some taxa the offspring are protected by the
carapace during part of their development. Branchiopod crustaceans (clam shrimps and water
fleas) are probably best known for this habit, but also in certain ostracods, ascothoracidan
thecostracans, and thermosbaenacean malacostracans, the carapace offers protection during
development.
In spinicaudatan and laevicaudatan (Fig. 4.7A) branchiopods (clam shrimps), the eggs
(embryos) are retained in a pair of clusters under the carapace valves, kept in position by vari-
ous supporting structures of the female’s appendages. In both these taxa the eggs are kept
under the carapace but only during a short part of their development, and they are released as
free-swimming nauplii or nauplia-like larvae (Olesen and Grygier 2003, 2004, Olesen 2005).
Cyclestheria hislopi, a clam shrimp with many similarities to Spinicaudata but now recog-
nized as a sister group to the Cladocera (water f leas) (e.g., Martin and Davis 2001, Richter
et al. 2007), has taken it a step further and retains the offspring under the carapace attached to
dorsal filaments of the trunk limb exopods until they are released as small adultlike juveniles
(“direct development”; Olesen 1999) (Fig. 4.7B; see also Fig. 4.11C, below). In the taxonomi-
cally diverse Cladocera, development is also direct and takes place dorsally under the cara-
pace (a single exception are the winter eggs of Leptodora kindtii, from which free-swimming
metanauplii hatch), but different from C. hislopi, the embryos are not attached to the female
via filaments. In most cladocerans, the inside of the brood chamber is directly connected
with the surrounding media, but in a few taxa (Moinidae, Onychopoda, Penilia), the develop-
ing embryos are nourished by a placenta-like organ, a so-called nä hrboden, inside the brood
chamber (e.g., Claus 1877, Potts and Durning 1980, Egloff et al. 1997, Dumont and Negrea
2002). Branchiopods are well known for producing diapause eggs, or resting eggs, as a part of
their life cycle, which appear when conditions are unfavorable (winter or drought), and in the
diverse Anomopoda the carapace is used in various ways as a container for the shed resting
eggs (ephippia), a habit that is unique among branchiopods (Fryer 1996). Probably familiar
to most students of zoology is the characteristic ephippium of Daphnia (Fig. 4.7C), which is
a modified part of the carapace housing two resting eggs and is the most specialized of such
structures among anomopods. In many anomopods, such as macrothricids and chydorids, the
ephippium is less elaborate than that of Daphnia and basically consists of the entire, unmodi-
fied carapace that after molting separates from the individual and comes to persist as an inde-
pendent envelope for a number of eggs. Even the simplest ephippia can withstand drought
(Fryer 1996). The ephippia of Daphnia with its resting eggs inside probably ensures that the
population can be continued after the winter or after drought but probably also plays a role
in dispersal. In some taxa, such as Streblocerus serricaudatus (Fig. 4.7D,E), the ephippium is
attached to vegetation and so reduces the chance of dispersal, which suggests that it is often
advantageous to ensure persistence of a population instead of undertaking the risks involved
in dispersing (Fryer 1996).
A C D
Eggs
sexual cycle mating
Ephippium
sexual egg
Ephippium (carapace)
hatching
Carapace after parthenogenetic
diapause cycle
Embryonised
B parthenogenetic
larvae haploid E
daughter
egg
formation
parthenogenetic
son
Carapace
Carapace Embryo
Carapace
F Carapace G H
Eye
egg
Antennule
Pleopod 1
Fig. 4.7.
Carapace as brood chamber in various crustaceans. (A) Lynceus brachyurus (Branchiopoda,
Laevicaudata) with a cluster of eggs in a dorsal brood chamber between body and carapace valves (from
Sars 1896). (B) Cyclestheria hislopi (Branchiopoda, Cyclestherida) with well-developed embryos in dor-
sal brood chamber attached to limb filaments (from Sars 1887). (C) Life cycle of Daphnia (Branchiopoda,
Cladocera), where a part of the carapace is modified to a characteristic ephippium housing the rest-
ing eggs (from Ebert 2005, used with permission from the author). (D) Ephippium of Streblocerus ser-
ricaudatus (Branchiopoda, Cladocera) consisting of carapace attached to leaf (from Fryer 1972, with
permission from Wiley and Sons). (E) Embryos of S. serricaudatus near the point of hatching from a rest-
ing egg (from Fryer 1972, with permission from Wiley and Sons). (F) Vestalenula cornelia (Ostracoda)
with right valve removed (from Smith et al. 2006, with permission from the Royal Society of London).
(G) Thermosbaena mirabilis (Thermosbaenacea) with dorsal brood chamber containing embryos
(from Barker 1962, with permission from the Company of Biologists, Ltd.). (H) Amphionides reynaudii
(Amphionidacea), which has been proposed to have a ventral brood chamber between carapace valves
with elongate first pleopods forming the roof of the chamber (but brooding never directly observed)
(from Williamson 1973, with permission from Brill).
For Ostracoda, Maddocks (1992) reports that many burrowing and swimming forms brood
their eggs and young instars within the posterior part of the carapace (Fig. 4.7F). In many taxa,
however, eggs are laid individually or in clutches on plants or other substrata before develop-
ment (Maddocks 1992). Brooding was recently also reported for a Silurian ostracod where a
specimen with eggs, perhaps even juveniles, has been described, demonstrating that brooding is
a very conserved strategy within ostracods (Siveter et al. 2007).
Within Thecostraca, many species of Ascothoracida brood their offspring inside the cara-
pace that is sometimes much enlarged (Kolbasov et al. 2008). Grygier and Fratt (1984) reported
that, for Ascothorax gigas, a parasite in the bursae of the brittlestar Ophionotus victoriae, the
number of offspring varies between a few hundred and well more than a thousand per female.
They identified five distinct larval stages, which, according to the authors, may not represent all
the instars that A. gigas passes through before release.
Within the Malacostraca, only the Thermosbaenacea brood the embryos dorsally under
a swollen carapace. Barker (1962) examined Thermosbaena mirabilis and found that the cara-
pace in breeding females is greatly enlarged by successive molts to form a brood pouch, which
carries an average of 10 embryos constantly agitated by the inhalant respiratory current (Fig.
4.7G). Barker (1962) suggested that this current may also play a role in sucking the embryos into
the brood pouch after they have appeared from the posteriorly directed vaginae. The embryos
emerge from the brood pouch as miniature adults.
For the aberrant Amphionides reynaudii (Malacostraca, Amphionidacea), Williamson (1973)
suggested that the enlarged female carapace forms a brood chamber where the long, anteriorly
directed first pleopods form the roof of the chamber (Fig. 4.7H). However, specimens with eggs
or embryos within this putative brood pouch are yet to be discovered.
ONTOGENY, EVOLUTION, AND MORPHOLOGICAL DIVERSIT Y OF THE CARAPACE

IN SELECTED CRUSTACEA
The Branchiopod Carapace
The Branchiopoda is an ideal case study on carapace evolution since this taxon is fairly well
defined but still offers some variation in the morphology and function of the carapace.
Branchiopod carapaces include a broad range of types: a more or less flattened dorsal shield
(Notostraca, Fig. 4.1A; see also Fig. 4.10C, below), bivalved carapaces sometimes capable of
enclosing the whole body (clam shrimps and cladocerans, Figs. 4.1B, 4.4, 4.5A, 4.7A–E; see also
Figs. 4.9, 4.11C, 4.12C, below), and dorsally attached brood pouches showing only little resem-
blance to the carapace in other branchiopods (raptorial cladocerans, Fig. 4.1C; see also Figs.
4.13C, 4.14C, below).
As suggested by Walossek (1993) and appreciated by Fryer (1996) in his review of the
branchiopod carapace, the well-preserved Cambrian microfossil Rehbachiella kinnekullensis
Mü ller, 1983 provides important information on early carapace development in Branchiopoda.
Rehbachiella has been suggested by Walossek (1993) to be an early branchiopod, and while there
is room for discussion of its precise phylogenetic position, a branchiopod affinity seems most
convincing. The carapace of Rehbachiella and its growth mode are taken here as an indication
of how the ancestral branchiopod carapace looked and are therefore summarized in the follow-
ing. Walossek (1993) showed very clearly that the carapace of Rehbachiella originates as a simple
extension of the original naupliar shield. In the earliest stage, the naupliar shield covers an area
dorsally that corresponds to the naupliar appendages: the first and second antennae and the
mandibles (Fig. 4.8A). A few stages later, the naupliar shield includes also the first maxilla seg-
ment (Fig. 4.8B) but not the second maxilla segment. Later the shield starts to grow into what
can now be termed a carapace since it has a free posterior fold starting to overgrow the second
maxilla segment and more segments posteriorly (Fig. 4.8C). Free folds also develop laterally
and start overgrowing the limbs. At a later stage, when the posterior margin of the carapace has
become freed, the dorsum of the second maxilla has become fused with the carapace (Fig. 4.8D),
so that the carapace fold at this and later stages appears topographically to be an extension of the
posterior margin of the second maxilla segment, while it can be argued that it is more correct to
consider it as developing from the first maxilla segment. At the latest known stage, the carapace
of Rehbachiella is attached in the “cephalic” region (which includes the maxilla 2 segment) and
has developed free folds posteriorly and laterally overhanging about seven somites posteriorly
and the proximal parts of the limbs (including cephalic appendages).
Maxilla 2
Antennule Maxilla 1
Mandible Carapace
A
C
Antenna 2
Antennule
Antenna 2 Mandible Antennule

Maxilla 2
D Maxilla 1
Mandible
Antenna 2
Carapace
Mandible
Antennule
Antenna 2
Maxilla 1
Maxilla 2
Fig. 4.8.
Carapace development in Rehbachiella kinnekullensis, a Cambrian crustacean that most likely is a close
relative to the Branchiopoda, from Walossek’s (1993) series A (A–C) and series B (D), not to same scale.
Figures used with permission from Blackwell Publishing.
Given the presumed close relationship between Rehbachiella and other branchiopods,
it seems safe to assume that the carapace types in other branchiopods have evolved from a
Rehbachiella type of carapace. The phylogeny of Branchiopoda is relatively well understood
(Richter et al. 2007, Olesen 2009) (Fig. 4.9), from which a number of conclusions can be drawn.
The first off-split within Branchiopoda is the anostracan lineage (Sarsostraca), which consists
of the recent Anostraca and the Devonian fossil Lepidocaris rhyniensis, both of which lack a
carapace. Based on parsimony, a carapace may have been lost in this lineage. It is not yet cer-
tain which taxon constitutes the next branch within Branchiopoda. Traditionally (based on
morphology), Notostraca has been considered the sister group to a monophyletic Diplostraca
(= clam shrimps and water fleas), but most molecular work has suggested the Notostraca as an
ingroup of Diplostraca (Stenderup et al. 2006, Richter et al. 2007) (Fig. 4.9, dashed line with
question mark). This uncertainty holds importance for the idea of carapace evolution in the
Notostraca. If Notostraca really is a diplostracan ingroup, then it may be assumed that the noto-
stracan ancestor had some kind of bivalved carapace as seen in Spinicaudata, Cyclestherida,
and Laevicaudata. In this context, it is interesting that the carapace of Triops cancriformis has a
clear paired anlage in early larvae (Møller et al. 2003) (Fig. 4.10A), very similar to that seen in
the larvae or embryos of Spinicaudata, Cyclestherida, and Haplopoda (Olesen 1999, Olesen and
(6)
(4) (10)
(12)
(5) (8)
(3)
(7) (13)
(9)
(11)
(1) (2)
)
1)
a 6
3)
)
)
4)
7)
8)
a 9)
a 11
s 3
da 1
)
a 10
2)
is
ata
)
ata
lla
hr
ca 5
eri
ra 1
od
)
ca 2
ari
po
hie
ud
art
ud
oll
od
sth
op
tra
do
oc
ho
ica
ca
ac
ac
kh
op
tra
om
cle
tos
pid
pto
ini
hb
str
yc
za
ev
en
os
Cy
On
No
An
Ka
Sp
Ca
Re
La
Le
Ct
Le
An
Gymnomera
? Cladocera
Cladoceromorpha
Sarsostraca Calmanostraca
Diplostraca
Phyllopoda
Branchiopoda (s. str.)

Branchiopoda (s. lat.)
Fig. 4.9.
Phylogeny of the Branchiopoda showing variation in the morphology of the branchiopod carapace
(in gray). Dashed line with question mark indicates alternative position of the notostracan clade
(Calmanostraca). From Olesen (2007), with permission from the Crustacean Society.
Grygier 2003, 2004, Olesen et al. 2003). Despite the similar developmental origin in the men-
tioned taxa, the subsequent development leads to adult carapace types that are quite different:
in Notostraca, the paired larval anlagen are precursors of a large univalved dorsal plate continu-
ous with the head in the adults (Fig. 4.1A, 4.10C), whereas in the Spinicaudata and Cyclestherida
the paired anlagen develop into the bivalved carapace, where each anlage corresponds to the
left or right valve (Fig. 4.11). The paired anlagen of the univalved carapace in Notostraca may
be an indication of a bivalved origin independently of whether or not Notostraca is a diplost-
racan ingroup. The longitudinal dorsal keel seen on the carapace of Triops, for example (e.g.,
Fig. 4.1A), may be a reminiscence of an earlier simple articulation like the ones seen in recent
Spinicaudata. The appearance of a univalved carapace in Notostraca from a bivalved carapace
of some type may have evolved alongside a shift in feeding strategy from filtration, as seen in
Anostraca and Spinicaudata, to a benthic lifestyle as omnivorous scavengers and opportunistic
predators. The Kazacharthra, a Jurassic extinct sister taxon to Notostraca (McKenzie and Chen
1999, Olesen 2009), also has a carapace that apparently is a dorsal plate, but not enough details
are known to be considered in this context.
Walossek (1993) noted that the carapace in diplostracan branchiopods (clam shrimps and
cladocerans) is “disconnected” from the head in the sense that the carapace in these taxa
does not appear as a simple posterior and lateral growth of the margins of a head shield as it
does in Rehbachiella. Consequently, he termed the diplostracan carapace a secondary shield
Carapace anlagen Carapace
Mandible
Antenna 1
Antenna 1 Antenna 2
A 100 μm B 100 μm
Antenna 2
Carapace
1 mm
C
Fig. 4.10.
Carapace development in Triops (Notostraca): (A and B) stages I and II (from Møller et al. 2003, with per-
mission from Wiley and Sons, Ltd.) and (C) adult (from Olesen 2009, with permission from Senckenberg
Gesellschaft f ü r Naturforschung).
Carapace
Carapace
A 50 μm
Carapace
Embryonised larva
B 50 μm C 500 μm
Fig. 4.11.
Carapace development in Cyclestheria hislopi (Cyclestherida): lateral (A) and dorsal (B) view of embry-
onized larva and (C) adult female with left carapace valve removed. From Olesen (1999), with permission
from Wiley and Sons, Ltd.
(e.g., Cyclestheria embryos in Fig. 4.11A,B). I agree with Walossek (1993) that this is a signifi-
cant evolutionary novelty in branchiopod carapace formation and therefore a synapomorphy at
some level. As explored elsewhere (Richter et al. 2007, Olesen 2009), there is some evidence that
Notostraca qualifies to be included in this group, since the carapace anlage in early larvae of
Triops (Fig. 4.10A) is disconnected from the head region in a way similar to that of Cyclestheria
hislopi, for example (Fig. 4.11A). But setting this aside, the lack of a (probably lost) carapace in
the anostracan lineage leaves uncertainty as to how early in branchiopod evolution this discon-
nection evolved between an anterior head shield and a posterior free carapace fold. It could
have been as early as in the branchiopod ancestor. In any case, the disconnection has taken
place, and it is therefore relevant to consider how. The ontogeny of Lynceus may provide a clue
since it exhibits both types of carapaces but in two different parts of its life cycle. In the larvae,
the carapace is an extension of the head shield as in Rehbachiella but with a unique morphology
(Olesen 2005) (Fig. 4.12A,B). In juveniles and adults, the carapace is large, bivalved, noncon-
tinuous with the “head,” and clearly of the “secondary shield” type as outlined by Walossek
(1993) (Figs. 4.7A, 4.12C). The shift in carapace morphology takes place from one instar to the
next. This abrupt change in morphology between two stages may in some way reflect what took
place in evolution. Hence, Lynceus exhibits at the same time, but in different stages, a plesio-
morphic head shield type of carapace (in larvae) and an apomorphic “disconnected” secondary
shield type of carapace (juveniles and adults).
Carapace Carapace
A 50 μm
Carapace
Antenna 1
B 50 μm C 500 μm
Labrum
Fig. 4.12.
Carapace development in Lynceus (Laevicaudata): (A and B) dorsal (A) and lateral (B) view of larva of L.
brachyurus (from Olesen 2005, with permission from Wiley and Sons, Ltd.) and (C) frontal view of adult of
L. tatei (from Olesen 2009, with permission from Senckenberg Gesellschaft f ü r Naturforschung).
Cladoceran carapace origin and evolution pose other interesting questions concerning
carapace evolution. Cladocerans are often thought to have evolved neotenically from clam
shrimp ancestors, with free-living clam shrimp larvae as the starting point (e.g., Schminke
1981). However, since it is now known that Cyclestheria hislopi (Cyclestherida), which has
embryonized larvae (see Olesen 1999), is the sister taxon to Cladocera, free-living clam shrimp
larvae cannot have been the starting point for an eventual neotenic origin of cladocerans. If
neoteny (more generally, heterochrony) has been involved, then the embryos of Cyclestheria
hislopi would have instead been the starting point. It is striking to note that all it takes to
“make” a cladoceran carapace from an Cyclestheria-like ancestor is to stop the carapace devel-
opment of Cyclestheria before it starts overgrowing the head region (e.g., at stage VII; see
Olesen 1999).
Most cladocerans have a bivalved carapace where left and right side valves cover the body
and the trunk limbs (the head is free) (e.g., Figs. 4.4, 4.5A, 4.7C). But in the raptorial/preda-
tory cladocerans, Onychopoda and Haplopoda, the carapace has been modified further and
constitutes only a dorsal brood pouch, with no free valves covering the body and trunk limbs.
This has been taken to an extreme in the large, predatory Leptodora kindtii (Haplopoda), where
the carapace in adults is a saclike structure placed very far behind on the body (Fig. 4.13C). In
this respect, L. kindtii is different from other Crustacea, where the carapace in adults often is a
posterior extension of the cephalic region or at least is placed very close to this. Interestingly,
in the early ontogeny of Leptodora, the carapace appears as a narrow dorsal swelling behind the
mandibular region (Fig. 4.14A), which is far more anterior than the position of the carapace/
brood pouch in the adult female would indicate. During development, a posterior displacement
of the carapace takes place that can be followed step by step by studying the embryonized lar-
vae in the female’s brood pouch. After having appeared as a narrow, dorsal anterior fold, the
carapace becomes a dorsal flap (Fig. 4.14B,C) that gradually grows in size while it apparently
moves posteriorly until it constitutes a large, dorsal brood pouch as found in adults (Samter 1895,
Olesen et al. 2003) (Fig. 4.13). Olesen et al. (2003) suggested the anterior part of the carapace has
gradually fused to the dorsal part of the thorax during ontogeny, leaving only the posterior parts
of the valves free. The posterior displacement of the carapace in the ontogeny probably reflects
what took place during evolution of the characteristic brood pouch in Leptodora. A comparable
ontogeny has been described for certain malacostracans where the carapace also “fuses” with
the thoracomeres (see “Ontogeny of the Carapace in Some Malacostracans with Free Larvae,”
below).
The Malacostracan Carapace
Morphological Diversity of the Malacostracan Carapace
A carapace is present in many malacostracans and may have played a major role in the success
of this highly diverse taxon in combination with other features of the caridoid facies, such as
the muscular pleon (Hessler 1983, Hessler and Watling 1999). Not all taxa have a carapace, but
those that do exhibit a variation (Fig. 4.2) that is fascinating not only from a functional perspec-
tive (see summary of carapace functions above) but also from an evolutionary-morphological
perspective. The diverse Malacostraca with their variation in carapace sizes, cephalothorax
sizes, and development modes have provided much room for discussing carapace homolo-
gies, challenged in complexity perhaps only by an even more convoluted discussion on
limb homologies. However, the carapace/cephalothorax structures exhibited by malacost-
racans indeed provide a toolbox for considering very important aspects of malacostracan
evolution.
A
B
Fig. 4.13.
Carapace development in Leptodora kindtii (Cladocera): three different developmental stages (A–C)
showing that the free part of the carapace (brood pouch, arrows) are migrating in posterior direction dur-
ing development. From Samter (1895), with permission from Elsevier.
Carapace anlage Carapace
Antenna 1
Antenna 2
Mandible
Trunk limb 1
A 50 μm B 100 μm
Carapace
Antenna 2
Antenna 1
Labrum
Trunk limb 1
C 100 μm
Fig. 4.14.
Carapace development in Leptodora kindtii (Cladocera). (A) Lateral view of head with early carapace lobe
behind the head. (B) Lateral view of head and thorax showing the early carapace as a small lobe having
migrated slightly more posterior than in A. (C) Juvenile with a small carapace lobe. From Olesen et al.
(2003), with permission from Wiley and Sons, Ltd.
Taxa such as amphipods and isopods lack a carapace entirely. Only a few taxa, Leptostraca
and Mysidacea, have as adults what could be characterized a classical Calman type of carapace
enveloping a larger part of the thoracic region (Figs. 4.2A,E, 4.6A,B; see also Fig. 4.16A,B, below).
In both decapods and euphausiids, the head and thorax regions are combined into an unseg-
mented cephalothorax (Fig. 4.2D,F,H), which is also the case for stomatopods (Fig. 4.2B) but
involving a smaller part of the thorax. Other malacostracans, such as cumaceans, have a shorter
carapace fused with the first three thoracic segments but with free lateral lobes enclosing the
appendages that serve for respiration and feeding (Figs. 4.2G, 4.6D–F). Thermosbaenaceans (at
least Thermosbaena mirabilis) are unique among malacostracans since females carry the devel-
oping embryos dorsally beneath the carapace (Fig. 4.7G).
Evolution of the Malacostracan Carapace
One of the key questions concerning carapace evolution in the Malacostraca is whether a
Calman type of carapace was present in the common malacostracan ancestor, and the lack of it,
or various modifications, is therefore secondary. Calman suggested that a free carapace envel-
oping the thoracic region was a primitive attribute of the Malacostraca along with a number of
other shrimplike characteristics (his “caridoid facies”) (Fig. 4.15A). This suggestion was based
on the straightforward observation that a carapace of that type occurs in what he called the more
“primitive members” of the main taxa into which he divided the Malacostraca (e.g., Mysidacea
within Peracarida). This view has been adopted by later authors such as Hessler (1983) and
Newman and Knight (1984). Richter and Scholtz (2001) also interpreted the lack of a carapace as
a derived character within the Malacostraca. On the contrary, Dahl (1983, 1991) preferred a cara-
paceless Anaspides-like type of “caridoid facies” (= morphology of common ancestor) for the
Malacostraca. Also, Watling (1999), based on an alternative phylogenetic hypothesis, suggested
that the “caridoid facies” with its Calman-type carapace was not a part of the ground pattern
for the Malacostraca but rather a specialization in a caridoid clade consisting of Lophogastrida,
Mysida, Euphausiacea, and Decapoda.
Any considerations of character evolution, such as carapace evolution, should preferably
be done on the background of a well-supported phylogeny. For the Malacostraca, despite the
attempts mentioned above, it has been surprisingly difficult to obtain a robust result, and the
existing molecular and morphological evidence seems insufficient (Jenner et al. 2009, Richter
et al. 2009). However, if Leptostraca, which also have a large carapace enveloping the thoracic
region (Figs. 4.2A, 4.16A,B) is indeed the sister group to the remaining malacostracans, as per-
ceived by many authors (e.g., Siewing 1963, Richter and Scholtz 2001, Meland and Willassen
2007, Wirkner and Richter 2009, Regier et al. 2010), then it seems simplest to assume its pres-
ence in the malacostracan ancestor, retained largely unchanged in the Mysidacea, modified or
even lost in other taxa, exactly as was implied by Calman (1909).
Ontogeny of the Carapace in Some Malacostracans with Free Larvae
Within the Malacostraca, it seems that dendrobranchiate decapods, euphausiids, and stomato-
pods are particularly useful for considering early carapace evolution since, in these taxa, the
carapace during early larval development is a free fold attached to the posterior margin of the
head region (e.g., Figs. 4.15B,C, 4.16C–F). In adults of these taxa, the free carapace has been
transformed into a cephalothorax involving a varying number of thoracic somites (e.g., Fig.
4.2B,D,F,H). The presence of a naupliar sequence in the development of euphausiids and den-
drobranchiate decapods is most often considered primitive for Malacostraca. Scholtz (2002),
Carapace
A
Carapace
B
Carapace
Fig. 4.15.
Calman’s (1909) hypothetical malacostracan ancestor and two malacostracan free-living larvae with the
carapace as posterior extension of the head shield not involving thorax segments. (A) Calman’s (1909)
illustration of a generalized type of Malacostraca showing a morphology that he called “caridoid fascies”
(shrimplike). He suggested that a large carapace overhanging the thorax was ancestral to Malacostraca.
(B) Antizoea of Lysiosquilla eusebia (Stomatopoda) (from Gurney 1942, with permission from the Ray
Society/Natural History Museum, London). (C) Protozoea of Penaeopsis species (from Gurney 1942, with
permission from the Ray Society/Natural History Museum, London).
on the contrary, suggested secondary reappearance of free-living nauplii within Malacostraca,

based partly on parsimony using the phylogeny of Richter and Scholtz (2001). However, since
the phylogeny of Malacostraca is still highly uncertain ( Jenner et al. 2009, Richter et al. 2009),
which weakens parsimony arguments, and since the early larvae (naupliar sequences) of for
example, both euphausiids and dendrobranchiates in many respects are indeed very similar to
larvae of nonmalacostracans, it is here assumed that an anamorphic development, probably
in many respects similar to that of dendrobranchiate decapods, is ancestral for Malacostraca.
Considering dendrobranchiate development, it is really striking that the early carapace of pro-
tozoea larvae of Penaeopsis (Gurney 1942, Fig. 4.15C) or Penaeus monodon (Fig. 4.16E,F), for
example, is very similar to that of the “Orsten” crustaceans Rehbachiella (Fig. 4.8) or Bredocaris.
The carapace in all of these taxa is an extension of the posterior margin of the naupliar shield.
And, as in Rehbachiella, it seems in Penaeopsis as though the segment of the second maxilla is not
Carapace
A 100 μm B 100 μm
Carapace
Carapace
C 200 μm D 200 μm
Carapace Carapace
E F 50 μm
50 μm
Fig. 4.16.
Carapace development in various malacostracans. (A and B) Nebalia longicornis (Leptostraca) (from
Olesen and Walossek 2000, with permission from Springer): lateral view of late juvenile (A) and posterior
view showing dorsal attachment of carapace (B). (C and D) Lateral (C) and posterior (D) view of antizoea
of Squilla species (Stomatopoda). (E and F) Protozoea of Penaeus monodon (Penaeidae) (material provided
by G. Scholtz; data in Biffis et al. 2009): early protozoea with free posterior carapace fold (E) and later
protozoea where carapace has started to fuse to thorax (F). The arrow points at the cuticle between the
carapace and the thorax, in the process of shifting backward.
incorporated into the carapace in early stages (Fig. 4.15C), highlighting that a carapace “origi-
nating” from a second maxilla segment is not crucial when considering carapace homologies
among different taxa (see discussion below).
It has long been known that the free carapace in larvae of dendrobranchiate decapods devel-
ops into the well-known decapod type of cephalothorax, but the exact way this happens ontoge-
netically has been difficult to elucidate. According to Newman and Knight (1984), who looked
at the development of several dendrobranchiates and one euphausiid, it takes place as follows.
In the first protozoea, the carapace is represented by a backward and somewhat lateral extension
of the shield, which covers a portion of the thorax. Then, during ontogeny, which is achieved by
successive ecdyses, the thoracic and carapace cuticles are shed, and the underlying new carapace
cuticle shifts farther back on the thorax as molting progresses, until the posterior margin of the
last thoracic segment is reached. Also, as stated by Newman and Knight (1984), in effect the cuti-
cle underlying the carapace and overlying the thorax is withdrawn, and in the process, the tissue
of the two structures melds or fuses together. Thus, the dorsal surface of the cephalothorax in the
adult is formed by the previous surface of the carapace in the larva. Figure 4.16F shows a proto-
zoea stage of Penaeus monodon caught in the middle of transformation of the carapace from a free
shield to a cephalothorax (the arrow points at the cuticle between the carapace and the thorax, in
the process of shifting backward). Casanova (1991, 1993) and Casanova et al. (2002) use another
terminology for describing carapace formation in a number of malacostracans, but there seems to
be a basic congruence with the description of Newman and Knight (1984). Casanova et al. (2002)
described the fusion between the carapace and the thorax in Penaeus indicus as involving a “split-
ting” of the thorax tergites.
It is well known that there is a fundamental connection between development and evo-
lution of living organisms. Any change in morphology must necessarily involve a change
of something in development, for example, a change in the rate or timing of the ontogeny of
certain structures (= heterochrony). With respect to the decapod carapace, it is tempting to
suggest that the way in which the cephalothorax is formed ontogenetically in, for example,
dendrobranchiate shrimps, as described by Newman and Knight (1984) and Casanova et al.
(2002), roughly ref lects the way in which the decapod cephalothorax approximately appeared
originally during evolution, that is, as a gradual withdrawal of cuticle between the carapace
and thorax.
ON CARAPACE HOMOLOGIES AND EARLY CARAPACE EVOLUTION
Calman’s Crustacean Carapace Hypothesis: Critical Survey of Recent Discussions
The term carapace has been used for Crustacea prior to Calman (1909), but since he gave a
brief and precise summary of the occurrence of the carapace within the Crustacea, his work has
often been used as a starting point when discussing its evolution. Because his summary has been
referred to so often in later works and has occasionally been rebutted (e.g., Dahl 1991), a brief
outline of what Calman actually wrote is given here. Calman (1909) suggested that since a dorsal
shield or carapace (he used both terms) occurs in the most diverse groups of Crustacea, it is prob-
ably a primitive attribute of the taxon. He also said that it originates as a fold of the integument
from the posterior margin of the cephalic region. Then he outlined some of the various forms a
carapace can take, such as in notostracan branchiopods, where the carapace loosely envelopes
more or less of the trunk, or as in other branchiopods (clams shrimps) and ostracods (mussel
shrimps), where it forms a bivalved shell completely enclosing body and limbs. Finally, he men-
tioned some of the extreme cases, such as adult cirripedes, where it forms a fleshy mantle usually
strengthened by shelly plates, and some malacostracans, where the carapace has coalesced with
the tergites of some or all thoracic somites, though it may project freely at the sides, overhanging,
as in Decapoda, the branchial chambers.
This short summary of Calman was excellent for the time and encapsulates a number of the
questions still discussed today. For example, the question of whether or not Crustacea originally
had a carapace was treated by Hessler and Newman (1975), who depicted two different possible
“urcrustaceans,” one with a carapace and one without. We have still not reached an entirely
convincing solution to this question, which, given the age, diversity, and morphological dispar-
ity of Crustacea, is not too surprising (see chapter 1 in this volume). Even Hexapoda (insects
and allies) may be an ingroup of Crustacea (e.g., Regier et al. 2010), which highlights the great
variation in crustacean body plans. Since a crustacean/arthropod carapace is an adaptation
to an aquatic lifestyle, no such structure is needed in the terrestrial/aerial hexapods and must
have been reduced if hexapods eventually turn out to have originated from carapace-bearing
crustaceans, or it may never have been present in the lineage leading to Hexapoda.
Dahl (1983, 1991) spent much effort attempting to weaken/invalidate Calman’s idea of the
carapace as a primitive (and therefore homologous) attribute of the Crustacea. The evolution-
ary status of the carapace for Crustacea as a whole is still uncertain, but at least some of the
main arguments used by Dahl were problematic. The essence of Dahl’s view seems to be that
if structures (e.g., a carapace) have dissimilar ontogenesis in different taxa, then they cannot
be homologous. He argued that since carapace structures originate ontogenetically in so many
different ways in Crustacea and, in Dahl’s (1991) view, seemingly never as a dorsal fold derived
from the cephalon, then this invalidates the “carapace hypothesis” of Calman (1909). Indeed,
the early ontogeny of the carapace in Crustacea is very diverse, and certainly a straightforward
ontogeny from the rear of the cephalon is rare, but is nevertheless seen in various malacostracan
free-living larvae (see above and Figs. 4.15B,C, 4.16C–F), in branchiurans, in various thecostra-
cans, in “Orsten” crustaceans such as Rehbachiella (Fig. 4.8), and in branchiopods such as Triops
(Fig. 4.10).
Dahl (1991) distinguished a number of different carapace types named after the part of the body
that gives rise to the early carapace fold, and even though he said that the terms used for describing
these were “purely descriptive and without evolutionary or phylogenetic implications,” this was
nevertheless probably his most important argument for considering Calman’s “carapace hypoth-
esis” as invalid. He named six types of early carapace ontogenies that differed with respect to the
specific location of the early carapace fold(s) (dorsal, lateral, etc.) and with respect to how much
of the body is involved in forming the early carapace lobe (e.g., how many segments) (Dahl 1991).
Watling (1999) summarized Dahl’s arguments and highlighted that early carapace formation in the
short-carapace peracarids, such as Cumacea, takes place as lateral outpouchings (so-called branchi-
ostegal folds). However, while it obviously speaks in favor of homology if the carapace in various
taxa can be shown ontogenetically to have the same origin, the opposite is not necessarily the case:
structures, such as a carapace, may still be homologous despite having dissimilar ontogenetic ori-
gins (for a summary of the connection between ontogeny and evolution, see de Beer 1958, 149–153).
It is well known that a given ontogenetic sequence in itself is also subject to evolutionary modifica-
tions, so the dissimilar ontogeny of various carapaces in Crustacea does not necessarily indicate
convergent evolution; they could with equal right be explained as modifications of the ontogenetic
sequence.
Much attention has been devoted to whether or not the “origin” of the carapace is maxil-
lary. Calman (1909) was cautious enough to specify the “origin” of the carapace as being in
the “cephalic region,” while later authors, including Dahl (1991), have taken this as Calman
(1909) specifically suggesting that the carapace folds originated from the rear of the second
maxilla segment. It is difficult to trace at what stage Calman’s carapace hypothesis became
modified from Calman’s broad statement to a more specific definition as the one referred
to by Dahl (1983, 198), who writes that “according to the classical concept the carapace is a
fold growing out from the maxillary segment.” But it seems that much of the discussion and
confusion of carapace homologies within Crustacea could have been avoided if the focus had
not been so much on whether the carapace is maxillary. As a matter of fact, there is no reason
for considering an ontogenetic origin of the carapace from the second maxilla segment as the
holy grail when it comes to carapace homologies within Crustacea. As outlined above, a dis-
similar ontogeny does not necessarily invalidate homology. The development of the carapace
in the Cambrian Rehbachiella kinnekullensis is here of special interest since, as outlined above,
the carapace in different phases of the development integrates a varying proportion of the
cephalic region. For example, at a certain stage, the carapace extends from the rear of the first
maxilla region (Fig. 4.8C) and later from the rear of the second maxilla (Fig. 4.8D) (Walossek
1993). In the same line, as highlighted by Dahl (1991), taxa such as Notostraca and Leptostraca
(see Fig. 4.16A,B) have carapaces that do not extend entirely freely from the cephalic region
but actually are fused to the dorsum of one or more thoracic segments. However, an integra-
tion of a few extra segments into the carapace does not necessarily indicate nonhomology to
the carapace of taxa where this is not the case.
Contribution to Carapace Discussion by Well-Preserved Cambrian “Orsten” Fossils
Important evidence on early carapace evolution within the Crustacea is provided by the stud-
ies on Cambrian microfossils such as Rehbachiella kinnekullensis and Bredocaris admirabilis
(see Mü ller and Walossek 1988, Walossek 1993). The early carapace development in both taxa
is rather similar and can be described as a simple growth of the posterior margin of the nau-
pliar shield present earlier in development, resulting in free posterior shield margins covering
a smaller or larger part of the trunk (Fig. 4.8). Actually, as already recognized by Fryer (1996),
such a simple type of carapace growing from the rear of the head region as seen in Rehbachiella
is indistinguishable from what was suggested primitively for Crustacea by Calman (1909).
Walossek (1993, 198) used the term “cephalic shield” for Rehbachiella but was aware of the
similarity to the “carapace” as this structure is understood by other authors since, for exam-
ple, he stated that the ‘free carapace’ of Newman and Knight (1984) is more or less synony-
mous with the cephalic shield of Rehbachiella and other taxa. As mentioned above, one of
the much-discussed dogmas concerning carapace homologies has been the assumed origin
from the second maxilla segment (“cephalic region” in Calman’s terms). Walossek (1993) has
clarified that this is a simplified discussion since in both Rehbachiella and Bredocaris the exact
segment from which the free carapace margins extend depends on which developmental stage
is considered (Fig. 4.8).
Of course, one should be careful assuming that the mode of carapace development in
Rehbachiella is ancestral just because Rehbachiella is old. Regardless, from an evolutionary point
of view, the carapace seen in Rehbachiella would seem as an ideal starting point for carapaces in
crustaceans such as malacostracans, branchiopods, branchiurans, and thecostracans. However,
the information provided by Cambrian “Orsten” fossils is ambiguous since some taxa lack a
carapace. Skara (see Mü ller and Walossek 1985), for example, is lacking a carapace that could be
an adaptation to an interstitial lifestyle. The even older Yicaris also lacks a carapace and has a
shield restricted to only the head region (Zhang et al. 2007).
CONCLUSIONS
The Crustacea exhibit a large variation in carapace structures with a wealth of functions inti-
mately linked to the lifestyle of the taxon. Some well-demonstrated functions are reduction of
drag during swimming, crawling, or during temporarily resting on the substratum; as a feeding
chamber; as a respiration chamber; and as a brooding chamber. It is clear that the plasticity of
the crustacean carapace has been an important component in crustacean evolution. It has often
been discussed whether a carapace extending from the rear of the cephalon and enveloping a
smaller or larger part of the body was present in the common ancestor to the Malacostraca or
even in the common ancestor to the Crustacea. The occurrence of a carapace of this type within
the Malacostraca, either as larvae or as adults, seems to suggest, in accordance with Calman
(1909), that such a structure was present in the Malacostraca originally, from which it follows
that it has been modified or lost in a number of malacostracan subtaxa.
Whether a carapace was present in the crustacean ancestor is more uncertain because of
a larger morphological gap between these taxa, but also similarities in carapace ontogeny in
certain taxa (malacostracans, branchiurans, branchiopods, and “Orsten” fossils) may suggest
a common origin. The fossil record is ambiguous on this question since some taxa have a cara-
pace (Rehbachiella, Bredocaris, Walossekia) and others lack it (Skara, Yicaris). The carapace in
the Cambrian fossil Rehbachiella kinnekullensis probably was close in morphology and ontogeny
to such an eventual crustacean ancestor. Differences in carapace ontogeny between different
crustacean taxa have sometimes been considered as evidence for parallel evolution of different
crustacean carapace types (e.g., Dahl 1991). However, in this chapter it is argued that differences
in ontogenetic origin of the carapace do not necessarily indicate nonhomology since an ontoge-
netic sequence in itself is also subject to evolution.
ACKNOWLEDGMENTS
I thank the editors of this book, Martin Thiel and Les Watling, for inviting me to contribute this
chapter. Gerhard Scholtz kindly provided specimens of Penaeus monodon used in Fig. 4.16. This
treatment greatly benefited from discussions with Jens Høeg, Stefan Richter, Dieter Waloszek,
and Les Watling at various occasions over the last years. Martin Thiel, Les Watling, and Stefan
Richter all read the chapter and gave useful comments. This work was supported by the Danish
Research Council (grant 09–066003).
REFERENCES
Abe, K., and J. Vannier. 1995 . Functional morphology and significance of the circulatory system of
Ostracoda, exemplified by Vargula hilgendorfii (Myodocopida). Marine Biology 124:51–58.
Atkinson, R.J.A., C. Froglia, E. Arneri, and B. Antolini. 1997. Observations on the burrows and burrow-
ing behaviour of Squilla mantis (L.) (Crustacea: Stomatopoda). Marine Ecology 18:337–359.
Barker, D. 1962. A study of Thermosbaena mirabilis (Malacostraca, Peracarida) and its reproduction.
Quarterly Journal of Microscopical Science 103:261–286.
Batang , Z.B., and H. Suzuki. 1999. Gill-cleaning mechanisms of the mud lobster Thalassina anomala
(Decapoda: Thalassinidea: Thalassinidae). Journal of Crustacean Biology 19:671–683.
Bauer, R.T. 1989. Decapod crustacean grooming: Functional morphology, adaptive value, and phy-
logenetic significance. Pages 49–73 in B.E. Felgenhauer , L. Watling , and A.B. Thistle, edi-
tors. Functional morphology and grooming in Crustacea. Crustacean Issues, Vol. 6. Balkema,
Rotterdam.
Bauer, R.T. 1998. Gill-cleaning mechanisms of the crayfish Procambarus clarkii (Astacidea: Cambaridae):
experimental testing of setobranch function. Invertebrate Biology 117:129 –143.
Biffis, C., F. Alwes, and G. Scholtz. 2009. Cleavage and gastrulation of the dendrobranchiate shrimp
Penaeus monodon (Crustacea, Malacostraca, Decapoda). Arthropod Structure and Development
38:527–540.
Blake, R.W. 1985 . Crab carapace hydrodynamics. Journal of Zoology (London) 207:407–423.
Bowman, T.E., S.P. Garner, R.R. Hessler, T.M. Iliffe, and H.L. Sanders. 1985 . Mictacea, a new order of
Crustacea Peracarida. Journal of Crustacean Biology 5:74–78.
Boxshall, G.A. 2004 . The evolution of arthropod limbs. Biological Reviews. 79:253–300.
Boxshall, G.A., and D. Jaume. 2009. Exopodites, epipodites and gills in crustaceans. Arthropod
Systematics and Phylogeny 67:229 –254.
Calman, W.T. 1909. Crustacea. Pages 1–346 in E.R. Lankester, editor. A treatise on Zoology, Part 7,
Fascicle 3. Adam and Charles Black , London .
Cannon, H.G. 1927. On the feeding mechanism of Nebalia bipes. Transactions of the Royal Society of
Edinburgh 55(2):355–369.
Cannon, H.G., and S.M. Manton. 1927. On the feeding mechanism of a mysid crustacean, Hemimysis
lamornae. Transactions of the Royal Society of Edinburgh 55:219 –253.
Casanova, B. 1991. Origine protocéphalique antennaire de la carapace chez les Leptostracés, Mysidacés
et Eucaridés (Crustacés). Comptes Rendus hebdomadaires des Séances de l’Académie des Sciences
Paris, Série III 312:461–468.
Casanova, B. 1993. L’origin protocéphalique de la carapace chez les thermosbaenacés, tanaidacés,
cumacés et stomatopodes. The protocephalic origin of the carapace in thermosbaenaceans, tanaid-
aceans, cumaceans, and stomatopods. Crustaceana 65:144–150.
Casanova, B., L. De Jong , and X. Moreau. 2002. Carapace and mandibles ontogeny in the
Dendrobranchiata (Decapoda), Euphausiacea, and Mysidacea (Crustacea): A phylogenetic interest.
Canadian Journal of Zoology 80:296 –306.
Childress, J.J. 1971. Respiratory adaptations to the oxygen minimum layer in the bathypelagic mysid
Gnathophausia ingens. Biological Bulletin 141:109–121.
Claus, C. 1877. Zur Kenntnis des Baues und der Organisation der Polyphemiden. Denkschrift
Kaiserlichen Academie der Wissenschaften, Vienna 37:137–160.
Claus, C. 1888. Ü ber den Organismus der Nebaliiden und die systematische Stellung der Leptostraken.
Arbeiten aus dem Zoologischen Institut der Universität Wien 8:1–149.
Crisp, D.J. 1955 . The behaviour of barnacle cyprids in relation to water movement over a surface. Journal
of Experimental Biology 32:569 –590.
Dahl, E. 1983. Malacostracan phylogeny and evolution. Pages 189–212 in F.R. Schram, editor. Crustacean
phylogeny. Crustacean Issues, Vol. 1. Balkema, Rotterdam.
Dahl, E. 1991. Crustacea Phyllopoda and Malacostraca: A reappraisal of cephalic and thoracic shield and
fold systems and their evolutionary significance. Philosophical Transactions of the Royal Society
London Series B 334:1–26.
de Beer, G.R. 1958. Embryos and ancestors. Clarenden Press, Oxford .
Dennell, R. 1937. On the feeding mechanism of Apseudes talpa, and the evolution of the Peracaridan feed-
ing mechanisms. Transactions of the Royal Society of Edinburgh 59:57–78.
Dingle, H., and R.L. Caldwell. 1972. Reproductive and maternal behavior of the mantis shrimp
Gonodactylus bredini Manning (Crustacea: Stomatopoda). Biological Bulletin 142:417–426.
Dumont, H.J., and S.V. Negrea 2002. Introduction to the class Branchiopoda. Guides to the Identification
of the Microinvertebrates of the Continental Waters of the World, Vol. 19. Backhuys, Leiden .
Dyer, M.F., and R.F. Uglow. 1978. Gill chamber ventilation and scaphognathite movements in Crangon
crangon (L.). Journal of Experimental Marine Biology and Ecology 31:195–207.
Ebert, D. 2005 . Ecology, epidemiology, and evolution of parasitism in Daphnia [excerpt]. U.S. National
Library of Medicine, National Center for Biotechnology Information, Bethesda, MD. Available:
http://www.ncbi.nlm.nih.gov/books/NBK2036/ (accessed May 16, 2012).
Egloff, D.A., P.W. Fofonoff, and T. Onbé 1997. Reproductive biology of marine cladocerans. Advances in
Marine Biology 31:79 –167.
Farrelly, C.A., and P. Greenaway. 1994 . Gas exchange through the lungs and gills in air-breathing crabs.
Journal of Experimental Biology 187:113–130.
Fryer, G. 1956. A report of the parasitic Copepoda and Branchiura of the fishes of Lake Nyasa.
Proceedings of the Zoological Society 127:293–344.
Fryer, G. 1960. The spermatophores of Dolops ranarum (Crustacea, Branchiura): Their structure, forma-
tion, and transfer. Quarterly Journal of Microscopical Science 101:407–432.
Fryer, G. 1968. Evolution and adaptive radiation in the Chydoridae (Crustacea, Cladocera): A study in
comparative functional morphology and ecology. Philosophical Transactions of the Royal Society
of London Series B 254:221–385.
Fryer, G. 1972. Observations on the ephippia of certain macrothricid cladocerans. Zoological Journal of
the Linnean Society 51:79 –96.
Branchiopoda). Philosophical Transactions of the Royal Society London Series B 321:27–124.
Fryer, G. 1991. Functional morphology and the adaptive radiation of the Daphniidae (Branchiopoda:
Anomopoda). Philosophical Transactions of the Royal Society of London Series B 331:1–99.
Fryer, G. 1996. The carapace of the branchiopod Crustacea. Philosophical Transactions of the Royal
Fryer, G., and G.A. Boxshall. 2009. The feeding mechanisms of Lynceus (Crustacea: Branchiopoda:
Laevicaudata), with special reference to L. simiaefacies Harding. Zoological Journal of the Linnean
Society 155:513–541.
Gicklhorn, J. 1925 . Ü ber spezifische und lokale Reduktion von Silber- und anderen Metallsalzen in den
Kiemensäckchen von Daphnia. Lotos 73:83–96.
Giesbrecht, W. 1910. Stomatopoden. Fauna Flora Golf Neapel 33:1–239.
Glenner, H., and J.T. Høeg. 1993. Scanning electron microscopy of metamorphosis in four species of
barnacles (Cirripedia Thoracica Balanomorpha). Marine Biology 117:431–439.
Gordon, I. 1957. On Spelaeogriphus, a new cavernicolous crustacean from South Africa. Bulletin of the
British Museum (Natural History) 5:31–47.
Gordon, I. 1960. On a Stygiomysis from the West Indies, with a note on Spelaeogriphus (Crustacea,
Peracarida). Bulletin of the British Museum (Natural History) Zoology 6:285–324.
Gravier, C., and P. Mathias. 1930. Sur la reproduction d’un Crustacé Phyllopode du groupe des
Conchostracés (Cyzicus cycladoides (Joly)). Comptes rendus de l’Académie des sciences 191:183–185.
Grindley, J.P., and R.R. Hessler. 1971. The respiratory mechanism of Spelaeogriphus and its phylogenetic
significance. Crustaceana 20:141–144.
Gruner, H.E. 1993. Arthropoda (ohne Insecta). A. Kaestner, editor. Lehrbuch der speziellen Zoologie.
Gustav Fischer, Stuttgart .
Grygier, M.J., and D.B. Fratt. 1984 . The ascothoracid crustacean Ascothorax gigas: Redescription, larval
development, and notes on its infestation of the Antarctic ophiuroid Ophionotus victoriae. Biology
of the Anarctic Seas XVI, Antarctic Research Series 41:43–58.
Gurney, R. 1942. The larvae of the decapod Crustacea. Ray Society, London .
Haase, W. 1975 . Ultrastruktur und Funktion der Carapaxfelder von Argulus foliaceus L. (Crustacea:
Branchiura). Zeitschrift f ü r Morphologie der Tiere 81:161–189.
Henninger, H.P., and W.H.I. Watson. 2005 . Mechanisms underlying the production of carapace vibra-
tions and associated waterborne sounds in the American lobster, Homarus americanus. Journal of
Experimental Biology 208:3421–3429.
Hessler, R.R. 1983. A defense of the caridoid facies; wherein the early evolution of the Eumalacostraca is
discussed. Pages 145–164 in F.R. Schram, editor. Crustacean phylogeny. Crustacean Issues, Vol. 1.
Balkema, Rotterdam.
Hessler, R.R., and W.A. Newman. 1975 . A trilobitomorph origin for the Crustacea. Fossils and Strata
4:437–459.
Hessler, R.R., and L. Watling. 1999. Les Péracarides: un groupe controversé. Pages 1–11 in J. Forest, edi-
tor. Traité de Zoologie. Anatomie, Systématique, Biologie, Tome VII, Fascicule IIIA. Crustacés
Péracarides, Vol. 19. Memoires de l’Institut Oceanographique Fondation Albert I, Monaco.
Høeg , J.T., N.C. Lagersson, and H. Glenner. 2004 . The complete cypris larva and its significance in
thecostracan phylogeny. Pages 197–215 in G. Scholtz , editor. Evolutionary developmental biology.
Balkema, Lisse, The Netherlands.
Høeg , J.T., and O.S. Møller. 2006. When similar beginnings leads to different ends: Constraints and
diversity in cirripede larval development. Invertebrate Reproduction and Development 49:125–142.
Høeg , J.T., M. Pérez-Losada, H. Glenner, G.A. Kolbasov, and K.A. Crandall. 2009. Evolution of mor-
phology, ontogeny and life cycles within the Crustacea Thecostraca. Arthropod Systematics and
Phylogeny 67:199 –217.
Hong , S.Y. 1988. Development of epipods and gills in some pagurids and brachyurans. Journal of Natural
History 22:1005–1040.
Jacklyn, P.M., and D.A. Ritz. 1986. Hydrodynamics of swimming in scyllarid lobsters. Journal of
Experimental Marine Biology and Ecology 101:85–99.
Jenner, R.A., C.N. Dhubhghaill, M.P. Ferla, and M.A. Wills. 2009. Eumalacostracan phylogeny and total
evidence: Limitations of the usual suspects. BMC Evolutionary Biology 9:21.
Jensen, P.G., J. Moyse, J.T. Høeg , and H. Al-Yahya . 1994 . Comparative SEM studies of lattice organs:
Putative sensory structures on the carapace of larvae from Ascothoracica and Cirripedia (Crustacea
Maxillopoda Thecostraca). Acta Zoologica 75:125–142.
Johnson, S.B., and Y.G. Attramadal. 1982. A functional-morphological model of Tanais cavolinii
Milne-Edwards (Crustacea, Tanaidacea) adapted to a tubicolous life-strategy. Sarsia 61:29 –42.
Kikuchi, S. 1983. The fine structure of the gill epithelium of a fresh-water flea, Daphnia magna
(Crustacea: Phyllopoda) and changes associated with acclimation to various salinities. Cell and
Tissue Research 229:253–268.
Koehl, M.A.R., and J.R. Strickler. 1981. Copepod feeding currents: Food capture at low Reynolds
number. Limnology and Oceanography 26:1062–1073.
Kolbasov, G.A., M.J. Grygier, J.T. Høeg , and W. Klepal. 2008. External morphology of the two cypridi-
form ascothoracid-larva instars of Dendrogaster: The evolutionary significance of the two-step
metamorphosis and comparison of lattice organs between larvae and adult males (Crustacea,
Thecostraca, Ascothoracida). Zoologischer Anzeiger 247:159 –183.
Korschelt, E., and K. Heider. 1890. Lehrbuch der Vergleichenden Entwicklungsgeschichte der
Wirbellosen Thiere. Gustav Fischer, Jena .
Lauterbach, K.-E. 1970. Der Cephalothorax von Tanais cavolinii Milne Edwards (Crustacea—
Malacostraca). Ein Beitrag zur vergleichenden Anatomie und Phylogenie der Tanaidacea.
Zoologische Jahrbücher Abteilung f ü r Anatomie und Ontogenie der Tiere 87:94–204.
Laverack , M.S., D.M. Neil, and R.M. Robertson. 1977. Metachronal exopodite beating in the mysid
Praunus flexuosus: A quantitative analysis. Proceedings of the Royal Society of London Series B
198:139 –154.
Lilljeborg , W. 1901. Cladocera Sueciae. Nova acta Regiae Societatis Scientiarum Upsaliensis Series 3,
19:1–701.
Lockhead, J.H. 1961. Locomotion. Pages 313–364 in T.H. Waterman, editor. The physiology of Crustacea:
Sense organs, integration, and behavior. Academic Press, New York.
Maas, A., C. Haug , J.T. Haug, J. Olesen, X. Zhang , and D. Waloszek. 2009. Early crustacean evolution and
Maddocks, R.F. 1992. Ostracoda. Pages 415–441 in F.W. Harrison and A.G. Humes, editors. Microscopic
anatomy of invertebrates, Vol. 9, Crustacea. Wiley-Liss, New York.
Maitland, D.P. 1990a . Aerial respiration in the semaphore crab, Heloecius cordiformis, with or without
branchial water. Comparative Biochemistry and Physiology 95A:267–274.
Maitland, D.P. 1990b. Carapace and branchial water circulation, and water-related behaviours in the
semaphore crab Heloecius cordiformis (Decapoda: Brachyura: Ocypodidae). Marine Biology
105:275–286.
Maitland, D.P. 1992a . Carapace movements aid air breathing in the semaphore crab, Heloecius
cordiformis (Decapoda: Brachyura: Ocypodidae). Journal of Comparative Physiology B
162:375–382.
Maitland, D.P. 1992b. Carapace movements associated with ventilation and irrigation of the branchial
chambers in the semaphore crab, Heloecius cordiformis (Decapoda: Brachyura: Ocypodidae).
Journal of Comparative Physiology B 162:365–374.
Martin, J.W., and G.E. Davis. 2001. An updated classification of the recent Crustacea. Natural History
Museum of Los Angeles County, Science Series 39:1–124.
Martin, J.W., and G.E. Davis. 2006. Historical trends in crustacean systematics. Crustaceana
79:1347–1368.
Mauchline, J., and T. Nemoto. 1977. Integumental sensilla of diagnostic value in euphausiids. Journal of
the Oceanographical Society of Japan 33:283–289.
Mayrat , A., B.R. McMahon, and K. Tanaka. 2006. The circulatory system. Pages 3–84 in J. Forest ,
J.C. von Vaupel Klein, and F.R. Schram, editors. Treatise on zoology—anatomy, taxonomy,
biology The Crustacea revised and updated from the Traité de Zoologie, Vol. 2. Koninklijke Brill,
Leiden .
McKenzie, K.G., and P.-J. Chen. 1999. Kazacharthra. Pages 443–458 in E. Savazzi, editor. Functional
morphology of the invertebrate skeleton. John Wiley and Sons, Chichester.
Meland, K., and E. Willassen. 2007. The disunity of “Mysidacea” (Crustacea). Molecular Phylogenetics
and Evolution 44:1083–1104.
Møller, O.S. 2009. Branchiura (Crustacea)—survey of historical literature and taxonomy. Arthropod
Møller, O.S., J. Olesen, and J.T. Høeg. 2003. SEM studies on the early development of Triops cancriformis
(Bosc) (Crustacea: Branchiopoda: Notostraca). Acta Zoologica 84:267–284.
Mü ller, G.W. 1894 . Ostracoda . Fauna und Flora Golf Neapel 21:1–404.
Mü ller, K.J., and D. Walossek. 1985 . Skaracarida, a new order of Crustacea from the upper Cambrian of
Mü ller, K.J., and D. Walossek. 1988. External morphology of the Upper Cambrian maxillopod Bredocaris
admirabilis. Fossils and Strata 23:1–70.
Newman, W.D., and M.D. Knight. 1984 . The carapace and crustacean evolution—a rebuttal. Journal of
Oelze, A. 1931. Beiträge zur Anatomie von Diastylis rathkei Kr. Zoologische Jahrbücher. Abteilung f ü r
Anatomie und Ontogenie der Tiere 54:235–294.
Olesen, J. 1999. Larval and post-larval development of the branchiopod clam shrimp Cyclestheria hislopi
(Baird, 1859) (Crustacea, Branchiopoda, Conchostraca, Spinicaudata). Acta Zoologica 80:163–184.
Olesen, J. 2005 . Larval development of Lynceus brachyurus (Crustacea, Branchiopoda, Laevicaudata):
Redescription of unusual crustacean nauplii, with special attention to the moult between last nau-
plius and first juvenile. Journal of Morphology 264:131–148.
Olesen, J. 2007. Monophyly and phylogeny of Branchiopoda, with focus on morphology and homologies
of branchiopod phyllopodous limbs. Journal of Crustacean Biology 27:165–183.
Olesen, J. 2009. Phylogeny of Branchiopoda (Crustacea)—character evolution and contribution of
uniquely preserved fossils. Arthropod Systematics and Phylogeny 67:3–39.
Olesen, J., and M.J. Grygier. 2003. Larval development of Japanese “conchostracans”: Part 1, larval
development of Eulimnadia braueriana (Crustacea, Branchiopoda, Spinicaudata, Limnadiidae)
compared to that of other limnadiids. Acta Zoologica 84:41–61.
Olesen, J., and M.J. Grygier. 2004 . Larval development of Japanese “conchostracans”: Part 2, larval devel-
opment of Caenestheriella gifuensis (Crustacea, Branchiopoda, Spinicaudata, Cyzicidae), with notes
on homologies and evolution of certain naupliar appendages within the Branchiopoda. Arthropod
Structure and Development 33:453–469.
Olesen, J., S.T. Parnas, and J.F. Petersen. 2006. Tail flip and escape response of Tethysbaena argentarii
(Crustacea: Thermosbaenacea). Journal of Crustacean Biology 26:429 –432.
Olesen, J., S. Richter, and G. Scholtz. 2003. On the ontogeny of Leptodora kindtii (Crustacea,
Branchiopoda, Cladocera), with notes on the phylogeny of the Cladocera. Journal of Morphology
256:235–259.
Olesen, J., and D. Walossek. 2000. Limb ontogeny and trunk segmentation in Nebalia species.
Zoomorphology 120:47–64.
Patek , S.N., and R.L. Caldwell. 2006. The stomatopod rumble: Low frequency sound production in
Hemisquilla californiensis. Marine and Freshwater Behaviour and Physiology 39:99 –111.
Pérez Farfante, I. 1988. Illustrated key to penaeoid shrimps of commerce in the Americas. NOAA
Technical Report NMFS 64. U.S. Department of Commerce, Washington, DC.
Pirow, R., F. Wollinger, and R.J. Paul. 1999a . The importance of the feeding current for oxygen uptake in
the water flea Daphnia magna. Journal of Experimental Biology 202:553–562.
Pirow, R., F. Wollinger, and R.J. Paul. 1999b. The sites of respiratory gas exchange in the planktonic
crustacean Daphnia magna: An in vivo study employing blood haemoglobin as an internal oxygen
probe. Journal of Experimental Biology 202:3089 –3099.
Potts, W.T.W., and C.T. Durning. 1980. Physiological evolution in the branchiopods. Comparative
Biochemistry and Physiology 67B:475–484.
Rathbun, M.J. 1930. The cancroid crabs of America of families Euryliidae, Portunidae, Atelecyclidae,
Cancridae, and Xanthidae. Bulletin of the American Museum of Natural History 152:1–593.
Regier, J.C., J.W. Shultz , A. Zwick, A. Hussey, B. Ball, R. Wetzer, J.W. Martin, and C.W. Cunningham
2010. Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding
sequences. Nature 463:1079 –1084.
Richter, S., O.S. Møller, and C.S. Wirkner. 2009. Advances in crustacean phylogenetics. Arthropod
Richter, S., J. Olesen, and W.C. Wheeler. 2007. Phylogeny of Branchiopoda (Crustacea) based on a com-
bined analysis of morphological data and six molecular loci. Cladistics 23:301–336.
Ruello, N.V. 1973. Burrowing, feeding, and spatial distribution of the school prawn Metapenaeus macleayz
(Haswell) in the hunter river region, Australia. Journal of Experimental Marine Biology and
Ecology 13:189 –206.
Rybakov, A.V., J.T. Høeg , P.G. Jensen, and G.A. Kolbasov. 2003. The chemoreceptive lattice organs
in cypris larvae develop from naupliar setae (Thecostraca: Cirripedia, Ascothoracida and
Facetotecta). Zoologischer Anzeiger 242:1–20.
Samter, M. 1895 . Die Verä nderung der Form und Lage der Schale von Leptodora hyalina Lillj. wä hrend der
Entwicklung. Zoologischer Anzeiger 483:334–338, 484:341–344.
Sars, G.O. 1887. On Cyclestheria hislopi (Baird), a new generic type of bivalve Phyllopoda; raised from
dried Australian mud. Christiania Videnskabs-Selskabs Forhandlinger 1:1–65.
Sars, G.O. 1896. Fauna Norvegiæ. Bd. I. Beskrivelse af de hidtil kjendte norske Arter af Underordnerne
Phyllocarida og Phyllopoda [Descriptions of the Norwegian species at present known belonging to
the suborders Phyllocarida and Phyllopoda]. Joint-Stock, Christiania, Norway.
Schminke, H.K. 1981. Adaptation of Bathynellacea (Crustacea, Syncarida) to life in the interstitial (“Zoea
theory”). Internationale Revue der gesamten Hydrobiologie 66:575–637.
Systematics and Evolutionary Research 38:175–187.
Siewing , R. 1952. Morphologische Untersuchungen an Cumaceen. Zoologische Jahrbücher. Abteilung f ü r
Siewing , R. 1958. Anatomie und Histologie von Thermosbaena mirabilis. Ein beitrag zur Phylogenie der
Reihe Pancarida (Thermosbaenacea). Abhandlungen der Mathematisch Naturwissenschaftlichen
Klasse/Akademie der Wissenschaften und der Literatur in Mainz 7:195–270.
Siewing , R. 1963. Studies in malacostracan morphology: Results and problems. Pages 85–110 in H.B.
Whittington and W.D.I. Rolfe, editors. Phylogeny and evolution of Crustacea. Museum of
Comparative Zoology, Cambridge, MA .
Siveter, D.J., D.J. Siveter, M.D. Sutton, and D.E.G. Briggs. 2007. Brood care in a Silurian ostracod.
Proceedings of the Royal Society 274:465–469.
Smirnov, N.N., and A.A. Kotov. 2009. Morphological radiation with reference to the carapace valves of
the Anomopoda (Crustacea: Cladocera). International Review of Hydrobiology 94:580–594.
Smith, R.J., T. Kamiya, and D.J. Horne. 2006. Living males of the “ancient asexual” Darwinulidae
(Ostracoda: Crustacea). Proceedings of the Royal Society of London Series B 273:1569 –1578.
Stenderup, J.T., J. Olesen, and H. Glenner. 2006. Molecular phylogeny of the Branchiopoda
(Crustacea)—multiple approaches suggest a “diplostracan” ancestry of the Notostraca. Molecular
Phylogenetics and Evolution 41:182–194.
Swanson, K.M. 1989. Manawa staceyi n.sp. (Punciidae, Ostracoda): Soft anatomy and ontogeny. Courier
des Forschunginstitutes Senckenberg 113:235–249.
Tattersall, W.M., and O. Tattersall. 1951. The British Mysidacea. Ray Society, London .
Vannier, J., P. Boissy, and P. Racheboeuf. 1997. Locomotion in Nebalia bipes: A possible model for
Palaeozoic phyllocarid crustaceans. Lethaia 30:89 –104.
Walker, G. 2004 . Swimming speeds of the larval stages of the parasitic barnacle, Heterosaccus lunatus
(Crustacea: Cirripedia: Rhizocephala). Journal of the Marine Biological Association of the United
Kingdom 84:737–742.
Walker, G., and R.J.G. Lester. 2000. The cypris larvae of the parasitic barnacle Heterosaccus lunatus
(Crustacea, Cirripedia, Rhizocephala): Some laboratory observations. Journal of Experimental
Marine Biology and Ecology 254:249 –257.
Walker, G., A.B. Yule, and J.A. Nott. 1987. Structure and function in balanomorph larvae. Pages 307–327
in A.J. Southward, editor. Barnacle biology. Crustacean Issues, Vol. 5. Balkema, Rotterdam.
Watling , L. 1999. Toward understanding the relationship of the peracaridan orders: The necessity of
determining exact homologies. Pages 73–89 in F.R. Schram and J.C. von Vaupel Klein, editors.
Crustaceans and the biodiversity crisis. Brill, Leiden .
Williamson, D.I. 1973. Amphionides reynaudii (H. Milne Edwards), representative of a proposed new
order of Eucaridian Malacostraca. Crustaceana 25:35–50.
Wirkner, C.S., and S. Richter. 2007. The circulatory system in Mysidacea—implications for the phylo-
genetic position of Lophogastrida and Mysida (Malacostraca, Crustacea). Journal of Morphology
268:311–328.
Wirkner, C.S., and S. Richter. 2009. Evolutionary morphology of the circulatory system in Peracarida
(Malacostraca; Crustacea). Cladistics 25:1–25.
Zhang , X. -g., D.J. Siveter, D. Waloszek , and A. Maas. 2007. An epipode-bearing crown-group crustacean
from the Lower Cambrian. Nature 449:595–598.
Zimmer, C. 1932. Beobachtungen an lebenden Mysidaceen und Cumaceen. Sitzungsberichte der
Gesellschaft Naturforschender Freunde zu Berlin 18:326 –347.
Zimmer, C. 1941. Cumacea. Bronns Klassen und Ordnungen des Tierreichs, Band 5, Abteilung 1, Buch IV,
Teil 5. Akademische Verlagsgesellschaft, Leipzig.
Zimmer, C., and H.E. Gruner. 1956. Euphausiacea. Bronns Klassen und Ordnungen des Tierreichs, Band
5, Abteilung 1, Buch VI, Teil 3. Akademische Verlagsgesellschaft, Leipzig.
5
THE CRUSTACEAN INTEGUMENT: STRUCTURE AND FUNCTION
Richard M. Dillaman, Robert Roer, Thomas Shafer, and

Shannon Modla
Abstract
The dorsobranchial exoskeleton of decapods has served as the archetype for studies of the struc-
ture and formation of crustacean cuticle. This cuticle consists of four layers: the epi-, exo-, and
endocuticles, which are mineralized with calcium carbonate, and the inner membranous layer.
The inner three layers are formed from chitin-protein fibrils arranged in parallel lamellae that
have a constantly changing orientation from layer to layer. This results in a plywoodlike com-
posite, with the mineral aligning with the orientation of the fibrils. The exoskeleton is thus a
composite structure with remarkable biomechanical resistance to fracture propagation. In dif-
ferent species and within different regions of the body of individuals, the cuticle shows many
variations on this basic pattern. Both the numbers of layers and presence or degree of miner-
alization are highly variable. Examples of thin, pliable, uncalcified cuticles include those of the
arthrodial, gill, and branchial chamber, contrasted by the heavily mineralized cuticle of the tips
of the chelipeds, which may be reinforced with other minerals. The cuticle is cyclically shed and
reformed to permit growth. The hypodermis first separates from the old cuticle and, in general,
begins to secrete the components of the new epi- and exocuticle. When the animal emerges from
the old exoskeleton, the endocuticle and membranous layer are deposited. Again, modifications
of this scheme are seen in different cuticle types. The cyclical nature of cuticle formation and
the temporal and spatial separation of the events of matrix deposition and calcification render
the crustacean cuticle an excellent model for the study of the control of biomineralization.
INTRODUCTION
The crustacean cuticle shares many structural and functional features with the cuticle of other
arthropods, especially insects. One of the most obvious constraints of a rigid exoskeleton is that
140
The Crustacean Integument: Structure and Function 141
it must be periodically shed so that the organism can increase in size. This means that cuticle
deposition is not a singular event but, over a lifetime, is a succession of depositions interspersed
with the shedding or loss of the old cuticle. Any review of the crustacean cuticle must recog-
nize the outstanding work of early anatomists and physiologists who described the ultrastruc-
ture of the arthropod cuticle and who put it in both an anatomical and developmental context.
Much of this early work was done on insects (Wigglesworth 1933 from Travis 1963) and served
as the standard, or frame of reference, for investigations on the crustacean cuticle. For exam-
ple, Neville (1975), in his volume Biology of the Arthropod Cuticle, describes a basic plan for the
arthropod cuticle but one that recognizes that there is not a single type of cuticle. He therefore
describes four different plans: tanned (sclerotized, cross-linked) solid cuticle, untanned solid
cuticle, rubberlike cuticle, and arthrodial membrane.
Revealing the plan for the crustacean cuticle is even more complex because major portions of
the cuticle are calcified, thereby requiring a mechanism for deposition of the mineral as well as
a means for selective removal of the mineral prior to shedding the old cuticle. The extracellular
nature of the cuticle means that it accumulates over time. One consequence of this pattern is that
any changes in the composition of the cuticle are a direct reflection of changes in the activity of
the epithelium underlying the cuticle at a specific time. The changes in the layers can be either
structural (e.g., a change in the composition or organization of the components of the cuticle)
or functional (e.g., the ability or inability of the cuticle to mineralize). Furthermore, in the latter
case function may not be expressed immediately upon deposition but may be expressed at a later
time (e.g., the ability to calcify may be determined early in premolt but not expressed until post-
molt). This type of expression pattern makes it particularly important that one be able to identify
candidate proteins and glycoproteins that are associated with various aspects of cuticle deposi-
tion and also to determine the pattern of gene expression for those proteins and glycoproteins.
Another factor that must be considered when characterizing cuticle formation is that differ-
ent regions of the cuticle vary considerably in structure and timing of their deposition. Structural
differences, of course, lead to functional differences. For example, the arthrodial membranes
have a flexible, noncalcified cuticle, thereby allowing movement of the appendages, but they
are deposited at the same time as the calcified dorsal carapace (Williams et al. 2003). Likewise,
differences in timing have functional consequences. For example, the thin, uncalcified cuticle
of the gills, which presents a minimal barrier to diffusion, is not replaced until all of the other
regions of the cuticle have been synthesized (Andrews and Dillaman 1993).
STRUCTURE AND COMPOSITION OF THE CUTICLE
The dorsal carapace of decapod brachyuran crustaceans (e.g., Carcinus maenas, Callinectes sap-
idus, Scylla serrata) has been the most widely studied and characterized region of the exoskel-
eton. It will thus serve as the prototype for the following description of the structure and
composition of the cuticle and for comparison with other taxonomic groups and regions of the
skeleton. An understanding of the function, development, and dynamics of the dorsal carapace
requires knowledge of its structure when fully elaborated, at the intermolt period. While current
descriptions of the crustacean exoskeleton have been refined since our previous reviews (Roer
and Dillaman 1984, 1993), the basic organization remains remarkably similar to that portrayed
in early studies of the insect cuticle by such icons as Locke (1959, 1960, 1961) and Neville (1975).
In common, current terminology, the four layers of the crustacean cuticle are (from distal to
medial) the epicuticle, exocuticle, endocuticle, and membranous layer. The organization and
structure of these layers are shown in Figs. 5.1 and 5.2. The epicuticle itself is approximately 5 μm
in thickness (Roer and Dillaman 1984) and comprises three layers: the outer surface coat, a cuti-
culin layer that has five sublayers, and a thick inner epicuticle that contains amorphous material
A B C G
epicuticle
exocuticle epicuticle
exocuticle
endocuticle
membranous layer
hypodermis endocuticle
F
E
D
membranous layer
hypodermis
Fig. 5.1.
(A–F) Schematic of the molt cycle in Callinectes sapidus showing the layers present at intermolt (A; stage C4),
apolysis (B; stage D0), late premolt (C; stage D3–D4), early postmolt (D; stage A 1), middle postmolt (E;
stage B), and late postmolt (F; stage C3). (G) Section through an intermolt cuticle stained with acridine
orange.
and fibers (~6 nm in diameter) perpendicular to the surface (Compére 1995). Intercalated
within this set of fibers are others that extend down into the outer margin of the exocuticle
below (Modla 2006; Fig. 5.3A).
The exo- and endocuticles comprise a highly organized, organic framework of chitin-protein
fibrils and, in many regions, are hardened by sclerotization and/or impregnation with mineral
salts. The basis for the laminate structure of these fibrils has been a matter of study and debate
for many years (Bouligand 1972). Recent reports employing more sophisticated analytical tech-
niques have revealed a continuum of organization from the molecular to the tissue levels (Raabe
et al. 2005a, 2005b, 2007, Fabritius et al. 2009). These analyses explain not only the underlying
structure but also many of the composite biomechanical properties of the cuticle.
At the molecular level, the chitin fibrils are composed of β -1,4-linked N-acetylglucosamine
residues arranged in antiparallel chains of α-chitin. Groups of 18–25 chitin fibrils are wrapped
by proteins to form nanofibrils that are 2–5 nm in diameter and approximately 300 nm in length
(Raabe et al. 2005a, 2005b, 2007, Sachs et al. 2006, Romano et al. 2007, Fabritius et al. 2009).
The nanofibrils, in turn, cluster to form chitin-protein fibers that are 50–250 nm in diameter. As
the fibers aggregate into flat sheets parallel to the apical surfaces of the epithelial cells, they are
arranged around the microvilli forming pore canals. This gives the chitin-protein sheets a fenes-
trated appearance when viewed in tangential planes. The chitin-protein sheets are stacked, one
upon the next, with a slight rotation in the axis of the fiber orientation relative to the previous
layer (Fig. 5.2A). This imparts a plywoodlike structure to the cuticle, originally described for the
crustacean exoskeleton by Bouligand (1972). Each lamella in the exo- or endocuticle represents a
180° rotation in the orientation of the chitin-protein fibers within the sheets. The thickness of a
lamella is greater in the endocuticle (~8 μm) than in the exocuticle (~2 μm; see Fig. 5.2), which is
thought to be due to the relative angle between adjacent sheets of fibers, that is, smaller angles of
rotation in the endocuticle resulting in thicker lamellae since more layers are required to effect a
Fig. 5.2.
Microstructure of lobster cuticle. (A) Schematic representation of the different hierarchical levels in the
microstructure of lobster cuticle starting with the N-acetyl-glucosamine molecules (I) forming antiparal-
lel α-chitin chains (II). Between 18 and 25 of these molecules wrapped with proteins form nanofibrils (III),
which cluster to form chitin protein fibers (IV) that are arranged in horizontal planes in which the long
axes of the fibers are all oriented in the same direction. The fibers are arranged around the cavities origi-
nating from the extremely well-developed pore canal system that gives the structure a honeycomb-like
appearance (V). These chitin protein planes are stacked with the orientation of the fibers in superimposed
layers rotating gradually around the normal axis of the cuticle, thus creating a typical twisted plywood
structure (VI). (B) Scanning electron microscropic (SEM) micrograph showing a cross section through
the three-layered cuticle. The different stacking density of the twisted plywood layers (tp) in the exo-
and endocuticle can be clearly seen. (C) SEM micrograph of obliquely fractured endocuticle displaying
two superimposed twisted plywood layers (tp) and showing their typical honeycomb-like structure. The
arrows indicate the pore canals. From Romano et al. (2007, fig. 1), with permission from Elsevier.
180° rotation. Presumably, the stacking angles are determined by the proteins that wrap the chi-
tin fibrils. In fact, differences in the exo- and endocuticular proteins have been well documented
(Skinner et al. 1992), as have differences in the sugar residues associated with cuticular glycopro-
teins (Marlowe et al. 1994; Compére et al. 2002). These differences also account, at least in part,
for the differences in tanning or sclerotization that occur between these layers. The exocuticle
is stabilized and hardened by quinone cross-linking effected by phenoloxidase, whereas such
tanning does not occur in the endocuticle.
The parallel, planar orientation of the chitin-protein lamellae and associated min-
eral is reflected in the predominant chitin and mineral crystallographic axes as revealed by
Fig. 5.3.
Transmission electron microscopic images of 1-hour postmolt cuticle of Callinectes sapidus fixed with 2.5%
glutaraldehyde. (A) Cross section through epicuticle. Note the dense vertical fibers (dvf), epicuticular
fibers (ef), epicuticular canals (ec), epicuticular roots (er), and inner (ie) and outer (oe) epicuticle. (B)
Cross section through single lamella of exocuticle. Note the vertical fibers (vf) and horizontal fibers
(arrowheads). (C) Tangential section through the proximal exocuticle. Note the anchoring fibers (af),
horizontal fibers (hf), pore canals (pc), pore canal fibers (pcf), and pore canal sheaths (pcs). (D) Cross
section through proximal exocuticle and tendinous epidermal cell. Note the insertion of the tonofibers (tf)
into the cell as well as the dense structures (d) and microtubules (mt) in the cell. (E) Tangential section
through the proximal exocuticle above a tendinous epidermal cell. Note the electron-dense rods (r) and
tonofibers (tf). (F) Tangential section through the exocuticle. Note the region of the interprismatic septa
(IPS). From Modla (2006, figs. 1a, 2d, 5e, 6d, 7d, and 9b), used with permission from the author.
synchrotron Bragg diffraction (Raabe et al. 2005a, 2007) and X-ray diffraction of cuticular
samples (Raabe et al. 2006, 2007, Krywka et al. 2007, Al-Sawalmih et al. 2008). When the dif-
fraction patterns are projected upon the {020} crystallographic plane, which runs normal to
the surface in the transverse direction (90° to the long axis of the body of the lobster Homarus
Fig. 5.4.
Survey of the {020} synchrotron pole figures of the orthorhombic α-chitin taken from different parts of
the cuticle. LD, longitudinal reference direction; ND, reference direction normal to the local surface; TD,
transverse direction. Specimens were taken from a highly mineralized part of the cuticle on pincher claw
(left cheliped), crusher claw (right cheliped), cephalothorax, and abdomen. Specimens were also taken
from poorly mineralized positions on the telson or abdomen (dashed line). From Raabe et al. (2007, fig. 5),
with permission from Elsevier.
americanus), pole figures (as shown in Fig. 5.4) demonstrate a strong orientation along the long
axis of the body (Raabe et al. 2007). A pole figure is a crystal orientation measurement and is so
named because it is often plotted in polar coordinates consisting of the tilt and rotation angles
with respect to a given crystallographic orientation. These data are interpreted to reflect the
orientation of the chitin-protein molecules within the lamellae that are parallel to the cuticle
surface. The pole figures, however, also reveal a secondary crystallographic axis normal to the
surface of the cuticle. It was concluded that this represents chitin and mineral associated with
the vertical pore canals perpendicular to the lamellar elements. As discussed below, numerous
vertical elements are found in the exoskeleton of Callinectes that could also contribute to the
observed orientation in the normal dimension.
Investigations in our laboratory on the ultrastructure of late premolt and early postmolt blue
crabs have demonstrated that numerous fibrous structures run parallel to the twisted-ribbon
shaped pore canals and therefore perpendicular to the horizontal chitin protein fibers forming
the Bouligand or twisted plywood layers. Modla (2006) used transmission electron microscopy
after conventional glutaraldehyde fixation or uranyl acetate fixation and described the morphol-
ogy and distribution of a variety of fiber types. The epicuticle consists of a thin, three- to five-
layer outer epicuticle and a thicker inner epicuticle that is composed of epicuticular roots (er,
Fig. 5.3A) separated from one another by epicuticular canals (ec, Fig. 5.3A). The canals often
contain dense epicuticular fibers (ef, Fig. 5.3A). The predominant fibers in the exocuticle are
the chitin-protein horizontal fibers (hf, Fig. 5.3C), which run parallel to the cuticle surface and
rotate in successive planes. All other fiber types are oriented perpendicular to the cuticle sur-
face. Within the exocuticle, dense vertical fibers (dvf, Fig. 5.3A) extend from the epicuticle to
distal regions of the exocuticle. Vertical fibers (vf, Fig. 5.3B) are present in the distal and medial
exocuticle and are most likely contiguous with pore canal sheaths (pcs, Fig. 5.3C), which are
fibers associated with pore canal membranes in the medial and proximal exocuticle. Anchoring
fibers (af, Fig. 5.3C) are located in the medial and proximal exocuticle and traverse the cuticle by
intersecting bundles of horizontal fibers. Pore canal fibers (pcf, Fig. 5.3C) are proximally distrib-
uted and are associated with both the outer pore canal membrane and microtubules in the hypo-
dermis. Tonofibers (tf, Fig. 5.3D,E) and electron-dense rods (r, Fig. 5.3E) are specialized fibers
occurring in regions of muscle attachment. Uranyl acetate fixation differed from conventional
fixation in that it did not preserve cellular components, but it greatly increased the contrast of
all fiber types. Uranyl acetate fixation also permitted the visualization of the calcification initia-
tion sites along the epicuticle-exocuticle interface and interprismatic septa (IPS, Fig. 5.3F). The
interprismatic septa delineate an array of roughly hexagonal columns in the exocuticle that have
similar proportions and orientation as the lateral margins of the underlying hypodermal cells
that elaborate the cuticle (Giraud-Guille 1984, Compére 1995). Fig. 5.5 summarizes the distribu-
tion of the vertical and horizontal fibers in the epi- and exocuticle.
All three outer layers (epi-, exo- and endocuticles) are mineralized. The epicuticle is par-
tially calcified, with crystals nucleated at the epi-/exocuticular margin growing up between the
vertical fibers of the inner epicuticle (Hegdahl et al. 1977, Compére 1995, Dillaman et al. 2005).
Electron-dense, amorphous deposits are sometimes seen to be associated with the surface
layer, but it is unclear whether they are synthesized by the crustacean or are a matrix associ-
ated with microorganisms on the outer surface (Read and Williams 1991). Terminations of the
pore canals are also seen on the surface of the epicuticle in some taxa (Halcrow and Bousfield
1987). Within the exo- and endocuticles, mineral is generally in the form of fused spherulites
that align with the chitin-protein fibers (Roer and Dillaman 1984, Romano et al. 2007) (Fig. 5.6,
inset).
Originally, the form of the mineral was thought to be calcium carbonate in the form of cal-
cite crystals. While substantial amounts of crystalline magnesian calcite have been confirmed
in the carapace of lobsters and crabs (Boselmann et al. 2007), it is now clear that more than one
calcium salt may be involved (depending upon the location and the species), as well as noncrys-
talline, amorphous forms of mineral. Pratoomchat et al. (2002) demonstrated the presence of
calcium phosphate (as dicalcium phosphate dehydrate and octacalcium phosphate) as a pre-
cursor to the formation of calcium carbonate during postmolt mineralization in the carapace
of the crab Scylla. Soejoko and Tjia (2003) observed that calcium phosphate minerals persist
throughout the postmolt and intermolt stages in the carapace of the giant prawn Macrobrachium
rosenbergii. The calcium phosphate is present both in crystalline and amorphous forms and
coexists with calcium carbonate in nearly equal proportions. In the terrestrial isopods Porcellio
scaber and Armadillidium vulgare, Becker et al. (2005) found the cuticle to contain crystalline
epi dvf vf
dvf vf
pc vf
pcs
pc
pcs
pcs
H
A B
af
af
pcf
pcf
C D
Fig. 5.5.
Diagrams illustrating the various vertical fiber types and features within the cuticle as well as their distri-
bution in tangential sections through the distal, medial, and proximal exocuticle. Each hexagonal prism
represents the cuticle overlying a single hypodermal cell. (A) Diagram showing the pore canals (pc)
extending from hypodermal cells (H) and dense vertical fibers (dvf) extending down from the epicuticle
(epi). (B) The distribution of vertical fibers (vf) and the pore canal sheath (pcs). Note that vertical fibers
are distal extensions of the more proximally located pore canal sheaths. (C) The distribution of anchoring
fibers (af). (D) The distribution of pore canal fibers (pcf). Adapted from Modla (2006, fig. 27d), used with
permission from the author.
magnesium calcite, amorphous calcium carbonate (ACC), and amorphous calcium phosphate.
These analyses were performed by X-ray diffraction and Fourier-transform infrared spectros-
copy (FTIR) of bulk specimens, so no precise distribution could be assigned to each of the
minerals and their morphs. However, the application of confocal-Raman spectroscopic imag-
ing has permitted mapping of the different minerals and their forms to the various cuticular
layers. In the isopods Porcellio and Armadillidium, Hild et al. (2008) clearly demonstrated that
Fig. 5.6.
Microstructure of purified chitin heat-treated at 220°C: detail images of the fibers near a pore canal.
Adjacent fibers seem to be connected by small fibrillar structures (circled areas, arrows in inset). From
Romano et al. (2007, fig. 7), with permission from Elsevier.
Epi 1 2 3 4 5 6
A
100
Peak area/counts a.u.
80
60
40
20 c
a
0 b
0 5 10 15 20 25 30 35 40 45
Distance (μm)
Fig. 5.7.
Raman spectroscopic images (A–C) and line scans (D) recorded from a sagittally cleaved and microtome
polished surface of the mineralized tergite cuticles (shown with the epicuticle to the left) of the isopod
Armadillidium vulgare show the local distribution of the various components. Calcium carbonate (A)
occurs within the whole exo- and endocuticle, whereas calcite (B) is located within the exocuticle only.
Pore canals (arrowheads) appear devoid of mineral. The amount of organic material (C) increases from
the distal to the proximal region of the cuticle. The membranous layer (position 6) is devoid of calcium
carbonate. Horizontal dotted lines in the Raman images (A–C) indicate the position where the line scans
(Epi, 1–6) were recorded for carbonate (a), calcite (b), and organic material (c) to determine material dis-
tribution. From Hild et al. (2008, fig. 5), with permission from Elsevier.
calcite was entirely restricted to the exocuticle, while the mineral in the endocuticle was uni-
formly ACC (Fig. 5.7).
The key characteristics that the dorsal carapace should exhibit in order to protect the
organism from predation are hardness and fracture resistance. The helicoidally arranged
lamellae of chitin-protein fibers and associated minerals constitute a composite material
with exceptional biomechanical properties in this regard. The force required to puncture
the dorsal carapace of lobsters (measured with a punch test) is dependent upon the thickness
of the cuticle and ranges from 6.7 kg in Homarus to 27.8 kg in the slipper lobster Scyllarides
latus (Tarsitano et al. 2006).
As would be expected, the cuticle is far more resistant to compressive forces than to ten-
sile forces. In a compressive test in the normal dimension (i.e., perpendicular to the surface),
the walking leg cuticle of the sheep crab Loxorhynchus grandis exhibited a stress to fracture
of 101 ± 11 MPa, a value comparable to aluminum and in excess of limestone (60 MPa) (Chen
et al. 2008). In contrast, the cuticle failed in a tensile test in the normal dimension at only
9.8 ± 2.6 MPa. Interestingly, the cuticle was substantially more resistant to tensile stresses
in the longitudinal dimension (shear), with a stress to fracture of 31.5 ± 5.4 MPa (Chen
et al. 2008).
HYPODERMIS AND THE MOLT CYCLE
The cuticle is underlain and periodically elaborated by the hypodermis in a cycle of deposition
and resorption referred to as the molt cycle (Drach 1939, Travis 1955, 1957, 1965, Skinner 1962,
Drach and Tchernigovtzeff 1967). These authors and others (as reviewed in Roer and Dillaman
1993) have attempted to standardize the terminology and the sequence of events of the molt
cycle by focusing on dynamics of the dorsal carapace. Recent observations have highlighted,
however, that this scheme may need to be modified for other tissues, as is detailed below.
When the cuticle of the dorsal carapace is fully elaborated, the animal is referred to as being
in intermolt (or stage C4). During this stage, the hypodermis is a simple epithelium that tends to
be squamous. While growth of the internal organs of a crustacean can occur during intermolt,
an increase in the external dimensions requires the shedding of the existing rigid exoskeleton.
A schematic representation of the molt cycle and associated cuticular changes is presented in
Fig. 5.1.
The first step in this process (referred to as early premolt or stage D0) is the separation of the
hypodermis from the cuticle, termed apolysis (Compére et al. 1998). The hypodermis is more
active during this period and becomes cuboidal and then columnar. The “old” cuticle is par-
tially degraded, and its components are resorbed during premolt stages D1 and D2 (Roer 1980,
Compére et al. 1998). Before the cuticle can enlarge, there must be an increase in the surface
area of the epithelium that secretes it and to which it is anchored by the pore canals. Stage D1 is
therefore the period of increased hypodermal mitotic activity that will result in the formation of
a larger new cuticle (Skinner 1965). The outer two layers of the new cuticle (the epi- and exocu-
ticles) begin to be deposited beneath the old cuticle during late stage D1 and stage D2. These are
often referred to as the preexuvial layers, and the organic components of these layers are thought
to be completely formed prior to the shedding of the old cuticle (termed ecdysis). It is important
to note (as discussed below) that mineralization of these layers cannot occur until the animal
emerges from the old exoskeleton and is fully expanded.
During this period of active cuticle synthesis, the individual columnar epithelial cells assume
a packing array that results in roughly hexagonal margins (Fig. 5.8A) and leads to the formation
of the interprismatic septa of the exocuticle. Furthermore, there are surface modifications of the
epithelial cells (Fig. 5.8A). The most obvious are cytoplasmic extensions resembling microvilli
that extend from the apical cell surface throughout the extracellular cuticular layers, referred
to as pore canals. Compére et al. (1998) have extensively documented the formation, extent, and
fate of the pore canals throughout the entire molt cycle. Another modification is the array of
short microvilli that constitute the “plaques” (Fig. 5.8B). These were first described in insects
(Locke 1961) and appear to be the sites of the initial polymerization and organization of the
developing cuticular components (Compére 1995, Greenaway et al. 1995, Elliott and Dillaman
1999). The plaques may provide the template for the orientation of the chitin-protein fibers that
permits them to interact with previously deposited layers. The fibers are then thought to self-
assemble in such a way that their plane of orientation is offset by a fixed angle relative to the
previous layer, thereby forming the Bouligand pattern of lamellae.
Once the organic lamellae of the preexuvial cuticle are fully formed, the next event is the
emergence of the crustacean from the old exoskeleton (exuviae). This extraordinary process of
ecdysis is initiated by the uptake of water. The resultant hydrostatic pressure causes the exuviae
to rupture at predetermined sites referred to as ecdysial sutures. Prior to the onset of postecdy-
sial tanning and mineralization, the mobility of the newly molted crab is possible because of a
hydrostatic support system. Taylor and coworkers (Taylor and Kier 2003, Taylor et al. 2007)
have demonstrated the transition from a hydrostatic skeleton to a rigid skeleton in the very early
postmolt period.
Fig. 5.8.
(A) Scanning electron micrograph of early postmolt cuticle from Callinectes sapidus. Note the fracture
along the interface between the hypodermis (h) and the exocuticle (exo) revealing the roughly hexagonal
margins of the individual hypodermal cells (arrows). In the inset, note the pore canals extending from
the surface of the hypodermal cells (arrowheads). (B) Transmission electronic micrograph of dorsal cara-
pace from premolt cuticle of Callinectes sapidus: high magnification of cross section through the proximal
exocuticle and hypodermis. Note the assembly zone (AZ) and transition zone (TZ) above the microvilli
(mv) of a tendinous epidermal cell and the electron-dense apical plaques at the microvilli (arrowheads)
and abundant microtubules (mt) in the cytoplasm (from Modla 2006, fig. 8b, used with permission from
the author). (C) Backscattered electron micrograph of 24-hour postmolt cuticle from Callinectes sapidus.
Mineralized areas appear white. Note the calcified epicuticle (arrows) and interprismatic septa of the exo-
cuticle (arrowheads) as well as the more fully calcified endocuticle (endo) (from Dillaman et al. 2005, fig.
4d2, used with permission).
The onset of cuticular hardening may be brought on by the release of the hormone bursi-
con, which has been characterized as the agent responsible for the tanning of postmolt insect
cuticle. Bursicon transcripts have recently been found in the green crab Carcinus maenas
(Wilcockson and Webster 2008). While the precise mechanisms by which tanning and min-
eralization are prevented during premolt and initiated during postmolt are not fully under-
stood (and are addressed in more detail below), the patterns of postecdysial mineralization
are apparent.
Within 3 hours of ecdysis (stages A 1 and A 2) in the blue crab Callinectes sapidus, evidence of
calcium carbonate precipitation can be seen at the epicuticle/exocuticle boundary (Dillaman
et al. 2005). Fronts of mineralization then extend along the interprismatic septa, both dis-
tally and proximally, until they meet in the center of the exocuticle, forming calcified margins
delineating the hexagonal prisms (Fig. 5.8C). This general pattern of calcification has been
described in other species (Bouligand 1972, Giraud 1977, Giraud-Guille and Quintana 1982,
Giraud-Guille 1984, Sakamoto et al. 2009). In addition to a defined sequence characteriz-
ing the pattern of mineralization, the form of the mineral also follows a prescribed sequence.
Initially, the mineral at the epi-/exocuticular boundary is presumed to be ACC based on its
solubility. Subsequently, the ACC is transformed into crystalline calcium carbonate in the
form of calcite as ACC is deposited along the interprismatic septa. This mineral also transi-
tions to calcite, completely encasing the prisms in crystalline material. The prisms themselves
then begin to calcify from the distal toward the proximal portion of the exocuticle; there is
some question as to the final mineral morph in these regions.
At the same time that the preexuvial layers are hardening (stages A 2, B1, and B2), the endo-
cuticle organic matrix is being deposited and, within a short time, calcified. The mineral
morph deposited in the blue crab has not been characterized, but that within the endocuti-
cle of isopods (Hild et al. 2008) and the lobster (Al-Sawalmih et al. 2008) is in the form of
ACC. Another component of the mineralized cuticle appears to be calcium phosphate, based
on elemental analysis (Pratoomchat et al. 2002, Soejoko and Tjia 2003), but X-ray diffraction
and FTIR spectroscopy fail to detect apatite, suggesting that this mineral is amorphous as
well. The deposition and mineralization of the endocuticle continues through postmolt stages
(C1–C3). The transition to intermolt is defined by the completion of the deposition of a non-
calcified membranous layer.
VARIATIONS IN CUTICLE T YPE AND STRUCTURE
Arthrodial Cuticle
Much of our knowledge regarding the control of tanning and mineralization is based upon
observed differences in the composition and the degree of mineralization in different cuticle
types from different regions of the body. Perhaps the most striking difference is between cuti-
cles that mineralize and those that do not.
The arthrodial cuticle is found, as the name implies, in the joints of crustacean appendages
and must remain flexible to allow for locomotion. The basic structure of arthrodial cuticle
and the timing of its deposition are similar to those of the dorsal carapace and the mineralized
cuticle with which it is contiguous. It has an epicuticle that is very similar to that of the dorsal
carapace and a Bouligand pattern of chitin-protein fibers that extend from the epicuticle to the
hypodermis. While the arthrodial cuticle of the blue crab has pore canals (the cuticle-encased
cytoplasmic extensions of the epithelial cells; Fig. 5.9A,B), some authors have stated that in
other species arthrodial cuticle lacks such structures (Raabe et al. 2007). The lamellar portion
of the arthrodial cuticle appears homogeneous, but staining of the carbohydrate moieties of the
cuticular glycoproteins clearly reveals that this lamellar portion can be divided into two lay-
ers (Fig. 5.9C). These two layers correspond spatially to the adjacent exo- and endocuticle of
the calcified cuticle, indicating that they are deposited at the same time. Indeed, the change in
thickness of the arthrodial cuticle mirrors that of the calcified cuticle in both pre- and postmolt
(Williams et al. 2003). Interestingly, the boundary between the two cuticle types is not perpen-
dicular to the cuticular surface; rather, the boundary is oblique to the surface (Fig. 5.9D). This
implies that a given patch of hypodermis must begin synthesizing arthrodial cuticle and change
to synthesizing calcified cuticle during the pre- and postmolt depositional periods. The advan-
tage of this phenomenon is that the interface between the calcified and noncalcified regions has
much greater surface area, reinforcing the junction between the two.
Branchial Chamber Cuticle
The cuticle that lines the branchial chamber of the crab is also noncalcified. In contrast to
the arthrodial cuticle, this structure is only about 6.5 μm thick in the blue crab. It is lamellar
Fig. 5.9.
(A) Transmission electronic micrograph of arthrodial membrane of stage D4 Callinectes sapidus: cuti-
cle showing the numerous lamellae and cytoplasmic extensions (arrows) roughly perpendicular to the
surface of the cuticle. (B) Note the cytoplasmic extensions (arrows) extending into the newly deposited
arthrodial membrane and the abundant microtubules (arrowheads) in the cytoplasm of the hypodermal
cells. (C) Intermolt, stage C 4, arthrodial membrane of Callinectes sapidus stained with periodic acid-Schiff
and hematoxylin. Note the boundary between the preexuvial and postexuvial cuticle (arrowhead). (D)
Section of intermolt, stage C 4, cuticle of Callinectes sapidus at the boundary between the calcified cuticle
and arthrodial membrane (a) and stained with hematoxylin and eosin. Note the diagonal margin for both
the exocuticle (exo) and endocuticle (endo). From Williams et al. (2003, figs. 2c, 2d, 5f, and 5c), used with
permission.
but possesses only approximately 30 lamellae. A feature of such thin, noncalcified cuticles in
crustaceans is a modification of the timing of deposition during the molt cycle. The branchial
chamber cuticle is secreted in its entirety during premolt, being completed by the late premolt
stage, D3 (Elliott and Dillaman 1999). Despite the fact that this cuticle is completely elaborated
at the time of the molt, it is still subject to extreme tensile forces during extraction from the old
cuticle at ecdysis. To resist these tensile forces, the hypodermal cells underlying the branchial
chamber cuticle, which were cuboidal to columnar during their secretory phase, become filled
with microtubules along their long axis and assume the structure and function of tendon cells,
anchoring the new cuticle to the connective tissue below. These microtubule-filled cells persist
through ecdysis but during early postmolt revert to the intermolt/early premolt morphology.
Gill Cuticle
The cuticle that lines the outer surface of the gills not only protects these organs from dam-
age but also represents a potential barrier to the free diffusion of respiratory gases and the
transport of ions across the gill surfaces. Consequently, the gill cuticle is extremely thin. In
the crayfish Procambarus clarkii , the cuticle surrounding the gill filaments is between 0.3 and
2 μm thick. Like the dorsal carapace, the gill cuticle usually consists of an epi-, exo-, and endo-
cuticle, albeit much thinner. In the crayfish, we observed differences among the cuticles of
the transporting filaments and the afferent and efferent channels of the respiratory filaments
(Dickson et al. 1991). The cuticle of the transporting filaments differs from the dorsal carapace
model not only in lack of mineralization and dimension (~2 μm thick) but also in the relative
proportions of the exo- and endocuticles. Whereas the endocuticle is the predominant layer
in the carapace, the composition of the cuticle of the transporting filament is approximately
two-thirds exocuticle.
The cuticle of the afferent channel of the respiratory filaments is approximately the same thick-
ness as the transport filament cuticle and is also composed of lamellate exo- and endocuticles, but
the proportions are more similar to the dorsal carapace, with the endocuticle representing more
than two-thirds of the thickness. The cuticle of the efferent channel of the respiratory filaments
is only 0.3–0.5 μm thick. It appears to possess an outer epicuticle, but the cuticle below does not
appear to be lamellate and has no obvious delineation into an exo- and endocuticle.
Like the branchial chamber cuticle, the gill cuticle is fully elaborated during premolt, with no
postmolt deposition (Andrews and Dillaman 1993). In fact, the formation of the respiratory cuticle
is delayed until late stage D2 to early D3, and deposition in the transporting gills is delayed until
early in the short, final premolt stage, D4. The net effect of these delays is that transport of ions and
diffusion of respiratory gases are subjected to a double barrier (old and new cuticular layers) for
only a very brief period of time. This principle may apply to the branchial chamber cuticle as well,
since it has been well documented that gas exchange may occur across this surface, particularly
in the case of semiterrestrial and terrestrial crabs (Greenaway and Farrelly 1984, 1990, Taylor and
Greenaway 1984).
Cheliped Cuticle
Whereas the dorsal carapace is adapted for resistance to compression and fracture propaga-
tion to protect the organism from predation, the claws must resist wear and be hard enough to
allow crushing of other mineralized structures. As mentioned in the discussion of biomechan-
ics above, one strategy for increasing hardness is simply increasing the thickness of the cuticle
(Tarsitano et al. 2006). Indeed, the cuticular thickness, even within the calcified cuticle, can
vary markedly from one region to another. Additionally, the relative proportions of exo- and
endocuticle is variable (Fig. 5.10). However, additional structural modifications of the cheliped
cuticle provide wear resistance and impart hardness. For example, the propodus of the cheliped
is some four times harder than that of the pereopods, within both the endocuticle (471 ± 50 vs.
142 ± 17 MPa) and exocuticle (947 ± 74 vs. 247 ± 19 MPa), as revealed by microindentation tests
on the sheep crab Loxorhynchus (Chen et al. 2008). Local differences in hardness have been
described within the claw of the lobster Homarus, the exocuticle of the lateral surface of the claw
being ~325 MPa and the tooth of the claw being 590 MPa. Similar differences were noted in the
stiffness (Young’s modulus) in these regions. The endocuticle of the lateral surface exhibited
a value of 6.9 GPa, compared to 11 GPa for the exocuticle (roughly equivalent to bone). The
endocuticle of the tooth had a stiffness value of 3.7 (comparable to polystyrene), while the tooth
exocuticle was measured at 25.7 (close to that for concrete) (Chen et al. 2008).
Melnick et al. (1996) compared the mechanical properties of the pigmented versus white
regions of the cheliped of the stone crab Menippe mercenaria and found that the black areas had a
higher density, elastic modulus, hardness, and fracture toughness compared to light areas. These
differences were attributed to a decreased porosity in the dark areas and perhaps a greater degree
of tanning. However, hardness may not be the desired characteristic in all chelipeds. Some
crabs employ the claws for rasping and grasping, rather than crushing, and these differences in
Fig. 5.10.
Scanning electron micrographs of transversally fractured lobster cuticle from different body parts, expos-
ing the cross sections. (A) Cuticle from the claws; the exocuticle (exo) is thin in relation to the massive
endocuticle (endo). The detail image shows fibers oriented perpendicular to the fiber planes forming the
twisted plywood layers in the pore canals (pc) and lining them (arrows). (B) Cuticle from the carapace;
exo- and endocuticle have nearly the same thickness. In the detail image, fibers oriented in the normal
direction (arrows) are also present in the pore canals (pc). (C) Cuticle from the tergites; the exocuticle is
about twice as thick as the endocuticle. At a higher magnification, fibers oriented in the normal direction
(arrows) are again visible in the pore canals (pc). (D) Cuticle from the uropods; the exocuticle is very thick
in relation to the very thin endocuticle. Fibers oriented in the normal direction (arrows) are present in the
pore canals (pc), too, but their volume fraction is smaller than in the other mineralized parts of the lobster.
(E and F) Cross section of cuticle from the joint membranes (E), with detail image (F). No pore canals are
present in these unmineralized parts of the lobster; fibers oriented in directions other than in plane with
the cuticle surface cannot be observed. From Raabe et al. (2007, fig. 10), used with permission.
function are reflected in the structure of the cuticle. Cribb et al. (2009) studied the cheliped tips
in the grapsid crab Metopograpsus frontalis and found that this region was poorly mineralized but
contained high levels of halogens. The outer exocuticle was enriched with chlorine, while the
inner exocuticle had elevated bromine. The inner endocuticle also contained abundant chlorine
(Fig. 5.11). The cuticle tips were less hard and less stiff than the carapace but had values equiva-
lent to those found for insect cuticle lacking metals. It was hypothesized that the high levels of
Fig. 5.11.
Scanning electron microscopic images of the cheliped tip of the crab, Metopograpsus frontalis.
(A) Backscattered electron image of M. frontalis cheliped tip: darker contrast indicates lower average
atomic number. Outer surface is to the left. (B–D) X-ray intensity maps for chlorine, bromine, and chlo-
rine plus bromine, respectively, across a cheliped tip from an area similar to that shown in A. X-ray inten-
sity maps use a thermal color scale; here, gray indicates the higher X-ray intensity for an element, white
lower, and black the lowest. Scale bars, 30 μm. From Cribb et al. (2009, fig. 1f,h,i,j) with permission from
Elsevier.
halogens imparted an increased hardness and low elastic modulus to the chitin-protein matrix.
The cheliped tips of Metopograpsus also have an unusual structural feature. Horizontal, rodlike
structures were observed in the fractured surfaces of the exocuticle (Fig. 5.12). The obvious anal-
ogy is that they resemble reinforcing rods in concrete.
Ecdysial Suture
Variations in cuticular structure may include local modifications of the cuticle. Such is the case
with the ecdysial suture, which is the narrow region of the ventral branchial carapace in crabs
that ruptures during ecdysis (Priester et al. 2005). Modifications include a significant decrease
in thickness, such that the location of the suture is visible to the naked eye in the intermolt crab.
Others include a decrease in mineral density and alteration in matrix composition. The decrease
in mineral density in the cuticle is achieved in a number of ways. First, the exocuticle mineralizes
only along the epicuticle/exocuticle boundary and the interprismatic septa. The prisms of the
exocuticle never fill with mineral. Second, the wedge of endocuticle immediately beneath the
less mineralized exocuticle has a demonstrably lower concentration of mineral than the adjacent
endocuticle (Fig. 5.13A). Third, while it is uncertain if the mineralogy of the suture differs from
the surrounding cuticle, elemental analysis conducted on the exo- and endocuticle components
showed that the suture contained significantly less magnesium (0.86 ± 0.29 vs. 1.75 ± 0.24 for
Fig. 5.12.
Scanning electron micrographs of noncalcified cheliped and leg tips from Metopograpsus frontalis, in trans-
verse section. (A) Fractured surface across a cheliped tip showing multiple layers (2–5). Outer surface is to
the left. Scale bar, 20 mm. (B) Fractured surface of a cheliped tip showing rods (r) filling and protruding
from holes in the layer 3 region. Scale bar, 20 mm. From Cribb et al. (2009, fig. 2a,c), with permission from
Elsevier.
the exocuticle; 0.81 ± 0.30 vs. 1.31 ± 0.14 for the endocuticle). High magnesian calcite has a lower
solubility, so it is possible that this difference renders the mineral of the suture more soluble and
labile. Assuming that the composition and location of the mineral are affected by the associated
organic matrix, one would expect to be able to detect such differences between the suture and
the adjacent cuticle. In fact, lectin binding studies revealed such differences (Fig. 5.13B). The net
effect of these alterations is that during premolt cuticle resorption, the suture region is preferen-
tially removed and weakened (Fig. 5.13C–F) so that the increase in hydrostatic pressure in stages
D4 and E is sufficient to allow the old carapace to break open along the line of the suture. The
resorption is more intense at the posterior region of the suture line, thus allowing the carapace to
open from the posterior margin, making it possible for the crab to back out of the exuviae.
TEMPORAL VARIATIONS IN CUTICULAR SYNTHESIS
The timeline for deposition of some of the aforementioned types of cuticle is summarized in
Fig. 5.14. Considering the wide diversity in the timing of deposition among these few cuticle
types that have been examined, additional variations in depositional patterns will likely be
found as other regions and types are studied.
The temporal disparities in the onset and completion of cuticle synthesis among tissues within
a single organism certainly pose interesting questions regarding the control of the cellular events
involved in the molting process. The complexity represented by these differences speaks against
a regulatory system based upon universal changes in the titers of a small number of hormones.
Nowhere is this more evident than in the biphasic molting of isopod crustaceans, in which the min-
eral of the posterior cuticle is mobilized and stored as ACC in anterior sternal deposits, followed by
the molting of the posterior cuticle, remobilization of the mineral for calcification of the posterior
cuticle, and finally the molting of the anterior cuticle (Steel 1980, 1982, Ziegler et al. 2005, 2007). In
the sea roach Ligia exotica, the temporal separation of posterior and anterior molts is approximately
24 hours, despite having an open circulatory system presumably carrying hormones throughout
both halves of the body. In fact, injections of the molting hormone ecdysterone failed to alter the
delay in molting between the two halves of the animal (Montane 1988).
Fig. 5.13.
(A) X-ray map of the calcium (Ca) distribution in an embedded and polished posterior piece of dorsal
carapace of Callinectes sapidus that includes the suture. Note the region of the suture in the exocuticle
(ex) as indicated by the arrowhead and in the endocuticle (en) as bounded by the arrows (from Priester
et al. 2005, fig. 7b, used with permission). (B) Intermolt cuticle of Callinectes sapidus in the region of the
suture stained with the fluorescein isothiocyanate–labeled lectin Lens culinaris agglutinin. Note the lack
of staining in the exocuticle (ex), the heavy staining in the suture (arrowhead), and the moderate staining
of the endocuticle (en) except in the region of the suture (arrow) (from Priester et al. 2005, fig. 1b). (C–F)
Backscattered electron micrographs of embedded and cut samples of Callinectes sapidus cuticle in early
(C) and late D2 (D–F) stages in the region containing the suture. Arrows indicate the suture region of the
endocuticle (en); arrowheads, the suture region of the exocuticle (ex). Note the different rate of etching in
the three regions of the cuticle: anterior (D), middle (E), and posterior (F) (from Priester et al. 2005, fig.
5). All figures used with permission.
Apolysis Ecdysis
Intermolt Premolt Postmolt
Calcified
cuticle
Dorsal
C4 D0 D1’ D1’’ D1’’’ D2 D3 D4 A1 A2 B1 B2 C1-C3
Carapace
Arthrodial C4 D0 D1’ D1’’ D1’’’ D2 D3 D4 A1 A2 B1 B2 C1-C3

Membrane
Inner
Uncalcified
Cuticle
Cuticle
Respiratory
Gill
Transport
Gill
No deposition Postmolt deposition
Premolt deposition
Fig. 5.14.
Timeline for cuticle deposition in various tissues of Callinectes sapidus. From Williams et al. (2003, fig. 6),
used with permission.
CONTROL OF MINERALIZATION
As mentioned above, in order for animals to enlarge their exoskeletons and grow as they molt,
they must take up water soon after ecdysis and expand the new layers of the cuticle before they
begin to harden (Drach 1939, Mykles 1980). Only after this postecdysial expansion during stage
A1 do the new epi- and exocuticle undergo quinone tanning (Travis 1957) and mineralization
by deposition of calcium carbonate (Drach 1939, Bouligand 1970, Giraud-Guille and Quintana
1982). Thereafter, the endocuticle is synthesized and mineralizes as it is deposited (postecdysial
stages A 2 through C3). Obviously, the timing of the onset of tanning and calcium carbonate
deposition is of critical importance.
The deposition of mineral within a biological system requires a number of criteria to be met.
The prime criterion is the establishment of concentrations of the composite ions that exceed the
solubility product for precipitation. This generally occurs in the context of a microenvironment
with identifiable boundaries, one of which is commonly an epithelium that can transport ions
into and out of this compartment. Second, there is an organic component that serves to hetero-
geneously nucleate the mineral by lowering the superficial energy of precipitation. The organic
matrix also is responsible for determining the mineral morph and directing the second-order
pattern of mineralization.
Permeability Changes
The microenvironment within the calcifying cuticle is bounded on the inner surface by the
hypodermis, while the outer boundary is the epicuticle. Calcium is transported into this
space by the hypodermis via the action of a calcium-ATPase and sodium-calcium exchanger
(Roer 1980, Greenaway et al. 1995). The transport of bicarbonate is mediated by carbonic anhy-
drase and likely involves the activities of HCO3–-ATPase, a Cl–/HCO3– exchanger, and a Na+/
H+ exchanger (Giraud 1981, Roer and Dillaman 1993). However, during premolt, the preexu-
vial cuticle (including the epicuticle; Fig. 5.15A,B) is freely permeable to ions and breakdown
Fig. 5.15.
(A–C) Transmission electronic micrograph of dorsal carapace from a 1-hour postmolt crab freshly fixed by
uranyl acetate: low (A) and high (C) magnification of cross sections through the epicuticle. (B) Tangential
sections through the inner epicuticle and distal exocuticle. Note the dense vertical fiber (dvf), epicu-
ticular canals (ec), epicuticular fibers (ef), epicuticular roots (er), horizontal fibers (hf), inner epicuticle
(ie), and outer epicuticle (oe) (from Modla 2006, fig. 10a–c, used with permission from the author). (D)
Scanning electron micrograph of the epicuticle in early postmolt cuticle in Callinectes sapidus. Note the
spaces between the perpendicular fibers of the epicuticle (arrowheads) and the continuous outer layer of
the epicuticle (arrows).
products of the organic matrix that pass through it during the resorption of the old exoskeleton
(Roer 1980, Compére et al. 1998). Following ecdysis, mineralization cannot commence until
the outer boundary of the cuticular microenvironment, the newly exposed epicuticle, becomes
impermeable to calcium and bicarbonate (see Fig. 5.15C,D). This transition occurs within 15 min-
utes postecdysis (Williams et al. 2009).
Matrix Proteins and Glycoproteins
Evidence suggests that the control of calcium carbonate deposition in crustacean cuticle resides
in the organic matrix of the cuticle itself, rather than in, for example, the ion-pumping activ-
ity of the underlying cellular layer (Roer and Dillaman 1984, Roer et al. 1988, Roer and Towle
2005). Using an in vitro nucleation assay, it was shown that pieces of cuticle isolated as early as
3 hours after ecdysis, stripped of all underlying cellular material, and decalcified with EDTA
can nucleate calcium carbonate crystals, whereas pieces containing the same cuticle layers
removed from a preecdysial or an ecdysial animal and treated in the same way cannot nucleate
calcite (Roer et al. 1988, Shafer et al. 1995). That is, during preecdysis and early postecdysis,
the new cuticle is incapable of nucleating calcite. Soon after ecdysis, however, mineralization
commences.
Thus, in the preexuvial layers of the crustacean cuticle, we are presented with an organic
matrix that at one time (preecdysis and early postecdysis) cannot mineralize but that over a
period of only a few hours after ecdysis is transformed into a matrix that can and does mineral-
ize. This synchronized temporal separation of the definitive control events potentially allows
for isolation and identification of the regulatory proteins involved. Moreover, the cuticle con-
tains regions that calcify (e.g., the dorsal carapace) and regions that neither calcify nor tan (the
arthrodial cuticle). Comparisons of these two types of cuticle can provide an excellent means
to elucidate those cuticular proteins important for mineralization. Comparisons of cuticular
proteins across arthropod groups can also be instructive since insects do not mineralize their
exoskeletons. Finally, a search for matrix proteins that stabilize ACC is also instructive. Control
is necessary for the persistence of ACC in the cuticle since crystalline forms of calcium carbon-
ate (calcite and aragonite) are thermodynamically favored and more stable. Evidence for such a
matrix protein has recently been described by Shechter et al. (2008). A 65-kDa protein, GAP-65,
was found in the gastrolith (the storage organ for calcium carbonate in the crayfish). This pro-
tein binds ACC and inhibits the formation of calcite.
Dramatic postecdysial changes in crab cuticular glycoproteins synchronous with initial min-
eralization were documented at the histochemical level (Marlowe et al. 1994), by lectin blotting
following SDS-PAGE (Shafer et al. 1994, 1995) and by their ability to affect calcite nucleation
(Coblentz et al. 1998). Based on these data, it was hypothesized that acid-soluble proteins form
nucleating sites in the cuticle and that glycoproteins active only in preecdysis and for the first
few hours postecdysis shield nucleating proteins from calcium and carbonate ions or otherwise
inhibit their action (Coblentz et al. 1998). A cuticular glycoprotein that disappears from lectin
blots postecdysis (Shafer et al. 1995) was assumed to be the inhibitor. Its purification from rela-
tively large amounts of ecdysial cuticle provided strong support for this hypothesis (Tweedie
et al. 2004). This glycoprotein is mucinlike, being 55% carbohydrate and having both N- and
O -linkages. Immunoblot analysis suggests that several changes occur in its glycosylation pat-
tern during the first few hours after ecdysis. Immunohistochemical staining decreases in the
interprismatic septa as early as 2 hours after ecdysis, coincident with the first appearance of
mineralization. This temporal and fine-scale spatial correlation between the loss of a possible
inhibitor and the initiation of calcium carbonate deposition, and the fact that the protein does
not exist in the arthrodial membrane pre- or postecdysis, strongly suggests a role in control of
nucleation.
The means by which cuticular glycoproteins can be modified in situ after the molt is still a
matter of active investigation. However, evidence suggests that N-acetylhexosaminidase treat-
ment can alter cuticular glycans and change the ability of cuticle explants to calcify in a way that
mimics in vivo postecdysis processes (Pierce et al. 2001). A glycosidase with this activity appears
in the cuticle during the early postecdysial hours coincident with the changes in glycoprotein
profiles observed in vivo (Roer et al. 2001, Roer and Towle 2004).
Cuticular matrix proteins have been sequenced from several decapod crustaceans, either
directly or by virtual translation of cDNA sequences. They include multiple sequences from
Homarus (Kragh et al. 1997, Andersen 1998, Nousiainen et al. 1998), Cancer pagurus (Andersen
1999), Marsupenaeus japonicus (Endo et al. 2000, Watanabe et al. 2000), Callinectes (Wynn and
Shafer 2005, Faircloth and Shafer 2007), and Portunus pelagicus (Kuballa et al. 2007). Functions
for these proteins are at present only matters of speculation. However, a group of proteins from
the crayfish Procambarus have been produced in recombinant systems and actually evaluated
for their ability to bind calcium carbonate. Calcification-associated peptides 1 and 2 (CAP-1 and
CAP-2), expressed in the crayfish tail fan during postecdysis, have been shown to affect in vitro
calcium carbonate formation and have been implicated as components that control the initiation
of mineralization (Inoue et al. 2001, 2003, 2004). CAP-1 can alter the structure of nanocrystals
deposited on chitin-coated surfaces (Sugawara et al. 2006). Additionally, Casp-2, a more soluble
Procambarus cuticular protein with an unrelated structure, also regulates calcium carbonate
formation when the recombinant protein is added to in vitro systems (Inoue et al. 2008).
CONCLUSION AND FUTURE DIRECTIONS
While there is considerable conservation in the basic architecture of the arthropod exoskeleton
across a wide array of taxa, there are also remarkable differences in cuticle characteristics. These
differences manifest across the crustacean taxa and even among different species of decapods.
Differences are also evident within an individual, depending upon the mechanical and physi-
ological function that the cuticle serves in different regions of the body. Cuticles in the gills of
aquatic crabs and the branchial chambers of terrestrial crabs are thin, nonmineralized, soft, and
highly permeable, while that of the cheliped is heavily mineralized, hard as concrete, and com-
pletely impermeable. Moreover, cuticles in different regions of the body of an individual crusta-
cean undergo synthesis and degradation during different times within the molt cycle, perhaps
most strikingly in the biphasic molting of isopods. These variations reflect temporal delays or
differential sensitivities of the underlying hypodermis to the hormonal cues that initiate these
events in preparation for the molt.
Clearly, the hypodermis holds the key to understanding the differences in cuticle structure,
function, and formation within the molt cycle. Recent work in our laboratory and others has
begun to elucidate the different expression of proteins and glycoproteins both spatially and tem-
porally and may explain the differences in cuticular structure and thus function. This approach
has perhaps been most successful in providing insight into the ability of cuticle to calcify (Inoue
et al. 2001, 2003, 2004, 2008, Wynn and Shafer 2005, Sugawara et al. 2006, Faircloth and Shafer
2007). The establishment and expansion of expression libraries for crustaceans hold great prom-
ise for discovering the cuticular components that are crucial for defining the differences in cuti-
cle morphology and function.
ACKNOWLEDGMENTS
We acknowledge the invaluable assistance of Mr. D. Mark Gay with the preparation of the fig-
ures. We thank the Drs. Raabe, Romano, Cribb, and Hild for supplying high-resolution images
of their figures and their publishers for permission to use them.
REFERENCES
Al-Sawalmih, A., C. Li, S. Siegel, H. Fabritius, S. Yi, D. Raabe, P. Fratzl, and O. Paris. 2008. Microtexture
and chitin/calcite orientation relationship in the mineralized exoskeleton of the American lobster.
Advanced Functional Materials 18:3307–3314.
Andersen, S.O. 1998. Characterization of proteins from arthrodial membranes of the lobster Homarus
americanus. Comparative Biochemistry and Physiology Part A 121:375–383.
Andersen, S.O. 1999. Exoskeletal proteins from the crab, Cancer pagurus. Comparative Biochemistry and
Physiology Part A 123:203–211.
Andrews, S.C., and R. M. Dillaman . 1993. Ultrastructure of the gill epithelia in the crayfish Procambarus
clarkii at different stages of the molt cycle. Journal of Crustacean Biology 13:77–86.
Becker, A., A. Ziegler, and M. Epple. 2005 . The mineral phase in the cuticles of two species of Crustacea
consists of magnesium calcite, amorphous calcium carbonate, and amorphous calcium phosphate.
Dalton Transactions 2005:1814–1820.
Boselmann, F., P. Romano, H. Fabritius, D. Raabe, and M. Epple. 2007. The composition of the exoskel-
eton of two Crustacea: The American lobster Homarus americanus and the edible crab Cancer
pagurus. Thermochimica Acta 463:65–68.
Bouligand, Y. 1970. Aspects ultrastructuraux de la calcification chez les crabes. Septieme Congres
Internationale de Microscopie Electronique (Grenoble) 3:105–106.
Bouligand, Y. 1972. Twisted fibrous arrangements in biological materials and cholesteric mesophases.
Tissue and Cell 4:189 –190, 192–217.
Chen, P.-Y., A.Y.-M. Lin, J. McKittrick , and M.A. Meyers. 2008. Structure and mechanical properties of
crab exoskeletons. Acta Biomaterialia 4:587–596.
Coblentz , F.E., T.H. Shafer, and R.D. Roer. 1998. Cuticular proteins from the blue crab alter in vitro cal-
cium carbonate mineralization. Comparative Biochemistry and Physiology Part B 121:349 –360.
Compére, P. 1995 . Fine structure and morphogenesis of the sclerite epicuticle in the Atlantic shore crab
Carcinus maenas. Tissue and Cell 27:525–538.
Compére, P., M.F. Jaspar-Versali, and G. Goffinet. 2002. Glycoproteins from the cuticle of the Atlantic
shore crab Carcinus maenas: I. Electrophoresis and Western-blot analysis by use of lectins.
Biological Bulletin 202:61–73.
Compére, P., A. Thorez , and G. Goffinet. 1998. Fine structural survey of old cuticle degradation during
pre-ecdysis in two European Atlantic crabs. Tissue and Cell 30:41–56.
Cribb, B.W., A. Rathmell, R. Charters, R. Rasch, H. Huang , and I.R. Tibbetts. 2009. Structure, composi-
tion and properties of naturally occurring non-calcified crustacean cuticle. Arthropod Structure
and Development 38:173–178.
Dickson, J.S., R.M. Dillaman, R.D. Roer, and D.B. Roye. 1991. Distribution and characterization of
ion transporting and respiratory filaments in the gills of Procambarus clarkii. Biological Bulletin
180:154–166.
Dillaman, R., S. Hequembourg , and M. Gay. 2005 . Early pattern of calcification in the dorsal carapace of
the blue crab, Callinectes sapidus. Journal of Morphology 263:356 –374.
Drach, P. 1939. Mue et cycle d’intermue chez les crustacés décapodes. Annales d’Institut Oceanographie,
Paris 19:103–391.
Drach, P., and C. Tchernigovtzeff. 1967. Sur la méthode de détermination des stades d’intermue et son
application générale aux crustaces. Vie et Milieu 18:595–610.
Elliott, E.A., and R.M. Dillaman. 1999. Formation of the inner branchiostegal cuticle of the blue crab,
Callinectes sapidus. Journal of Morphology 242:47–56.
Endo, H., P. Persson , and T. Watanabe. 2000. Molecular cloning of the crustacean DD4 cDNA
encoding a Ca 2+-binding protein. Biochemical and Biophysical Research Communications
276:286 –291.
Fabritius, H.-O., C. Sachs, P.R. Triguero, and D. Raabe. 2009. Influence of structural principles on the
mechanics of a biological fiber-based composite material with hierarchical organization: The
exoskeleton of the lobster Homarus americanus. Advanced Materials 21:391–400.
Faircloth, L.M., and T.H. Shafer. 2007. Differential expression of eight transcripts and their roles in
the cuticle of the blue crab, Callinectes sapidus. Comparative Biochemistry and Physiology Part B
146:370 –383.
Giraud, M.M. 1977. Histochemistry of 1st stages of mineralization of Carcinus maenas cuticle—attempt
of localization of carbonic anhydrase. Comptes Rendus Hebdomadaires des Seances de l’Academie
des Sciences Serie D 284:1541–1544.
Giraud, M.M. 1981. Carbonic anhydrase activity in the integument of the crab Carcinus maenas during
the intermolt cycle. Comparative Biochemistry and Physiology Part A 69:381–387.
Giraud-Guille, M.M. 1984 . Calcification initiation sites in the crab cuticle: The interprismatic septa. An
ultrastructural cytochemical study. Cell and Tissue Research 236:413–420.
Giraud-Guille, M.M., and C. Quintana. 1982. Secondary ion microanalysis of the crab calcified cuticle:
Distribution of mineral elements and interactions with the cholesteric organic matrix. Biologie
Cellulaire 44:57–67.
Greenaway, P., R.M. Dillaman, and R.D. Roer. 1995 . Quercitin-dependent ATPase activity in the
hypodermal tissue of Callinectes sapidus during the moult cycle. Comparative and Biochemical
Physiology Part A 111:303–312.
Greenaway, P., and C.A. Farrelly. 1984 . The venous system of the terrestrial crab Ocypode cordimanus
(Desmarest 1825) with particular reference to the vasculature of the lungs. Journal of Morphology
181:133–142.
Greenaway, P., and C. Farrelly. 1990. Vasculature of the gas-exchange organs in air-breathing brachy-
urans. Physiological Zoology 63:117–139.
Halcrow, K., and E.L. Bousfield. 1987. Scanning electron microscopy of surface microstructures of some
gammaridean amphipod crustaceans. Journal of Crustacean Biology 7:274–287.
Hegdahl, T., F. Gustavsen, and J. Silness. 1977. The structure and mineralization of the carapace of the
crab (Cancer pagurus L.): The exocuticle. Zoologica Scripta 6:101–105.
Hild, S., O. Marti, and A. Ziegler. 2008. Spatial distribution of calcite and amorphous calcium carbonate
in the cuticle of the terrestrial crustaceans Porcellio scaber and Armadillidium vulgare. Journal of
Structural Biology 163:100 –108.
Inoue, H., T. Ohira, N. Ozaki, and H. Nagasawa. 2003. Cloning and expression of a cDNA encoding
a matrix peptide associated with calcification in the exoskeleton of the crayfish. Comparative
Biochemistry and Physiology Part B 136:755–765.
Inoue, H., T. Ohira, N. Ozaki, and H. Nagasawa. 2004 . A novel calcium-binding peptide from the cuticle
of the crayfish, Procambarus clarkii. Biochemistry and Biophysics Research Communications
318:649 –654.
Inoue, H., N. Ozaki, and H. Nagasawa. 2001. Purification and structural determination of a phosphor-
ylated peptide with anti-calcification and chitin-binding activities in the exoskeleton of the cray-
fish, Procambarus clarkii. Bioscience Biotechnology and Biochemistry 65:1840–1848.
Inoue, H., N. Yuasa-Hashimoto, M. Suzuki, and H. Nagasawa. 2008. Structural determination and func-
tional analysis of a soluble protein associated with calcification of the exoskeleton of the crayfish,
Procambarus clarkii. Bioscience Biotechnology and Biochemistry 72:2697–2707.
Kragh, M., L. Mølbak , and S.O. Andersen. 1997. Cuticular proteins from the lobster, Homarus americanus.
Comparative Biochemistry and Physiology Part B 118:147–154.
Krywka, C., C. Sternemann, M. Paulus, N. Javid, R. Winter, A. Al-Sawalmih, S. Yi, D. Raabe, and M.
Tolan. 2007. The small-angle and wide-angle X-ray scattering set-up at beamline BL9 of DELTA.
Journal of Synchrotron Radiation 14:244–251.
Kuballa, A.V., D.J. Merritt, and A. Elizur. 2007. Gene expression profiling of cuticular proteins across the
moult cycle of the crab Portunus pelagicus. BMC Biology 5:45 .
Locke, M. 1959. The cuticular pattern in an insect, Rhodnius prolixus Stal. Journal of Experimental
Biology 36:459 –476.
Locke, M. 1960. The cuticular pattern in an insect—the intersegmental membranes. Journal of
Experimental Biology 37:398 –407.
Locke, M. 1961. Pore canals and related structures in insect cuticle. Journal of Biophysical and
Biochemical Cytology 10:589 –618.
Marlowe, R.L., R.M. Dillaman, and R.D. Roer. 1994 . Lectin binding by the crustacean cuticle: The cuti-
cle of Callinectes sapidus throughout the molt cycle, and the intermolt cuticle of Procambarus clarkii
and Ocypode quadrata. Journal of Crustacean Biology 14:231–246.
Melnick , C.A., Z. Chen, and J.J. Mecholsky. 1996. Hardness and toughness of exoskeleton material in the
stone crab, Menippe mercenaria. Journal of Materials Research 11:2903–2907.
Modla, S. 2006. The effect of fixation on the morphology of the late premolt and early postmolt cuticle of
the blue crab, Callinectes sapidus . MS thesis, University of North Carolina, Wilmington .
Montane, M.M. 1988. A study of the biphasic molt mechanism of the supralitoral isopod, Ligia exotica .
MS thesis, University of North Carolina, Wilmington .
Mykles, D.L. 1980. The mechanism of fluid absorption at ecdysis in the American lobster, Homarus
americanus. Journal of Experimental Biology 84:89 –101.
Neville, A.C. 1975 . Biology of the arthropod cuticle. Springer, New York.
Nousiainen, M., K. Rafn, L. Skou, P. Roepstorff, and S.O. Andersen. 1998. Characterization of exoskel-
etal proteins from the American lobster, Homarus americanus. Comparative Biochemistry and
Physiology Part B 119:189 –199.
Pierce, D.C., K.D. Butler, and R.D. Roer. 2001. Effects of exogenous N-acetylhexosaminidase on the
structure and mineralization of the post-ecdysial exoskeleton of the blue crab, Callinectes sapidus.
Pratoomchat, B., P. Sawangwong , R. Guedes, M. de Lurdes Reis, and J. Machado. 2002. Cuticle
ultrastructure changes in the crab Scylla serrata over the molt cycle. Journal of Experimental
Zoology 293:414–426.
Priester, C., R.M. Dillaman, and D.M. Gay. 2005 . Ultrastructure, histochemistry, and mineralization
patterns in the ecdysial suture of the blue crab, Callinectes sapidus. Microscopy and Microanalysis
11:479 –499.
Raabe, D., A. Al-Sawalmih, S.-B. Yi, and H. Fabritius. 2007. Preferred crystallographic texture of а-chitin
as a microscopic and macroscopic design principle of the exoskeleton of the lobster Homarus ameri-
canus. Acta Biomaterialia 3:882–895.
Raabe, D., P. Romano, C. Sachs, A. Al-Sawalmih, H.-G. Brokmeier, S.-B. Yi, G. Servos, and H.G.
Hartwig. 2005a . Discovery of a honeycomb structure in the twisted plywood patterns of fibrous
biological nanocomposite tissue. Journal of Crystal Growth 283:1–7.
Raabe, D., P. Romano, C. Sachs, H. Fabritius, A. Al-Sawalmih, S.-B. Yi, G. Servos, and H.G. Hartwig.
2006. Microstructure and crystallographic texture of the chitin-protein network in the biological
composite material of the exoskeleton of the lobster Homarus americanus. Materials Science and
Engineering A 421:143–153.
Raabe, D., C. Sachs, and P. Romano. 2005b. The crustacean exoskeleton as an example of a structurally
and mechanically graded biological nanocomposite material. Acta Materialia 53:4281–4292.
Read, A.T., and D.D. Williams. 1991. The distribution, external morphology and presumptive function of
the surface microstructures of Gammarus pseudolimnaeus (Crustacea: Amphipoda) with emphasis
on the calceolus. Canadian Journal of Zoology 69:853–865.
Roer, R.D. 1980. Mechanisms of resorption and deposition of calcium in the carapace of the crab,
Carcinus maenas. Journal of Experimental Biology 88:205–218.
Roer, R.D., S.K. Burgess , C.G. Miller, and M.B. Dail. 1988. Control of calcium carbonate nucleation in
pre- and postecdysial crab cuticle. Pages 21–24 in C.S. Sikes and A.P. Wheeler, editors. Chemical
aspects of regulation of mineralization. University of South Alabama Publication Service, Mobile.
Roer, R.D., and R.M. Dillaman. 1984 . The structure and calcification of the crustacean cuticle. American
Zoologist 24:893–909.
Roer, R.D., and R.M. Dillaman. 1993. Molt-related change in integumental structure and function.
Pages 1–37 in M. Horst and J.A. Freeman, editors. The crustacean integument—morphology and
biochemistry. CRC Press, Boca Raton, FL.
Roer, R.D., K.E. Halbrook , and T.H. Shafer. 2001. Glycosidase activity in the post-ecdysial cuticle of the
blue crab, Callinectes sapidus. Comparative Biochemistry and Physiology Part B 128:683–690.
Roer, R.D., and D.W. Towle. 2004 . Partial nucleotide sequence of a putative cuticular hexosaminidase
from the blue crab, Callinectes sapidus. Bulletin of the Mount Desert Island Biological Laboratory
43:40–42.
Roer, R.D., and D.W. Towle, 2005 . Partial nucleotide sequence and expression of plasma membrane
Ca-ATPase in the hypodermis of the blue crab, Callinectes sapidus. Bulletin of the Mount Desert
Island Biological Laboratory 44:40 –42.
Romano, P., H. Fabritius, and D. Raabe. 2007. The exoskeleton of the lobster Homarus americanus as an
example of a smart anisotropic biological material. Acta Biomaterialia 3:301–309.
Sachs, C., H. Fabritius, and D. Raabe. 2006. Hardness and elastic properties of dehydrated cuticle from
the lobster Homarus americanus obtained by nanoindentation. Journal of Materials Research
21:1987–1995.
Sakamoto, K., W. Honto, M. Iguchi, N. Ogawa, K. Ura, and Y. Takagi. 2009. Post-molt processes of
cuticle formation and calcification in the Japanese mitten crab Eriocheir japonicus. Fisheries Science
75:91–98.
Shafer, T.H., R.D. Roer, C. Midgette-Luther, and T.A. Brookins. 1995 . Postecdysial cuticle alteration in
the blue crab, Callinectes sapidus: Synchronous changes in glycoproteins and mineral nucleation.
Journal of Experimental Zoology 271:171–182.
Shafer, T.H., R.D. Roer, C.G. Miller, and R.M. Dillaman. 1994 . Postecdysial changes in the protein and
glycoprotein composition of the cuticle of the blue crab Callinectes sapidus. Journal of Crustacean
Biology 14:210 –219.
Shechter, A., L. Glazer, S. Cheled, E. Mor, S. Weil, A. Berman, S. Bentov, E.D. Aflalo, I. Khalaila, and A.
Sagi. 2008. A gastrolith protein serving a dual role in the formation of an amorphous mineral con-
taining extracellular matrix. Proceedings of the National Academy of Science USA 105:7129 –7134.
Skinner, D.M. 1962. The structure and metabolism of a crustacean integumentary tissue during a molt
cycle. Biological Bulletin 123:635–647.
Skinner, D.M. 1965 . Amino acid incorporation into protein during the molt cycle of the land crab,
Gecarcinus lateralis. Journal of Experimental Zoology 160:225–233.
Skinner, D.M., S.S. Kumari, and J.J. O’Brien . 1992. Proteins of the crustacean exoskeleton. American
Zoologist 32:470–484.
Soejoko, D.S., and M.O. Tjia. 2003. Infrared spectroscopy and X ray diffraction study on the morphologi-
cal variations of carbonate and phosphate compounds in giant prawn (Macrobrachium rosenbergii)
skeletons during its moulting period. Journal of Materials Science 38:2087–2093.
Steel, C.G.H. 1980. Mechanisms of coordination between moulting and reproduction in terrestrial iso-
pod Crustacea. Biological Bulletin 159:206 –218.
Steel, C.G.H. 1982. Stages of the intermoult cycle in the terrestrial isopod Oniscus asellus and their rela-
tion to biphasic cuticle secretion. Canadian Journal of Zoology 60:429 –437.
Sugawara, A., T. Nishimura, Y. Yamamoto, H. Inoue, H. Nagasawa, and T. Kato. 2006. Self-organization
of oriented calcium carbonate/polymer composites: Effects of a matrix peptide isolated from the
exoskeleton of a crayfish. Angewandte Chemie International Edition 45:2876 –2879.
Tarsitano, S.F., K.L. Lavalli, F. Horne, and E. Spanier. 2006. The constructional properties of the exoskel-
eton of homarid, palinurid, and scyllarid lobsters. Hydrobiologia 557:9 –20.
Taylor, H.H., and P. Greenaway. 1984 . The role of the gills and branchiostegites in gas exchange in a
bimodally breathing crab, Hothuisana transversa: Evidence for a facultative change in the distribu-
tion of the respiratory circulation. Journal of Experimental Biology 111:103–121.
Taylor, J.R.A., J. Hebrank , and W.M. Kier. 2007. Mechanical properties of the rigid and hydrostatic
skeletons of molting blue crabs, Callinectes sapidus Rathbun. Journal of Experimental Biology
210:4272–4278.
Taylor, J.R.A., and W.M. Kier. 2003. Switching skeletons: Hydrostatic support in molting crabs. Science
301:209 –210.
Travis, D.F. 1955 . The molting cycle of the spiny lobster, Panulirus argus Latreille. II. Pre-ecdysial his-
tological and histochemical changes in the hepatopancreas and integumental tissues. Biological
Bulletin 108:88 –112.
Travis, D.F. 1957. The molting cycle of the spiny lobster, Panulirus argus Latreille. IV. Post-ecdysial
histological and histochemical changes in the hepatopancreas and integumental tissues. Biological
Bulletin 113:451–479.
Travis, D.F. 1963. Structural features of mineralization from tissue to macromolecular levels of organiza-
tion in the decapod Crustacea. Annals of the New York Academy of Science 109:177–245.
Travis, D.F. 1965 . The deposition of skeletal structures in the Crustacea. 5. The histomorphological and
histochemical changes associated with the development and calcification of the branchial exoskel-
eton in the crayfish, Orconectes virilis Hagen. Acta Histochemica 20:193–222.
Tweedie, E.P., F.E. Coblentz , and T.H. Shafer. 2004 . Purification of a soluble glycoprotein from the
uncalcified ecdysial cuticle of the blue crab Callinectes sapidus and its possible role in initial miner-
alization. Journal of Experimental Biology 207:2589 –2598.
Watanabe, T., P. Persson, H. Endo, and M. Kono. 2000. Molecular analysis of two genes, DD9A and
B, which are expressed during the post molt stage in the decapod crustacean Penaeus japonicus.
Wigglesworth, V.B. 1933. The physiology of the cuticle and ecdysis in Rhodnius prolixus (Triatomidae,
Hemiptara); with special reference to the function of the oenocytes and of the dermal glands.
Quarterly Journal of Microscopical Science 76:269 –318.
Wilcockson, D.C., and S.G. Webster. 2008. Identification and developmental expression of mRNAs
encoding putative insect cuticle hardening hormone, bursicon in the green shore crab Carcinus mae-
nas. General and Comparative Endocrinology 156:113–125.
Williams, C.L., R.M. Dillaman, E.A. Elliott, and D.M. Gay. 2003. Formation of the arthrodial membrane
in the blue crab, Callinectes sapidus. Journal of Morphology 256:260–269.
Williams, D.L., S. Modla , R.D. Roer, and R.M. Dillaman. 2009. Post-ecdysial change in the
permeability of the exoskeleton of the blue crab, Callinectes sapidus. Journal of Crustacean
Biology 29:550–555.
Wynn, A., and T.H. Shafer. 2005 . Four differentially expressed cDNAs in Callinectes sapidus contain-
ing the Rebers-Riddiford consensus sequence. Comparative Biochemistry and Physiology Part B
141:294–306.
Ziegler, A., H. Fabritius, and M. Hagedorn. 2005 . Microscopical and functional aspects of
calcium-transport and deposition in terrestrial isopods. Micron 36:137–153.
Ziegler, A., M. Hagedorn, G.A. Ahearn, and T.H. Carefoot. 2007. Calcium translocations during the
moulting cycle of the semiterrestrial isopod Ligia hawaiiensis (Oniscidea, Crustacea). Journal of
Comparative Physiology B 177:99 –108.
6
THE CRUSTACEAN INTEGUMENT: SETAE,
SETULES, AND OTHER ORNAMENTATION
Anders Garm and Les Watling
Abstract
The cuticle plays an important role in many aspects of crustacean biology, since it is the interface to
the surrounding world. Thus, the cuticle displays many structural specializations all over the body.
The structures considered here are setae, setules, denticles, and spines. We provide definitions for
them and discuss their functional morphology and development, with the main focus on setae.
We recognize seven types of setae based on their detailed external morphology: plumose, pap-
pose, composite, serrate, papposerrate, simple, and cuspidate. In support of the categorization of
these setae, each seems to correlate with a specific functional outcome such as feeding, grooming,
and locomotion. Setae are also important sensory organs, and in crustaceans they are normally
bimodal chemo- and mechanoreceptors, but there are also indications of thermo-, osmo-, and
hygrosensitivity. Little can be learned about the sensory functions from the external morphology
of setae, but their ultrastructure seems to provide better cues. In particular, mechanoreceptors
display structures related to transduction mechanisms, with the scolopale as a good example. Still,
too few data are available outside malacostracans to draw general conclusions for all crustaceans,
underlining the need for multidisciplinary and broad intertaxon studies. Less is known about the
functional morphology and development of setules and denticles in the general cuticle, but they
seem to be homologous with similar structures on the setae. Arthropods outside Crustacea also
have setae in their cuticle, and many shared features can be found. They are especially well studied
in insects, where many correlations between structure and function have been shown.
INTRODUCTION TO THE STRUCTURES OF THE CRUSTACEAN CUTICLE:

DEFINITIONS/CLASSIFICATION
One of the defining characters of crustaceans as well as other arthropods is their external skel-
eton, the cuticle (see also chapter 5). The cuticle plays a major role in most aspects of crustacean
167
© 2013 Oxford University Press. Published 2013 by Oxford University Press.
biology, and this has led to a vast number of structural and functional specializations. Many
of these specializations lie within the detailed surface structures, and they are the topic of this
chapter. First, we provide an overview of the diversity of these structures and their functions
and use this to suggest a classification system. The main part of the review then focuses in detail
on the major group of cuticular specializations, the setae, since they are by far the most studied
and have the greatest functional diversity and importance. We end by comparing with data from
other arthropod groups and listing suggestions for where future research in this field is most
needed and will be most fruitful.
When observing crustaceans with the naked eye, many of the cuticular specializations are
visible in a large number of species (Fig. 6.1A). Some body parts and especially the appendages
appear furry (Fig. 6.1B), and the hairlike structures found in these areas are outgrowths of the
general cuticle, normally with a distinct articulation at the base, making them flexible (Figs.
6.1D, 6.2). There is a general consensus that these structures are homologous within Crustacea
and are also probably homologous with similar structures in other arthropods. Many terms have
been used for these structures, such as setae, sensilla, bristles, or even “hairs.” For crustaceans,
the most often used term is setae, and it will therefore be used here. Even though setae are in
general considered homologous, it is difficult to decide which cuticular projections to include
in this term. A number of authors have addressed this problem and provided definitions of what
they considered setae. Thomas (1970) was one of the first to do so, and he proposed that all
elongate outgrowths with distal pores were setae. His work was based on light microscopy, and
electron microscopy work has since shown his definition to be far too narrow. Fish (1972) con-
sidered elongate outgrowths filled with “cytoplasm” as setae, but this very broad definition will
include many other structures, such as spines (see below), and exclude setae with no cells in the
lumen. Some authors have used the size of the cuticular structures as a basis for classification.
This has led to such terms as microsetae (Jacques 1989) and microtrichs (Cuadras 1982, Steele
and Steele 1997, 1999), but we do not approve of this approach. If a structure complies with our
given definition (see below), we will consider it a seta no matter the size, and we see no reason to
believe that they cannot be small. In fact, we believe that in small crustaceans, such as nauplius
larvae, there has been strong selection pressure for miniaturizing the setae.
An evolutionary perspective was taken by Watling (1989), who stressed the need for a defini-
tion based on homologies. He suggested that the articulation with the general cuticle is such a
homology and used this structure to define setae from other cuticular outgrowths. This defini-
tion has been widely accepted as it seems to hold true for the vast majority of setae, and the “stem
seta” probably also had such an articulation. When considering the diversity of present-day
crustaceans, though, Watling’s definition runs into some problems, which were first addressed
in an earlier review (Garm 2004b).
Some of the articulated outgrowths have an external and internal morphology so similar to
long setules found on some of the setae that there are no structural arguments to consider them
as being different. They are commonly found on the mouthparts of decapods and peracarids
(Fig. 6.1C), and we suggest that they should be included in the term setules (see below). The
other problem concerns a loss of the articulation between the setae and the general cuticle.
This has probably happened a number of times in several crustacean lineages to encompass
mechanical functions requiring a very sturdy seta (Garm and Høeg 2001, Garm 2004a). Clear
examples of such loss are seen for the spinelike projection found on the basis of maxilla 1 of the
squat lobster Munida sarsi (Fig. 6.2B). These unarticulated projections are innervated, have a
continuous lumen, and have a cellular arrangement very similar to other setae. Further, struc-
tures undoubtedly homologous with the spinelike projections (they are situated in the same
place and arranged in the same two parallel rows in other decapod species) are typical setae
with clear articulation (Garm 2004b). The same situation is seen for unarticulated spinelike
Setae, Setules, and Other Ornamentation 169
A B
C D
E F G
Fig. 6.1.
Structures in the crustacean cuticle. (A) At the macroscopic level, many crustaceans, such as the hermit
crab Parapagurus sulcata, appear furry because of very heavy setation (picture courtesy of Dr. Jens T.
Høeg). (B) Maxilliped 1 of the hermit crab Pagurus bernhardus displaying heavy setation, especially on the
medial edges of the coxa and basis. Several types of setae are present. (C) Setules from paragnath of P. bern-
hardus are clearly articulated with the general cuticle (inset). (D) Between the setae (S) on the mouthpart
of Panulirus argus, the cuticle is filled with teethlike structures (denticles). (E) Ultrastructure of setules
from the paragnath of Penaeus monodon shows that they are made entirely of cuticle and lack a lumen and
innervation. (F) Ultrastructure of setae show a round, hollow base filled with sheath cells (ShC). Cu, setal
cuticle. (G) Close-up of the central part of the setal lumen showing that the semicircular sheath cells (ShC)
encircle the outer dendritic segments (ODS) of a number of sensory cells.
Fig. 6.2.
Details of the external morphology of setae. (A) Spinelike setae from maxilla 1 of Munida sarsi, with no
apparent articulation at the base (arrows). (B) Plumose setae displaying a supracuticular articulation
(arrows) with the general cuticle, making them very flexible. (C) Most setae have an infracuticular articu-
lation (arrows) with the general cuticle, reducing their flexibility. (D) Setules from a composite seta show-
ing an articulation (arrows) with the setal shaft. (E) Some setae display unarticulated teethlike structures
arranged parallel to the setal shaft. These denticles (De) are found in two rows on the distal half of the
setae often together with small setules (S). (F) On some setae, there is a graduated transformation between
setules (S) and denticles (De). (G) Many setae display a terminal pore (TP) at the tip, often associated with
small scalelike setules. (H) The tip of a seta used for grooming the gills. Such setae often have a specialized
tip. (I) A newly molted composite seta displaying a very distinct annulus (ringed) as a by-product from the
invagination during development.
setae on the dactylus of maxilliped 3 of the shrimp Palaemon adspersus. The definition we will
follow here was put forward by Garm (2004b, 1): “A seta is an elongate projection with a more
or less circular base and a continuous lumen. The lumen has a semicircular arrangement of
sheath cells basally.”
The available data on the ultrastructure of setae provide good support for the internal charac-
teristics—the continuous lumen and the semicircular sheath cells (Fig. 6.1F,G), also called envel-
oping cells (Alexander et al. 1980, Hallberg et al. 1992, Crouau 1997, Paffenhöfer and Loyd 2000).
That the sheath cells seem to be a unifying character for setae indicates that they play important
functional roles. They are involved in setal development, and this complex process could possibly
provide a more detailed definition. The continuous lumen is also functionally significant since it is
closely connected with the sensory properties of setae. Both of these topics are discussed in detail
in later sections.
It is often problematic to use internal characters because categorization is normally based
on light or scanning electron microscopy. The round shape of the basal part of a seta is there-
fore an important character, and it seems to be very consistent for setae found on all body parts
of many groups of crustaceans (see Garm 2004b for review). Still, using this character alone
will not suffice since it will not separate unarticulated setae and spines dealt with below.
Besides setae, there are other surface structures of the cuticle that we will briefly consider.
One group has already been mentioned—the setules. As said above, this is a term widely used
for certain outgrowths on setae, but we believe them to be a general feature of the cuticle. They
are elongate structures, 10–150 μm long, often inserted into the cuticle in a socket, making
them flexible (Fig. 6.1C). They are flattened in cross section and made entirely of cuticle, so
they are never innervated and do not contain semicircular sheath cells basally (Fig. 6.1E). Most
often they have a serrated edge distally. Such setules are commonly found in the general cuticle
throughout the Crustacea, especially on the mouth apparatus and in the foregut, but they have
typically been referred to as setae (Halcrow and Bousfield 1987, Holmquist 1989, Martin 1989,
Olesen 2001).
Another expression often used when describing the cuticle of crustacean is denticles. Like set-
ules, denticles are commonly found on setae but also in the general cuticle. This again stresses that
some of the structures generally considered special features of setae are in fact general cuticular
characteristics. Denticles are relatively small structures (normally < 30 μm long) and, as the name
implies, more or less tooth shaped (Fig. 6.1D). They are unarticulated, made entirely of cuticle,
and never innervated. There is some evidence that they are in fact evolutionarily related to setules
(Garm 2004b).
A common cuticular outgrowth is the spine. This term should be used with care since it
can be very hard to tell a true spine from an unarticulated seta. We consider a spine to be an
unarticulated extension of the general cuticle. It is hollow, and the lumen is lined with normal
epithelial cells; no innervation is present unless the spine carries setae (see, e.g., Martin and
Cash-Clark 1995, their fig. 19A,C). If ultrastructural data are not available, then comparison with
closely related species should be used to verify that they do not have setae in the same position.
While the other types of structures are probably homologies, we find it very likely that spines
have arisen several times and represent convergent evolution.
Scales, like spines, are cuticular outgrowths, but they are generally wider than long and are
not usually hollow (Klepal and Kastner 1980). Most often, scales follow one side of the outline
of the polygons often visible on crustacean cuticles when observed with the scanning electron
microscope.
While it was long known that the crustacean cuticle was often sculptured, the exact
details could not be seen until the invention of the scanning electron microscope. Some of
the main features are summarized by Meyer-Rochow (1980), Holdich (1984), and Halcrow
and Bousfield (1987). A terminology of surface sculpturing was proposed by Harris (1979)
for insects, but it seems equally applicable to crustaceans. The basic unit of sculpturing
seems to be a more or less well-defined polygon, which Hinton (1970) and Duncan (1985)
assert represents the surface mani festation of underlying epidermal cells (see also chap-
ter 5). Scales, microspines, micropores, and a large variety of other structures can be found
within and along the boundaries of polygons (e.g., Klepal and Kastner 1980, Halcrow and
Bousfield 1987). In many other crustaceans and insects, however, the polygon is obliter-
ated by cuticular secretions that form more elaborate sculpture (e.g., Hinton 1970, Meyer-
Rochow 1980).
THE EXTERNAL STRUCTURE OF SETAE
As discussed in the preceding section, setae constitute the largest and most diverse group of
structures, which is also why providing a general definition is not a trivial task. This diversity
is seen between species, but sometimes a single species carries close to the full diversity of seta
types. Most of the setae are found on the appendages, and especially the mouthparts are heav-
ily ornamented with setae, and a single segment (= article) of, for example, a maxilliped can
display quite a number of setal types (Fig. 6.1B). In the following we will try to deconstruct this
diversity and pinpoint some of the important structures that cause the diversity. Structures that
share some kind of similarities can be a product of the evolutionary history of setae and thereby
be considered homologies, and/or they can be products of shared functionality. As we discuss
further below, most of the similarities of setae stem from shared functions, and this will be used
to suggest a classification system.
First, it is important to recognize that all setae can be seen as having a more or less elongate
and round (at least at the base) central part, the shaft, which may or may not have specializations,
including different types of outgrowths. The length of the shaft varies from just a few microm-
eters to several millimeters in large decapods. They are found on all body parts, including inter-
nally in the foregut (Altner et al. 1986, Johnston 1999), and serve many different functions. This
diversity of function has undoubtedly added to the wide range of external morphology. Some
setae are long and slender with no apparent specializations along the setal shaft (Fig. 6.2F,G),
whereas others have many types of outgrowths, resembling feathers or pine trees (Fig. 6.2A,B).
Still others are thorn shaped or bent and appear as hooks. Despite the diversity, several substruc-
tures can be recognized in many setae and can be used to group the setae into different types. If
a classification includes too many details, there is a high risk that the designated setal types will
be highly specialized and appear only in a very limited number of taxa. Here, we try to avoid this
problem and consider only overall structural similarities found in most major crustacean taxa,
since this will have the broadest application and interest.
One of the prominent substructures concerns how the setae attach to the general cuticle.
Three types of attachments are seen: (1) an articulation in the form of a socket, which is drawn
into the general cuticle and gives the seta an infracuticular articulation (Fig. 6.3C)—this is by
far the most common type of attachment; (2) the socket is extended from the general cuticle,
giving the seta a supracuticular articulation (Fig. 6.3B)—this gives the seta great flexibility and
is often seen in setae experiencing large drag forces; (3) no articulation is seen, and the general
cuticle has a direct transition into the cuticle of the seta (Fig. 6.3A)—as mentioned earlier, the
articulation is probably reduced to obtain sturdiness.
Another feature concerning the sturdiness is the length:width (L:W) ratio of the shaft, where
the width is measured at the base of the seta. The vast majority of setae are slim, with a L:W ratio
of >15 (Fig. 6.2), but some setae are more stout and robust, with a L:W ratio <8 (Fig. 6.2G). Surely
there are setae with intermediate L:W ratios, but they seem to be rare.
Fig. 6.3.
Setal types. (A) Pappose setae, with long setules scattered along the entire shaft, from the mandibular
palp of Cherax quadrocarinatus. (B) Plumose setae, with two straight rows of long setules, from maxil-
liped 1 of Munida sarsi. (C) Composite setae, with small setules distally, from maxilliped 1 of Panulirus
argus. (D) Serrate setae, with two very distinct row of denticles, from maxilla 1 of C. quadrocarinatus. (E)
Papposerrate setae, with denticles and small setules distally and long setules proximally, from maxilla 2
of M. sarsi. (F) Simple setae, with an almost complete lack of surface structures, from maxilliped 1 of P.
argus. (G) Cuspidate setae, from maxilliped 2 of P. argus. Some cuspidate setae can have small setules on
the middle part.
An annulus situated on the proximal half of the shaft is found on most if not all setae (Fig. 6.3I)
(Garm 2004b). The annulus seems to have no function as such but is a by-product of the onto-
geny, when the setae develop in an invaginated state (for more details, see “Setal Development
and Ontogeny,” below). The annulus is most easily detected in newly molted animals since it
often diminishes as the cuticle thickens, stretches, and wears down during the intermolt stage
(Garm 2004b).
The tip of the seta also varies (Fig. 6.3F–H) but is always more or less pointed. In cases of
a seta with outgrowths, the latter often form the very tip. A specialization of the tip is seen in
peracarids, where some setae have a bifurcate tip (Fish 1972, Brandt 1988). Interestingly, the
thin “additional” tip holds all the sensory cells (Brandt 1988), and it might be a way of sepa-
rating mechanical and sensory functions. Another functionally interesting feature of the tip
is the presence or absence of a pore. The pore-bearing setae may have the pore in one of two
different positions: terminal or subterminal. Most common is a terminal pore situated at the
very tip of the seta, often bending to make the pore point to the side of the seta (Fig. 6.3G).
Less common is a subterminal pore situated on the side of the seta a little proximal to the
tip. In at least some cases, the pore is associated with chemoreception (see later section for
detailed discussion).
The main substructures causing the diversity of setae are the presence or absence of out-
growths on the setal shaft and, when present, their detailed structure and arrangement. We
divide the outgrowths into two types: denticles and setules. Denticles as defined above are
rather small (normally <30 μm long), flat, and pointed outgrowths with smooth edges and no
articulation with the setal shaft. They are solid cuticle; that is, they lack a lumen. On the setae
they occur in two parallel rows, are always oriented with their broad axis parallel to the setal
shaft, and point distally (Fig. 6.3E). Denticles arranged in this way are found distal to the
annulus.
Setules have a wide size range (2–150 μm long), but they share common features. They all
have an articulation with the setal shaft, although, especially in smaller setules, the articulation
is often weak. They are all flattened, with their broad axis perpendicular to the setal shaft at the
point of attachment. Setules taper distally and often have a serrate edge, with most of the minute
tooth-shaped extensions distally (Fig. 6.3D). Like denticles, setules are made of solid cuticle.
Setules always point toward the tip of the seta, but the angle changes with size. Long setules may
be almost perpendicular with the setal shaft, whereas small setules often lie almost flat against
the shaft (often referred to as scales). Long setules can be found along the whole length of a seta,
whereas small setules are normally found only distal to the annulus. They can form straight rows,
but most often they appear to be randomly arranged on the shaft. Even though denticles and set-
ules are normally very distinct and easy to separate, there are intermediate forms. In some cases,
rows of outgrowths gradually changing from setules to denticles (from base to tip) can be found
on the same seta (Fig. 6.3F).
TOWARD A GENERAL CLASSIF ICATION SYSTEM OF CRUSTACEAN SETAE
Setae are very diverse both in function and in morphology, thus necessitating a general clas-
sification system that will enable carcinologists to compare results obtained from a broad range
of taxa within Crustacea and possibly also with other arthropods. Many studies have provided
a setal classification system, but unfortunately, they are often based on a single or a few closely
related species and make use of a large number of structural details (e.g., Garm and Høeg 2000,
Coelho and Rodrigues 2001). While that approach provides good insight into the setal diversity
of the species studied, it has little or no value when setae in general are considered. Here we
try to set the basis for a more general classification system that can be used for most (if not all)
crustacean taxa.
We suggest that the vast majority of crustacean setae can be subdivided into seven catego-
ries or types based on the external morphological characters listed earlier and, to some extent,
their mechanical functions: plumose, pappose, composite, serrate, papposerrate, simple, and
cuspidate (see also Table 6.1). Note that the term serrulate used in earlier work (Watling 1989,
Table 6.1. Summary of the characteristics of the seven types of setae.
Seta type Annulus Articulation Long Short Denticles Length: Pore

setules setules width ratio
Pappose + Infra + +/– – >15 –
Plumose + Supra + – – >15 –
Composite + Infra – + – >15 Ter/–
Serrate + Infra – +/– + >15 Ter/
Sub/–
Papposerrate + Infra + +/– + >15 Ter/–
Simple + Infra – – – >15 Ter/–
Cuspidate + Infra/absent – +/– – <8 Sub/–
Abbreviations: Infra, infracuticular articulation; Supra, supracuticular articulation; Ter, terminal; Sub, subterminal; +,
present; –, absent.
Garm 2004b) has been changed to composite. The reason is that serrulate, meaning “small ser-
rate,” indicates the presence of denticles, which is never the case in these setae and why we
found it inappropriate. The reason for excluding the internal structures and thereby almost
all aspects of their sensory functions from this morphological description are that (1) we find
it unrealistic to expect that investigators in general can include these data since the quality of
the material (e.g., ethanol-fixed museum specimens) and time often do not allow this, and (2)
at present there are too few ultrastructural data at hand outside decapods to draw trustworthy
general conclusions on the functional morphology and/or evolutionary history of the internal
structures. However, internal structure is very important for inferring function, as we illus-
trate below.
The morphological characters used to group the setae are not put forward as suggestions of
homologies, even though some of them might be, and thus, the seven types of setae are not to
be considered as separate evolutionary lines. It is in fact very likely that some of the types (e.g.,
the simple setae) are based on shared morphological characters that are convergently derived.
There is little doubt that strong selection pressures have acted on the external morphology of
setae, which comes from the many mechanical functions they serve. The outgrowths of setae
directly involved in food handling, for example, should be closely correlated with the nature of
the food items. Such a situation is bound to result in convergences, and this may to a large extent
impede a homology-based classification system.
Pappose setae. The shaft of pappose setae is long and slender, and they never display a pore.
They have long (50–150 μm) setules with clear articulations scattered randomly along the
entire length of the shaft (Fig. 6.2A). The setules have a serrated edge, with most teeth situated
distally, and they normally project with an angle between 45° and 90° to the setal shaft. The
socket of pappose setae is infracuticular.
Plumose setae. Like pappose setae, plumose setae have long setules along the entire shaft,
but they are arranged in two strict rows on opposite sides of the shaft, giving them a feather-
like appearance (Fig. 6.2B). The setules are never serrated, have a weak articulation with the
setal shaft, and are often situated in a groove. Plumose setae are the only setae that may have a
supracuticular articulation, and they never display a pore.
Composite setae. Composite setae are slim, with a naked proximal part, but have small setules
(<15 μm long) distal to the annulus (Fig. 6.2C). The setules can be arranged in rows or occur
randomly along the shaft. The setules are usually smaller in size toward the tip and, for the most
part, point toward the tip of the seta with an angle of <45°. The setules on composite setae can
be leaf shaped, digitate, or palmate. Composite setae may or may not have a terminal pore, and
the socket has an infracuticular articulation.
Serrate setae. Serrate setae have a naked proximal half, but distal to the annulus they have two
rows of denticles pointing toward the setal tip, with 120–180° between them (Fig. 6.2D). The dis-
tal half may also have setules on the opposite side of the shaft from the denticles. When present,
the setules are small, have teeth along their edge, and lay almost flat against the shaft. Serrate
setae can have a terminal or a subterminal pore, and the articulation with the general cuticle is
infracuticular and often narrow.
Papposerrate setae. Like pappose and plumose setae, papposerrate setae are long and slender
(Fig. 6.2E). On their proximal half to two-thirds (proximal to the annulus), they have long, ran-
domly arranged setules like pappose setae, but on the distal part they have two rows of denticles
like serrate setae. In the area with the denticles, there may be additional small setules on the
opposite side of the denticles. The articulation of papposerrate setae with the general cuticle is
infracuticular and normally broad.
Simple setae. Simple setae are long and slender, and as the name implies, they completely
lack outgrowths on the setal shaft (Fig. 6.2F). They have an annulus typically one-third of the
way up the shaft and a pointed tip, which may or may not have a terminal pore. They have an
infracuticular articulation.
Cuspidate setae. Cuspidate setae are very robust, with a L:W ratio <8 when width is meas-
ured at the base of the seta (Fig. 6.2G). They have a broad base and taper gradually toward the
somewhat rounded tip. They may or may not have a subterminal pore, and in most cases they
have no outgrowths. They can have small setules in the midregion, often combined with a
weak curvature of the setal shaft with the outgrowths on the concave side. The distal part is
almost always naked but may be microtuberculate. In most cases they have an infracuticular
articulation with a very reduced membranous area, but sometimes the articulation is lacking
completely.
In our opinion, the vast majority of crustacean setae are easily put in one of the seven
described categories, but there is morphological variation within the groups, and this some-
times results in intermediate types of setae being described. Intermediate forms are occasion-
ally found between the following types. (1) Pappose and plumose, where the proximal part has
two distinct rows of setules, but on the distal part they are randomly spaced. (2) Pappose and
papposerrate, where the proximal part has long, randomly arranged setules, but the distal part
has short setules arranged in rows. (3) Pappose and composite, where the proximal part has a
few long setules, and the distal part has small or medium sized setules. (4) Composite and ser-
rate, where the proximalmost outgrowths are setules, but they change gradually into denticles.
(5) Composite and simple, where the seta has a few small setules on the distal part. (6) Serrate
and cuspidate, where the outgrowths are denticle-like, but the distal part is naked, and the seta
has a L:W ratio between 10 and 15. (7) Cuspidate and simple, where the seta has no outgrowths
and a L:W ratio between 8 and 15.
It should again be noted that by far the most available data stem from malacostracans, espe-
cially decapods and peracarids. This can, of course, turn out to be fatal for the suggested clas-
sification system, but when going through the descriptions of nonmalacostracan crustaceans, it
seems that it will apply to those groups also (see Garm 2004b for more details). The problem is
that none of the papers directly deal with setae, and therefore the pictures they present often do
not show the needed details. Further, since the authors did not make a survey of the seta, there
may be many other setae that are not shown. Hence, we might be able to say something about
which of these seven types are present but very little about whether additional types should be
named.
SETAL DEVELOPMENT AND ONTOGENY
The development of setae can be separated in two different events: (1) the development of a
new seta, and (2) the reconstruction of a seta during a molt. The first case is the more com-
plex and unfortunately only rarely studied. What little is known about formation of new setae
stems almost entirely from malacostracan olfactory setae, called aesthetascs. In decapods, the
aesthetascs are situated in discrete rows on the lateral flagellum of antenna 1. The flagellum
is annulated, and each annulus has one or more rows of setae. With each molt, the distalmost
annuli with their aesthetasc are shed, and new annuli with aesthetascs are added proximally on
the flagellum (Derby et al. 2002, Ekerholm and Hallberg 2002). In the spiny lobster Panulirus
argus, in antenna 1 a cell proliferation zone is found in the proximal part corresponding to the
area where the new aesthetascs will be situated (Steullet et al. 2000a, Derby et al. 2002). Here
new olfactory receptor neurons (ORNs) are formed continuously but with peaks in the prolifer-
ation rate occurring in the premolt state. The ORNs form in discrete clusters of about 300 cells
that will innervate a single aesthetasc (see further below for more details). In these studies, little
attention has been paid to the development of the rest of the seta, however. Earlier studies on
the development of the aesthetascs in peracarids included observations on the role of the sheath
cells and cuticle formation (Guse 1983). Here it was also shown that already in the intermolt
stage the new ORNs are formed and that the sheath cells are also present to encircle them in a
cavity filled with receptor lymph. The number of sheath cells seems to vary, depending on the
size of the seta. Large and thick decapod setae can have as many as 50 sheath cells (Fig. 6.1F,G).
In the small setae of the isopod Idotea baltica, eight sheath cells were most commonly found
(Guse 1983). During the premolt, the sheath cells protect the ORNs against the enzymes in the
exuvial fluid and start making the cuticle of the future seta. This process happens in an invagi-
nation of the epithelium, and the proximal part of the setal shaft is therefore also invaginated
(Fig. 6.4A). The sheath cells seem to work in pairs, and in the isopod aesthetascs, the two inner-
most ones form the distal part of the setal shaft (Guse 1983). The next two pairs form the middle
part, and the last pair forms the basis of the shaft and the socket. When the old cuticle is shed,
hydrostatic pressure everts the seta with its new soft cuticle. The annulus is left as a “scar” in the
new cuticle, indicating where the cuticle was folded during its formation.
The other type of setal development happens when the setae reform during a molt. Again,
little is known about the cellular processes, and the only ultrastructural data available stem from
malacostracan aesthetascs (Guse 1980, 1983) and for bimodal chemo- and mechanosensitive
composite setae of the shrimp Palaemon adspersus (Fig. 6.4C,D). In the premolt stage, the epi-
thelium starts to pull back from the cuticle, and in the isopod Idotea baltica, the sheath cells also
pull back. This means that the outer segments of the ORNs are exposed to the exuvial fluid and
are slowly digested, leaving the ORN insensitive for a period. The sheath cells pull back into an
invagination and start forming the cuticle of the new seta as described above. During this time,
the ORNs rebuild their outer segments, which is done by the time the old cuticle is shed and the
new seta is everted (Guse 1983). In other species such as the mysid Neomysis, not all the sheath
cells pull back; some stay in contact with the old cuticle and protect the outer segments during
most of the premolt stage. The way the tissue pulls back from the old cuticle to form the new one
is very standardized within species and is often used to stage the animal through the molt cycle
(e.g., Reaka 1975, Longmuir 1983, Hunter and Uglow 1998).
What is seen from the descriptions above is that both new setae and molting setae are formed
in an invagination, leaving them with an annulus. This means that the annulus is a by-product
of the complex setal development and that it could be another important character defining a
seta. Still, as stated earlier, it can be hard to detect in the intermolt, and there are indications that
some setae are not developed in this way (Fig. 6.4B; Watling 1989). This difference in ontogeny
suggests the question of whether these structures are true setae, which should be addressed
Fig. 6.4.
Setal development. (A) Crustacean setae form in an invagination during the premolt stage. After the molt,
the seta unfolds, due to hydrostatic pressure. The point of folding (arrowheads) becomes the annulus in
the new seta (see Fig. 6.3). (B) In some cases the new setae form without an invagination, as shown here
from maxilla 1 of the amphipod Uschakoviella echinophora. Asterisks indicate new setae inside the exuvium
(Ex). (C) Cross section of a composite seta during its formation in the premolt stage. Both the proximal
part of the cuticle (PC) and the distal part (DC) are lined with sheath cells (ShC). Outer dendritic seg-
ments (ODS) can be seen in the distal part. The lumen created by the invagination is partly filled with
extra-cellular matrix (ECM) closely encircling the setules (S). (D) Close-up of the tip of a forming seta
showing a thin cuticle (Cu) surrounding sheath cells and outer dendritic segments (ODS) with a dendritic
sheath (DS) around them.
with transmission electron microscopy. Even though the number of sheath cells seems to vary
greatly among different setae, their presence and similar arrangement leave the possibility that
the development might have many identical elements across crustacean taxa and setal types.
That said, far too little data are available from crustaceans at present to verify this. In insects, the
development of their sensilla (believed to be homologous with crustacean setae) follows very
strict patterns when it comes to the cells involved (Keil 1997).
SETAL MORPHOLOGY AND SENSORY MODALIT Y
Most but not all examined setae are sensory organs of some kind, and they are often referred to as
sensilla. There is experimental evidence for setae being mechano- and chemosensitive but also
indications of thermo-, osmo-, and hygrosensitivity. In most cases they appear to be bimodal
mechano- and chemoreceptors (see also chapter 7). The number of sensory cells that innervate
crustacean setae can vary from one to several hundred. Despite this diversity, there are shared
features in the organization and ultrastructure of sensory setae. In this section, we provide an
overview of the sensory properties of setae and discuss whether they can be predicted by some
of the external or internal structures of setae.
One feature common to all sensory setae is having sensory cells with cell bodies arranged in
clusters outside of the seta they innervate and a single dendrite innervating the seta. The den-
drite is composed of two parts, an inner dendritic segment (IDS) and an outer dendritic segment
(ODS). The IDS normally terminates at the setal base, but in some cases it continues into the
proximal part of the setal shaft. The ODS is a sensory cilium, and normally only a single ODS
protrudes from each IDS, but in the case of aesthetascs, the sensory cells often have two ODSs
(Gr ü nert and Ache 1988). In most cases, the ODS extends a long way up the lumen of the setal
shaft, but for some mechanoreceptor cells, the ODS terminates at the base of the seta, where it
contacts the cuticular part of the socket. Another shared feature of sensory setae is the presence
of sheath cells encircling the sensory cells. Besides the described role during setal formation,
little is known about the function of sheath cells. They enclose the dendrites in a fluid-filled
cavity, and even though not much is known about this fluid and what the sheath cells add to its
content, the sheath is known to protect the ODS against stress factors from the external envi-
ronment, such as low salinity (Gleeson et al. 2000). The innermost sheath cell often has special
functions. In mecha noreceptors it contains a scolopale, which is probably a prerequisite for the
signal transduction (see below for more details), and in many but far from all setae, the distal
part of the innermost sheath cell comprises the dendritic sheath, an extracellular structure that
encircles the ODS as it proceeds up through the setal shaft.
Chemosensation has been associated with a broad spectrum of setal types through elec-
trophysiological and morphological studies. In fact, most of the examined setae appear to be
chemoreceptive. Thus, there seems to be little if any evidence for external setal structures being
associated with chemosensitivity. One character that has been debated is the presence or absence
of a terminal or subterminal pore. There is some evidence that, at least for bimodal mechano-
and chemosensitive setae, a pore is needed for the ODS to contact the substratum (Fig. 6.5C)
(Alexander 1977, Garm et al. 2003, Schmidt and Derby 2005). But in other studies the pore has
been shown to be blocked by electron-dense material and it has been suggested that the pore is
a holdover from molting, a so-called molting pore (Haug and Altner 1984a). Further, the olfac-
tory aesthetascs almost always lack a terminal pore, showing that it is certainly not a necessity
for chemosensation in setae. Instead, aesthetascs have a thin and porous cuticle, letting through
the small molecules they detect, such as amino acids, ammonia, and adenosine monophosphate
(Derby et al. 1997, Steullet and Derby 1997, Derby 2000, Steullet et al. 2000b).
Interestingly, there might be external structures that indicate the absence of chemosensation.
To our knowledge, setae with long setules along the entire shaft (plumose and pappose setae)
have never been shown, including from ultrastructure, to be chemosensitive. In some cases these
setae are not innervated (Fig. 6.5A), which suggests that they have no sensory function. This can
be hard to tell, however, since mechanosensitive cells can be situated at a distance from a seta
and still detect displacement of the seta (Bender et al. 1984). In the few cases where they have
been shown to be sensory organs, plumose and pappose setae are mechanoreceptors detecting
waterborne vibrations (Vedel and Clarac 1976, Wiese 1976, Vedel 1985). This makes good sense
since the long setules make the setae more sensitive to water movements, and crustacean mech-
anoreceptors have been shown to respond to even the smallest setal displacements (Wiese 1976,
Fields et al. 2002). Arranging the setules in two rows, as for plumose setae, adds directionality
to the sensitivity. Long setules are by no means necessary for mechanoreception, though, and
mechanosensation has been either proven or at least indicated from ultrastructure for all major
types of setae (Tautz et al. 1981, Derby 1989, Garm et al. 2004, Garm 2005). Regarding osmo-,
Fig. 6.5.
Sensory properties of setae. (A) Cross section close to the base of a plumose seta showing several sheath
cells (ShC) but no sensory cells. S, setules. (B) Cross section of a serrate seta with both denticles (D) and
setules (S). The small lumen holds one outer dendritic segment (ODS). (C) Section through the terminal
pore of a serrate seta showing the outer dendritic segment protruding through the pore. (D) Most bimodal
chemo- and mechanosensory setae have their outer dendritic segments (ODS) enclosed by a dendritic
sheath (DS) until close to the tip. (E) The ciliary region of chemoreceptors (top) and mechanoreceptors
(bottom). In mechanoreceptors, the a-strands of the microtubules are electron dense (arrowhead) and
have dynein-like arms (arrow). (F) Almost all mechanosensory setae in crustaceans are of the scolopedial
type. The scolopale (Sc) is made of single strands of microtubules (arrowheads) connected by a dense
matrix of accessory proteins. (G) The inner dendritic segment (IDS) of mechanosensory cells displays a
large ciliary rootlet (CR), which has desmosomal connections (arrowheads) to the scolopale (Sc). (H) The
outer dendritic segments (ODS) of most mechanosensory cells have very densely packed single strands of
microtubules, which are thought to enhance their sensitivity to distortions.
thermo-, and hygroreceptors, far too little data are available to evaluate whether these modali-
ties are associated with any particular external structures (Tazaki 1975, Ache 1982, Ziegler and
Altner 1995, Garm et al. 2004). In conclusion, we find it highly questionable to address the sen-
sory functions of a seta from external characters alone even on the modality level.
From combined studies of sensory physiology and internal structure of setae, some structural
features, especially from the sensory cells, can be used to identify sensory modality (Altner et al.
1983, 1986, Schmidt and Gnatzy 1984, Hallberg et al. 1992, 1997, Derby et al. 2002). Interestingly,
information can be obtained at the histological level. The number of sensory cells can be deter-
mined in this way and in some cases can be used to identify chemosensitivity. From the existing
data, mechanosensation, and probably also osmo- and hygrosensation, is based on a maximum
of four sensory cells per seta (Mellon 1963, Schmidt and Gnatzy 1984, Ziegler and Altner 1995,
Garm et al. 2004). Chemosensation, on the other hand, is often based on many sensory cells,
with the aesthetascs of large decapods being the extreme, containing several hundred sensory
cells (Hallberg et al. 1992, Schmidt and Derby 2005, Hallberg and Skog 2011). The functional
explanation is probably that chemosensory setae need to detect a diversity of functionally rel-
evant chemical stimuli, which are often mixtures, and thus require a large number of receptor
molecules that are distributed nonhomogeneously across a population of sensory cells to iden-
tify the nature of those stimuli (Derby et al. 1994, 2001, Derby 2000). Since the functional unit
appears to be a single seta, each seta needs to contain this entire population of sensory cells
(Steullet et al. 2000b). It is important to keep in mind, though, that many sensory cells are not
a necessity for chemosensation in setae. Especially in small setae, there is strong evidence that
chemosensation can be based on very few cells (Altner et al. 1986, Elofsson and Hessler 1994,
Lagersson et al. 2003), but a small number of chemosensitive cells are also seen in some large
setae (Fig. 6.5B) (Altner et al. 1983). How the low number of sensory cells in these setae influ-
ences source identification is unknown.
On the ultrastructural level, there is better evidence for modality-specific structures. As
stated earlier, the ODS is a modified cilium and is the site of sensory transduction. For mech-
anoreceptors, it appears important that the ODS is anchored, possibly ensuring that the sensory
cells do not just follow the movements of the setae but are distorted when a seta moves. This
anchorage is located in the dendrite just proximal to the ODS, where the scolopale is found in
the innermost sheath cell (Fig. 6.5F,G). The scolopale is a very prominent structure made of
single strands of microtubules tied together by a large amount of associated protein (Fig. 6.5F)
(Schmidt and Gnatzy 1984). The ciliary rootlets of the mechanosensory cells contact the scol-
opale through desmosomes, and this connection provides the anchoring (Fig. 6.5G). Further
evidence for the role of the scolopale in mechanoreception comes from the fact that it is never
found in unimodal chemoreceptive setae. Still, there are some indications that putative osmore-
ceptors are also connected to the scolopale, but these cells were bimodal mechano- and osmore-
ceptors (Fig. 6.6) (Garm et al. 2004).
Within the sensory cells, the ciliary structures seem also to provide information on modality.
The ciliary rootlet of the mechanoreceptors is often very large, perhaps to enhance their stabil-
ity. The transition zone from IDS to ODS contains the ciliary region of the sensory cilium and
displays the classical 9 × 2 arrangement of the microtubules in a ring. In mechanosensory, but
not chemosensory, cells the a-strand is electron dense and carries arms resembling the motor
protein dynein (Fig. 6.5E). Further, the ciliary region of mechanoreceptors is several microm-
eters long, and it has been suggested that the stretch-sensitive ion-channels responsible for the
transduction from mechanical displacement to receptor potential are situated here (Crouau
1989). This is possibly true for some mechanoreceptive cells, but in other cases the transduction
occurs farther up the cilium (Calvet 2003, Praetorius et al. 2003, Garm et al. 2004, Garm and
Høeg 2006). In insects, most of the mechanoreceptors are not associated with a scolopale, but
A Bend-sensitive cell
Stimulus
Bend
B Bend-sensitive cell
Stimulus Dis Dis Dis

0s 2s 4s 6s 8s
C Stimulation on-set
0 sec 2 sec 4 sec 6 sec
DM
D E DS
Se Cu
Cu
MC
S
CR
CR
SD WD
SCR
LCR
ShC
0.5 μm
Type 1 Type 2 Type 3
Fig. 6.6.
Bimodal osmo- and mechanosensitive cells. (A) Electrophysiological recordings from mechanosensi-
tive cells in simple setae of Panulirus argus responding only to bending. (B) The same cell as in A did not
respond to displacements in the socket. (C) The bend-sensitive cells also responded to changes in osmo-
larity. Arrowheads indicate bend-sensitive cell; arrows indicates additional smaller units in the recording.
(D) The seta containing the bimodal osmo- and mechanosensitive cell displays an isolated outer dendritic
segment in the distal part (arrowhead), which is suggested to be the bimodal cell. (E) Schematic drawing
of the three types of sensory cells from simple setae in P. argus, identified by their ultrastructure. Type 3
is suggested as the bimodal cell. Abbreviations: CR, ciliary region; Cu, cuticle; DM, dense microtubules;
DS, dendritic sheath; LCR, large ciliary rootlet; MC, membranous cuticle; S, scolopale; SCR, small ciliary
rootlet; SD, strong desmosomal connection; Se Cu, setal cuticle; ShC, sheath cell; WD, weak desmosomal
connection.
instead, the dendrite ends in a tubular body composed of densely packed microtubules where
transduction is believed to take place (Keil 1998). Structurally similar sensory cells have been
found in association with setae of the terrestrial isopod Titanethes alba (Crouau 1995).
There are also indications that the distal part of the sensory cilium of mechanoreceptors has
special features. Their microtubules are often densely packed in most of the modified cilium
above the ciliary region, where the microtubules diverge in single strands (Fig. 6.5H), perhaps
enhancing the sensitivity of the cell (French 1988). Interestingly, sensory cilia can be activated
by bending without disturbing the proximal part (Praetorius et al. 2003). This has also been
found in mouthpart setae of the spiny lobster Panulirus argus, and in accordance with this
different way of stimulation, it was found that the cells have a short ciliary region, a weak con-
nection to the scolopale, and a small ciliary rootlet (Fig. 6.6). The same cells also respond to
osmotic changes, and it is not known if any of the modifications of the structures associated
with mechanoreception are due to this bimodality.
Transduction in chemoreceptor cells is mediated through G-coupled receptors situ-
ated in the ODS (Couto et al. 2005). These cells seem to be in no need for anchorage, as they
are never connected to the scolopale, and their ciliary rootlet is small and often fragmented
(e.g., Snow 1973). Most likely, as a further consequence of their difference in transduction, their
ciliary region is short, often <1 μm, and the ODS has few loosely packed single strands of micro-
tubules. The ODS of chemosensory cells continues to the very tip of the seta they innervate
(Fig. 6.5B,C), but so far it has not been proven where the stimulation of the receptor molecules
takes place. The ultrastructural data indicate that there might be differences here. In bimodal
mechano- and chemosensory setae, the ODSs are wrapped in a dendritic sheath up close to the
tip and sometimes also by projections of the sheath cells (Fig. 6.5D) (Garm et al. 2003, Garm
and Høeg 2006). Even though nothing is known about the functionality of this arrangement,
it indicates that the ODSs are not in contact with the external environment except for the last
few micrometers. This is supported by the setal shaft having a thick and dense cuticle up to
the tip (Fig. 6.5B). The situation is different in aesthetascs, which have no dendritic sheath,
a thin cuticle, and ODSs branching shortly after the ciliary region, resulting in a larger mem-
brane surface area (Gr ü nert and Ache 1988). Chemical stimuli can probably contact the ODS
along its entire length in aesthetascs (Blaustein et al. 1993), and these structural differences
may partly account for the reported threshold differences between the unimodal aesthetascs
and the bimodal mechano- and chemosensitive setae (Thompson and Ache 1980, Voigt and
Atema 1992, Garm et al. 2005).
A highly interesting and intriguing finding in sensory setae is the presence of bimodal
sensory cells. They can either be mechano- and chemosensors (Hatt 1986) or mechano- and
osmosensors (Tazaki 1975, Garm et al. 2004). Nothing is known about the ultrastructural
organization of the former, but in the latter case there are indications that it is intermediate
between mechano- and chemosensors (Garm and Høeg 2006). Bimodal cells have rarely been
identified in crustaceans, but a typical experimental setup applies either mechanical or chemi-
cal stimuli, and therefore, bimodal cells could easily have been missed because of lack of the
proper stimulus. Bimodal cells are also rare outside crustaceans but have been found in some
molluscs (Audesirk and Audesirk 1980).
Hygrosensitivity has never been proven by physiological experiments in crustaceans but has
been suggested from ultrastructure (Haug and Altner 1984b, Ziegler and Altner 1995). Studies
on insect hygroreceptors resulted in five characters suggesting hygroreception: (1) the ODS
proceeds into the seta, (2) the setal shaft has no apparent pores, (3) the ODS borders the setal
wall distally in the seta, (4) the ODSs are organized symmetrically in the setal lumen, and (5)
the setal wall is layered. From our experience, at least the first, second, fifth, and to some extent
the third characters are found in most of the examined bimodal chemo- and mechanoreceptive
setae (e.g., Altner et al. 1983, Crouau 1994).
Thermoreceptors are common in insect sensilla (Steinbrecht 1998), and several crustaceans
have been shown to respond to thermal stimulations and orient to a temperature gradient
(Barber 1961). The receptors responsible for these behaviors have not yet been identified, how-
ever, and might be other than setae.
To conclude, ultrastructural data suggest that crustacean sensory neurons have modal-
ity-specific structures at least for mechanoreceptors and chemoreceptors. Still, the largely
unknown bimodal cells and the possible presence of osmo-, hygro-, and thermoreceptors add a
question mark to what can be deduced about function of setae from their internal morphology.
Until these modalities have been examined in greater detail, no final conclusions can be drawn.
Furthermore, within each sensory modality, ultrastructure alone fails to reveal much about the
sensitivity of cells, such as what compounds and what concentrations stimulate a chemorecep-
tor cell.
SETAL MORPHOLOGY AND NONSENSORY FUNCTIONS
As shown in the preceding section, most setae are sensory organs, but setae also have other,
equally important functions. Especially important are mechanical functions during behav-
iors such as locomotion, digging, grooming, and feeding that mainly involve the setae on the
appendages. Combining macro-video recordings (Fig. 6.7) with scanning electron microscopy
has provided evidence that the mechanical functions are largely correlated with the size, shape,
and location of the setae and with the ultrastructure of the cuticle. In the following, we describe
some of the known mechanical functions of the setal types and how they relate to the setal mor-
phology (summarized in Table 6.2).
The cuticular outgrowths of the setae seem to be the character that offers most insights
about their mechanical function. Plumose setae with long fragile setules in two rows along their
entire length can be mechanoreceptors, but when situated on the pereopods or lateral mouth
appendages, they often serve as surface extensions used for water pumping or swimming (e.g.,
Kohlhage and Yager 1994). The two rows of long setules along the entire length of the setal shaft
operating at low Reynolds numbers ensure a large surface and thereby a large drag. They are also
flexible, which in the case of the water pump on the maxillipeds of decapods is enhanced by an
annulated setal shaft (Garm and Høeg 2000). Further, they are often arranged on the append-
ages such that they expand during the power stroke and collapse during the recovery stroke
(Burrows 2009). Pappose setae appear somewhat similar to plumose setae, but their setules are
randomly arranged along the shaft. Only in a few cases have their functions been studied, but
they have been shown to be involved in feeding in a number of decapods. In filter feeding deca-
pods such as galatheids and thalassinideans, they are found in high densities on the maxillipeds,
where they work as filters holding back small suspended particles (Nicol 1932, Nickell et al. 1998,
Stamhuis et al. 1998). In other crustaceans they are situated on the lateral mouthparts, perform
gentle prey handling, and in general create a setal barrier ensuring that small food particles do
not escape the mouth apparatus (Garm 2004a).
Many setae have small setules situated on the distal half, as in composite setae, and they
are also often involved in feeding (Schembri 1982, Lavalli and Factor 1995). They are typically
involved in gentle prey handling (Garm 2004a), and the small and often scalelike setules on the
distal part probably do not withstand rough handling but will provide a good grip on small par-
ticles. This, and their slender form, indicates that they do not apply much force to the prey items.
When not situated on the medial edge of the mouthparts, they are often involved in grooming
the neighboring mouthparts and head region, and their role during gill cleaning is well docu-
mented (Bauer 1989, 1998, 1999).
Serrate setae with the two rows of denticles on the distal part serve a variety of mechanical
functions. They are found on the mouthparts of almost all examined crustaceans, but again,
their function is best studied in decapods. Most are situated on the food-handling medial edges
and perform rough prey handling, such as holding and shredding (Hunt et al. 1992, Garm 2004a).
Another very common mechanical function of serrate setae is grooming of the head region, and
especially the antennae are groomed frequently. In decapods, specialized clusters on the pro-
podus and carpus of the endopod of maxilliped 3 are used in this behavior (Fig. 6.7E–H). Here
Fig. 6.7.
Mechanical functions of setae revealed by macro-video recordings. (A) Overview of the mouth appa-
ratus of Astacus astacus feeding on a mussel. (B) Close-up of Pagurus bernhardus eating a piece of fish.
The setae involved are found on the medial rim of maxilliped 1 and 2 (Mxp1–2), maxilla 2 (Mx2), and the
mandibular palp (MP). The incisor process of the mandibles (IP) and the labrum (La) are also shown.
(C) Endoscope recordings can reveal actions of otherwise hidden setae. Here large cuspidate setae from
the basis of maxilla 1 (Mx1) of Panulirus argus are seen between the incisor process (IP) and medial lobe
(ML). (D) A piece of mussel is held by setae on maxilliped 2 (Mxp2) of Penaeus monodon while setae
on the medial rim of maxilliped 1 (Mxp1) probe its surface. (E–H) Time series of serrate setae on the
endopod (endo) of maxilliped 3 (Mxp3) of P. bernhardus grooming the f lagellum of antenna 1 (Ant1).
Arrows indicate movements.
Table 6.2. Summary of the mechanical functions of the seven types of seta.
Seta type Mechanical function

Pappose Setal barriers, current direction, filtering
Plumose Surface extension of water pumps, setal barriers
Composite Gentle prey handling (reorientation and relocation of small prey

items), gentle grooming
Serrate Rough prey handling (collecting and holding prey and shredding soft
prey), rough grooming, filtering
Papposerrate Setal barriers, gentle prey handling
Simple Rough and gentle prey handling
Cuspidate Very rough prey handling (holding, shredding, and tearing large prey
items), restrict mouthpart movement, filtering
the denticles seemingly make the setae very efficient in scraping of debris, and their size can be
correlated with the robustness of the structure they groom (Garm and Høeg 2001). Grooming
by serrate setae is well documented in the literature (e.g., Bauer 1989, Pohle 1989, Fleisher et al.
1992). This suggests that when the serrate setae are found laterally on the mouthparts, such as
the endopods of the maxillae, they may function in grooming the neighboring limbs.
Papposerrate setae combine the long setules on the proximal part with denticles on the
distal part. They have been reported from a number of species (often as plumodenticulate
setae), but their mechanical functions have been studied only in a few species. In the crayfish
Austropotamobius pallipes and Cherax quadricarinatus, they were observed to perform gentle prey
manipulations such as pushing pieces of prey into the mouth (Thomas 1970, Garm 2004a).
A large number of setae have no outgrowths and appear more or less smooth, and such setae
are found in all crustaceans. Most of them are slender, and their length can vary from a few
micrometers to several millimeters. No mechanical functions have been documented for the
smaller of these simple setae, and the evidence points to them being unimodal chemorecep-
tors (Hipeau-Jacquotte 1986, Elofsson and Hessler 1994). The mechanical functions of the larger
simple setae seem to depend on their location. The aesthetascs on antenna 1 belong to this group,
and they are again unimodal chemoreceptors with no apparent mechanical functions (Hallberg
et al. 1992). When situated on the mouthparts of decapods, simple setae have been found to
perform a broad range of mechanical function, which is species dependent (Garm 2004a). In
some species, they appear mainly gustatory with reduced mechanical functions, but in P. argus,
they are the dominant setal type performing rough prey handling. In the latter case, the lack of
outgrowths is probably to avoid damage during feeding.
Cuspidate setae are also often without outgrowths, and they seem to perform the most rough
mechanical functions. This is clearly seen on the mouth apparatus, where they are involved in
shredding and tearing of the prey. Still, in the hermit crab Pagurus rubricatus, cuspidate setae on
the medial rim of maxilla 1 can act as a filter (Schembri 1982). This is a surprising function for
cuspidate setae and stresses that one should be careful not to assume the functions of setae from
their morphology alone.
Only a few nonsensory functions besides the mechanical functions have been documented
for setae. In a recent study, it was shown from ultrastructural data that some simple setae from
the mouthparts of the remipede Speleonectes tanumekes are associated with glands and might
therefore be involved in secretion (van der Ham and Felgenhauer 2008). Setae are also bound
to have an impact on the hydrodynamics of crustaceans, which will be most important for small
swimming species (see chapter 11).
FOSSIL SETAE
The cuticle is advantageous when you want to study the evolutionary history of crustaceans
since it fossilizes easily. Unfortunately, when it comes to fine structural details such as the setae,
information is often lacking (e.g., Collins et al. 2003). A uniquely well-preserved arthropod
fauna, called the “Orsten” fauna (see chapter 2), has been found in which the miniature ani-
mals from the Cambrian still display beautiful setae (Fig. 6.8). Surprisingly, these setae display
a great diversity, and several of the seven types we have suggested can be recognized. On the
mouthparts of the fossil crustaceans Rehbachiella, Bredocaris, and members of Skaracarida, at
least cuspidate, composite, and serrate setae were present (Fig. 6.8A–C) (Mü ller and Walossek
1985, 1988, Walossek 1993). Plumose and pappose setae were probably also present, but even
though well preserved, most of the setules are broken, impeding certainty about their original
Fig. 6.8.
Fossil setae. (A–C) Orsten fossils of Rehbachiella from the Cambrian show very well-preserved setae. The
mouthparts display many composite and serrate setae. Arrows indicate setules; the arrowhead indicates
denticles. (D) Agnostus pisiformis, also from the Orsten fauna, displays advanced setal types such as plu-
mose setae shown here. Arrows indicate setules. Pictures courtesy of Prof. Dieter Walossek.
length. One important aspect of these findings is that they strongly suggest that at least most of
the setal types we have put forward for crustaceans date back to their very early evolutionary
history. If the setal types represent homologies, this was to be expected since all major recent
subgroups of Crustacea seem to display all the seven types of setae, and setal differentiation
therefore predates their last common ancestor. There is even evidence in the fossil record that
some differentiation happened very early in arthropod history. Another member of the Orsten
fauna, Agnostus pisiformis, which is closely related to trilobites, also displays several of these
advanced setal types (Fig. 6.8D) (Mü ller and Walossek 1987).
Only a few authors have addressed the internal relationship and evolution of setae, but it
has been suggested that the most fundamental setal type is the simple seta and that the other
types have evolved from this type by adding more complex features to the setal shaft (Farmer
1974). If so, one would expect to find many simple setae in the early fossil record. Interestingly,
the animals from the Orsten fauna seem to have very few simple setae (Mü ller and Walossek
1985, 1987, 1988, Walossek 1993). The alternative hypothesis is that simple setae have arisen
from other setal types by reduction of the outgrowths. This is supported by setules and den-
ticles being general features of the cuticle and not structures that have evolved exclusively
on the setal shaft. Setules and denticles in the general cuticle appeared early in arthropod
history, which is also seen in the Orsten fauna, where these structures are numerous on the
appendages (Fig. 6.8C) (Walossek 1993). The general lack of simple setae on the mouthparts
of Orsten animals can perhaps be explained by their small size, since small present-day crus-
taceans in general have few simple setae on their mouth appendages (e.g., Høeg et al. 1994,
Olesen 2001). Further, simple setae have limited functionality, and more complex setae would
be needed to support the likely suspension feeding habit of these small animals. The little
change in the external morphology of setae during the last 550 million years also indicates
that the mechanical functions are preserved.
NONSETAL STRUCTURES OF THE CUTICLE
Compared to setae, much less is known about development and functions of other cuticular struc-
tures. Setules in the general cuticle seem to be found throughout Crustacea but almost exclusively
around the mouth apparatus. They are never innervated, and thus they have no sensory func-
tions. Their mechanical function has been studied only in a few decapods and only indirectly
(Garm 2004a). They are found on the paragnaths of some decapods, where they fill the space
between the paragnath and maxilla 1. In this way, they prevent small food particles from escaping
and groom the oral surface of maxilla 1. From their arrangement in other crustaceans, it is likely
that they serve similar functions (e.g., Alexander 1988, Olesen 2001), and it is noteworthy that this
coincides with the functions they serve when situated on setae. Whether setae have adopted set-
ules along with some of their functions from the general cuticle or whether cuticular setules repre-
sent heavily reduced setae are unknown. The fossil record does not shed any light on this question
since even Agnostus filiformis had both composite setae and setules on the cuticle (Mü ller and
Walossek 1987).
Denticles are found in the general cuticle of many crustaceans and can be found on most
body parts. Like setules, they are not sensory, but no other function has been associated with
them. They could play an important role in hydrodynamics, as has been shown for the dermal
teeth of sharks (Lang et al. 2008). Still, denticles are often found on the mouthparts and between
fields of setae (Fig. 6.1D), where they will have no contact with prey items or have effect on the
hydrodynamics, and their function here remains enigmatic. Spines, on the other hand, have
well-documented functions and serve mainly in rough prey handling and predator avoidance
(Briones-Fourzan et al. 2006). Spines are mostly found on the appendages, such as antenna 2 of
spiny lobsters, but can be found in many other places.
There are many other cuticular structures that are nonarticulated. Klepal and Kastner (1980)
arranged such features into the following categories: hump, protuberance, scale, tooth, fringe,
spine, and comb. Humps and protuberances are round or irregularly shaped areas, respectively,
that push outward from the surrounding cuticle. They have been documented from tanaids
and cumaceans. Scales are flat structures, usually curved, and as wide as or wider than long,
although these dimensions may vary (see Klepal and Kastner 1980, their figs. 6–13). Teeth are
solid, cone-shaped structures of varying length, and when together in a row, they form combs.
Fringes are similar to combs, but the cuticular structures are longer and may be flexible. The
one feature that Klepal and Kastner (1980) include in their list of nonsensory structures that
may need further investigation is what they call a “spine.” They define a spine as a large, strong,
hollow, cone-shaped structure, and their images clearly show an articulated base. It is likely that
these structures are, in fact, cuspidate setae.
When it comes to the development of the nonsetal structures, both when first appearing and
during a molt, little is known about the processes involved. To our knowledge, nobody has stud-
ied the development of setules and denticles in the cuticle. Transmission electron microscopic
data from both early and late intermolt indicates that they are not associated with sheath cells
(Fig. 6.1E), suggesting that their development differs from that of denticles and setules on setae
(see earlier section). This does not support the supposed homology between these structures,
but it is not at all impossible that sheath cells are involved during the formation of the new cuti-
cle and then later degenerate or transform.
COMPARISON WITH OTHER ARTHROPOD GROUPS
When observing the cuticle of other arthropods, it immediately becomes obvious that some of
the structures are homologous to what we have described from crustaceans. Again, the most
notable and best understood is setae, which are found in all examined arthropod subphyla. In
the following, we compare crustacean setae with those from insects and spiders, which, espe-
cially in the former, are well understood (for detailed reviews, see Steinbrecht 1997, Keil 1997,
1998).
Insects have setae, or sensilla, as they are most often called in this group, scattered on all body
parts, but just as for crustaceans, they are most commonly found on the appendages and in the
head region. When the detailed external morphology is examined, however, insect setae differ
from crustacean setae, probably at least partly due to their terrestrial habitat. First of all, as a
general trend, they have many fewer and smaller outgrowths; long setules would likely collapse
without the support of the water. Instead, insect mechanoreceptors are long and normally slen-
der setae (Keil 1998). They also have large leaf- or club-shaped mechanosensory setae special-
ized for gravity sensing. The ability to sense gravity directly in this way is again due to the lack
of surrounding water. The cuticle of insect chemosensory setae always seems to have detectable
pores. In the case of olfactory setae, two systems are present, double- and single-walled setae,
both with numerous pores in most of the setal shaft allowing the odors to contact the ODSs
(Steinbrecht 1997). The gustatory setae of insects are normally bimodal receptors as in crusta-
ceans, and they also display a prominent terminal pore. The olfactory setae have other speciali-
zations not seen in crustaceans because of the physical differences of their habitats. Since they
detect airborne odors, they need an interface to get them in contact with the ODS in the recep-
tor lymph. This is seen as a complex canal system in the cuticle, where the odors are collected
and transported by so-called odor-binding proteins (R ützler and Zweibel 2005).
The ontogeny of insect setae has been studied in detail and is well understood (Keil 1997).
The pattern of sheath cells (enveloping cells) and their function are much stricter than in crus-
taceans. Normally, three (sometimes two or four) sheath cells are involved in the development
of the setae: the trichogen, tormogen, and thecogen cell. Their functions are similar to what is
known from crustaceans, and they form the cuticle of the seta, protect the sensory cells, and
produce the receptor lymph. They encircle the receptor cells, which are normally fewer than
in crustaceans, although insect olfactory setae can hold up to 50 receptor cells (Hallberg and
Hansson 1999).
All insect setae are considered to be sensory and have been found to be mechano-, chemo-,
hygro-, thermo-, and carbon dioxide receptors. As for crustaceans, the most common are
chemo- or mechanoreceptors, but there seems to be a more strict division, with bimodal chemo-
and mechanosensitive setae being less common. This is partly because insects have many more
types of olfactory setae, which all seem to be unimodal as in crustacean aesthetascs (Hallberg
and Hansson 1999). In insects, the transduction mechanisms are known for most of the modali-
ties, not least because of the powerful molecular tools available to study Drosophila and some
other species (e.g., Caldwell and Eberl 2002). Insects do have scolopedial mechanoreceptors
similar to those of crustaceans, but most insect mechanoreceptors differ in that they have no
scolopale but instead a tubular body distally in the ODS, where both stimulation and trans-
duction takes place (Keil 1998). Here the mechanosensitive ODS stops at the setal base, where
movements of the seta distort the tubular body. This is again likely a terrestrial adaptation,
since structurally similar mechanoreceptors are found in terrestrial isopods (Crouau 1994).
From work on insects, it is also known that thermoreceptors are modified mechanoreceptors
(Mü ller et al. 2008), which is likely also true for hygroreceptors and carbon dioxide receptors
(Stange and Stowe 1999).
Setae in spiders are at least as diverse as in crustaceans and insects, and many of them appear
so similar to crustacean setae that it is difficult to tell them apart (Figs. 6.3, 6.9). Still, as in insects,
most of them have few and short outgrowths (Talarico et al. 2006), probably because of their ter-
restrial habitat. Unfortunately, rather little experimental work has been performed on their func-
tional morphology. They probably have many mechanical functions, and they are all putative
receptors. One of the mechanical functions that has been studied is how setae aid when adher-
ing to surfaces (Niederegger and Stanislav 2006). As for crustaceans, there seems to be a good
correlation between the detailed appearance of the setule-like outgrowths and their mechanical
function. Very little is known about the chemosensors, but some spider mechanosensors, the
trichobothria, are understood in great detail (Barth and Höller 1999). In trichobothria setae
(Fig. 6.9B), which are always unimodal mechanoreceptors, there is a strict correlation between
the structure and arrangement of the setal shaft and the sensory properties.
On the ultrastructural level, the existing data from spider setae indicate that the sensory cells
are similar to both insect and crustacean sensory cells and arranged in similar ways. The sensory
cilia of the chemoreceptors proceed a long way up the setal shaft, and in putative gustatory setae
they are enclosed by a dendritic sheath (Talarico et al. 2006). In olfactory setae, the dendritic
sheath is missing, and the ODSs lay against the setal cuticle and are in contact with the odors
through a pore system as in insects. The ultrastructure of spider mechanoreceptors appears very
similar to insect mechanoreceptors of the tubular body type (Talarico et al. 2006).
WHAT’S NEXT: INTERTAXON AND INTERMETHODOLOGICAL RESEARCH
What we hope to have illustrated in this review is that a fair amount of knowledge is availa-
ble about surface structures of the crustacean cuticle. What is also evident is that this knowl-
edge stems almost entirely from malacostracans and especially from decapod setae. This is
Fig. 6.9.
Setae from spiders. (A) Setae associated with the claws of Nicodamus mainae. Arrows indicate setae very
similar to crustacean serrate setae (compare with Fig. 6.3D). (B) Trichobothria from the palp of Mimetus
hesperus. These mechanosensitive setae closely resemble simple setae of crustaceans and are the most
studied and best-understood spider setae. The open socket (arrows) makes them very flexible, and in most
case they respond to tiny distortions. (C) Setae from the scopula of Copa flavoplumosa with outgrowths
that resemble setules. One type is similar to crustacean plumose setae (arrows; compare with Fig. 6.3B).
(D) A common type of spider seta from the abdomen of Pikelinia tam. The function is unknown, and it has
no obvious counterpart in crustaceans. (E) Setae from the metatarsa of a leg of Pseudolampona emmett.
These setae are so similar to many crustacean composite setae that they can hardly be distinguished from
them (compare with Fig. 6.3C). Pictures courtesy of Dr Mart í n J. Ram í rez.
unfortunate when the goal is to have a broad understanding of these structures functionally,
ontogenetically, and evolutionarily.
One of the issues we find of great importance is better understanding of how the different
structures in the cuticle group together and how these groups differ from each other. This should
be studied in an evolutionary context by finding homologies to define the groups. The develop-
mental processes seem to be the most promising place to start. Only a few malacostracan species
have been examined, and a study comparing setal development from a broad range of crustacean
groups is therefore highly desirable. A study of the development and formation of the setules and
denticles on the general cuticle is also wanted for comparison with the formation of the similar
structures on the setae. This is vital to test their possible homology.
Another of the very interesting aspects for crustacean setae is their functional morphology,
which for a large part can be separated into mechanical functions and sensory functions, as we
have described here. We have put forward a classification system based on the external struc-
tures and indicated that this system also follows their mechanical functions. Whether this is
a general rule within crustaceans is too early to decide, since almost all the data come from
large decapods. What is badly needed here are studies combining behavioral observations and
scanning electron microscopy from several distantly related taxa. It is necessary to make the
behavioral observations such that the actions of identifiable setae can be followed during feed-
ing, grooming, walking, and so forth. This is certainly a challenge, but with modern high-speed
and high-resolution video equipment, it is also possible.
The last point we want to make concerns the sensory functions of setae. The bulk of the
available evidence suggests that the most common type of sensory seta in crustaceans is a bimo-
dal chemo- and mechanoreceptor. This needs solid confirmation from more setal types through
electrophysiological experiments. By combining such studies with high-quality transmission
electron microscopy, the structural basis for these modalities can also be finally established. It is
also of the highest interest to get better confirmation on the possible presence of osmo-, hygro-,
and thermosensitive setae. Since there is evidence from insects that all of these modalities are
closely linked to mechanoreception, it is likely that they share many ultrastructural features.
This can turn out to cause serious problems to ultrastructural identification of sensory modal-
ity. The bimodal cells are somewhat of a mystery, and finding out how the combined trans-
duction works, along with how the nervous system separates the information, is of the greatest
interest, not only for crustacean sensory biology but also for neuroscience in general.
ACKNOWLEDGMENTS
We thank Associate Professor Nikolaj Scharff (Natural History Museum of Copenhagen) and
Mart í n J. Ram í rez and Mat ías A. Izquierdo (Museo Argentino de Ciencias Naturales) for pro-
viding pictures of arachnids (all parts of the Assembling the Tree of Life: Phylogeny of Spiders
project). Further, we are grateful for the pictures provided by Associate Professor Jens Høeg
(University of Copenhagen) and Professor Dieter Waloszek (University of Ulm) of Parapagurus
sulcata and fossil arthropods, respectively. We also acknowledge the financial support from the
Danish Science Council to A.G. (grant 272–07–0163).
REFERENCES
Ache, B.W. 1982. Chemoreception and thermoreception. Pages 369–398 in H.L. Atwood and D.C.
Sandeman, editors. The biology of Crustacea, Vol. 3. Academic Press, New York.
Alexander, C.G. 1977. Antennal sense organs in the isopod Ligia oceanica. Marine Behaviour and
Physiology 5:61–77.
Alexander, C.G. 1988. The paragnaths of some intertidal crustaceans. Journal of the Marine Biological
Association 68:581–590.
Alexander, C.G., J.P.R. Hindley, and S.G. Jones. 1980. Structure and function of the third maxillipeds of
the banana prawn, Penaeus merguiensis. Marine Biology 58:245–249.
Altner, I., H. Hatt, and H. Altner. 1983. Structural properties of bimodal chemo- and mechanosensi-
tive setae on the pereiopod chelae of the crayfish, Austropotamobius torrentium . Cell and Tissue
Research 228:357–374.
Altner, H., H. Hatt, and I. Altner. 1986. Structural and functional properties of the mechanoreceptors and
chemoreceptors in the anterior oesophageal sensilla of the crayfish, Astacus astacus. Cell and Tissue
Research 244:537–547.
Audesirk , G., and T. Audesirk. 1980. Complex mechanoreceptors in Tritonia diomedea 1. Responses to
mechanical and chemical stimuli. Journal of Comparative Physiology A 141:101–110.
Barber, S.B. 1961. Chemoreception and thermoreception. Pages 109–131 in T.H. Waterman, editor. The
physiology of Crustacea, Vol. 2. Academic Press, New York.
Barth, F.G., and A. Höller. 1999. Dynamics of arthropod filiform hairs. V. The response of spider tri-
chobothria to natural stimuli. Proceedings of the Royal Society of London Series B 354:183–192.
Bauer, R.T. 1989. Decapod crustacean grooming: Functional morphology, adaptive value, and phyloge-
netic significance. Pages 49–74 in B. Felgenhauer, L. Watling , and A.B. Thistle, editors. Functional
morphology of feeding and grooming in Crustacea. Balkema, Rotterdam.
Bauer, R.T. 1998. Gill cleaning mechanisms of the crayfish, Procambarus clarkii (Astacidea: Cambaridae):
Experimental testing of setobranch function. Invertebrate Biology 117:129 –143.
Bauer, R.T. 1999. Gill-cleaning mechanisms of a dendrobranchiate shrimp, Rimapenaeus similis (Decapoda,
Penaeidae): Description and experimental testing of function. Journal of Morphology 242:125–139.
Bender, M., W. Gnatzy, and J. Tautz. 1984 . The antennal feathered hairs in the crayfish: A non-innervated
stimulus transmitting system. Journal of Comparative Physiology A 154:45–47.
Blaustein, D.N., R.B. Simmons, M.F. Burgess, C.D. Derby, M. Nishikawa, and K.S. Olson. 1993.
Ultrastructural localization of 5’AMP odorant receptor sites on the dendrites of olfactory receptor
neurons of the spiny lobster. Journal of Neuroscience 13:2821–2828.
Brandt, A. 1988. Morphology and ultrastructure of the sensory spine, a presumed mechanoreceptor of
Sphaeroma hookeri (Crustacea, Isopoda), and remarks on similar spines in other peracarids. Journal
of Morphology 198:219 –229.
Briones-Fourzan, P., M. Perez-Ortiz , and E. Lozano-Alvarez . 2006. Defense mechanisms and antipreda-
tor behavior in two sympatric species of spiny lobsters, Panulirus argus and P. guttatus. Marine
Biology 149:227–239.
Burrows, M. 2009. A single muscle moves a crustacean limb joint rhythmically by acting against a spring
containing resilin. BMC Biology 27:1–17.
Caldwell, J.C., and D.F. Eberl. 2002. Towards a molecular understanding of Drosophila hearing. Journal
of Neurobiology 53:172–189.
Calvet, J.P. 2003. Ciliary signaling goes down the tubes. Nature Genetics 33:113–114.
Coelho, V.R., and S.A. Rodrigues. 2001. Setal diversity, trophic modes and functional morphology of
feeding appendages of two callianassid shrimps, Callichirus major and Sergio mirim (Decapoda:
Thalassinidea: Callianassidae). Journal of Natural History 35:1447–1483.
Collins, J.S.H., C. Lee, and J. Noad. 2003. Miocene and Pleistocene crabs (Crustacea, Decapoda) from
Sabah and Sarawak. Journal of Systematic Palaeontology 1:187–226.
Couto, A., M. Alenius, and J.B. Dickson. 2005 . Molecular, anatomical, and functional organization of the
Drosophila olfactory system. Current Biology 15:1537–1545.
Crouau, Y. 1989. Feeding mechanisms of the Mysidacea. Pages 153–172 in B.E. Felgenhauer , L. Watling ,
and A.B. Thistle, editors. Functional morphology of feeding and grooming in Crustacea. Balkema,
Rotterdam.
Crouau, Y. 1994 . Ultrastructure d’un organe sensoriel antennaire de l’isopode terrestre cavernicole,
Titanethes alba. Canadian Journal of Zoology 72:2199 –2204.
Crouau, Y. 1995 . Association in a crustacean sensory organ of two usually mutually exclusive mechano-
sensory cells. Biology of the Cell 85:191–195.
Crouau, Y. 1997. Comparison of crustacean and insect mechanoreceptive setae. International Journal of
Insect Morphology and Embryology 26:181–190.
Cuadras, J. 1982. Microtrichs of amphipod Crustacea. Morphology and distribution. Marine Behaviour
and Physiology 8:333–343.
Derby, C.D. 1989. Physiology of sensory neurons in morphologically identified cuticular sensilla of
crustaceans. Pages 27–48 in B.E. Felgenhauer, L. Watling , and A.B. Thistle, editors. Functional
Derby, C.D. 2000. Learning from spiny lobsters about chemosensory coding of mixtures. Physiology and
Behavior 69:203–209.
Derby, C.D., M.F. Burgess, K. Olson, T. Simon, and A. Livermore. 1994 . Mechanisms of detection and
discrimination of mixtures in the olfactory system of spiny lobster. Pages 775–777 in K. Kurihara ,
N. Suzuki, and H. Ogawa , editors. Olfaction and taste, Vol. 9. Springer, Tokyo.
Derby, C.D., H.S. Cate, and L.R. Gentilcore. 1997. Perireception in olfaction: Molecular mass sieving
by aesthetasc sensillar cuticle determines odorant access to receptor sites in the Caribbean spiny
lobster, Panulirus argus. Journal of Experimental Biology 200:2 073–2081.
Derby, C.D., P. Steullet, H.S. Cate, and P.J.H. Harrison. 2002. A compound nose: Functional organiza-
tion and development of aesthetasc sensilla. Pages 346–358 in K. Wiese, editor. The crustacean
nervous system. Springer, Berlin .
Derby, C.D., P. Steullet, A.J. Horner, and H.S. Cate. 2001. The sensory basis of feeding behaviour in the
Caribbean spiny lobster, Panulirus argus. Marine and Freshwater Research 52:1339 –1350.
Duncan, K.W. 1985 . Cuticular microstructures of terrestrial Amphipoda (Crustacea, Family Talitridae).
Zoologischer Anzeiger 215:140 –146.
Ekerholm, M., and E. Hallberg. 2002. Development and growth patterns of olfactory sensilla in malacos-
tracan crustaceans. Pages 376–385 in K. Wiese, editor. The crustacean nervous system. Springer,
Berlin .
Elofsson, R., and R.R. Hessler. 1994 . Sensory structures associated with the body cuticle of
Hutchinsoniella macracantha (Cephalocarida). Journal of Crustacean Biology 14:454–462.
Farmer, A.S. 1974 . The functional morphology of the mouthparts and pereiopods of Nephrops norvegicus
(L.) (Decapoda: Nephropidae). Journal of Natural History 8:121–142.
Fields , D.M., D.S. Shaeffer, and M.J. Weissburg. 2002 . Mechanical and neural response from the
mechanosensory hairs on the antennule of Gaussia princeps . Marine Ecology Progress Series
227:173–186.
Fish, S. 1972. The setae of Eurydice pulchra (Crustacea: Isopoda). Journal of Zoology 166:163–177.
Fleisher, J., M. Grell, J.T. Hoeg , and J. Olesen. 1992. Morphology of grooming limbs in species of
Petrolisthes and Pachycheles (Crustacea: Decapoda: Anomura: Porcellanidae) a scanning electron
microscopy study. Marine Biology 113:425–435.
French, A.S. 1988. Transduction mechanisms of mechanosensilla. Annual Review of Entomology 33:39 –58.
Garm, A. 2004a . Mechanical functions of setae from the mouth apparatus of seven species of decapod
crustaceans. Journal of Morphology 260:85–100.
Garm, A. 2004b. Revising the definition of the crustacean seta and setal classification systems based
on examinations of the mouthpart setae of seven species of decapods. Zoological Journal of the
Linnaean Society 142:233–252.
Garm, A. 2005 . Mechanosensory properties of the mouthpart setae of the European shore crab Carcinus
maenas. Marine Biology 147:1179 –1190.
Garm, A., C.D. Derby, and J.T. Høeg. 2004 . Mechanosensory neurons with bend- and osmo-sensitivity in
mouthpart setae from the spiny lobster Panulirus argus. Biological Bulletin 207:195–208.
Garm, A., C.D. Derby, and J.T. Høeg. 2005 . Chemosensory neurons in the mouthparts of the spiny
lobsters Panulirus argus and P. interruptus (Crustacea: Decapoda). Journal of Experimental Marine
Biology and Ecology 314:175–186.
Garm, A., E. Hallberg , and J.T. Høeg. 2003. Role of maxilla 2 and its setae during feeding in the shrimp
Palaemon adspersus (Crustacea: Decapoda). Biological Bulletin 204:126 –137.
Garm, A., and J.T. Høeg. 2000. Functional mouthpart morphology of the squat lobster Munida sarsi, with
comparison to other anomurans. Marine Biology 137:123–138.
Garm, A., and J.T. Høeg. 2001. Function and functional groupings of the complex mouth apparatus of the
squat lobsters Munida sarsi Huus and M. tenuimana G.O. Sars (Crustacea: Decapoda). Biological
Bulletin 200:281–297.
Garm, A., and J.T. Høeg. 2006. Ultrastructure and functional organization of mouthpart sensory setae of
the spiny lobster Panulirus argus. Journal of Morphology 267:464–476.
Gleeson, R.A., L.M. McDowell, H.C. Aldrich, K. Hammar, and P.J.S. Smith. 2000. Sustaining olfaction at
low salinities: Evidence for a paracellular route of ion movement from the hemolymph to the sensillar
lymph in the olfactory sensilla of the blue crab Callinectes sapidus. Cell and Tissue Research 301:423–431.
Gr ü nert, U., and B.W. Ache. 1988. Ultrastructure of the aesthetasc (olfactory) sensilla of the spiny lobster,
Panulirus argus. Cell and Tissue Research 251:95–103.
Guse, G.W. 1980. Development of antennal sensilla during moulting in Neomysis integer (Leach)
(Crustacea, Mysidacea). Protoplasma 105:53–67.
Guse, G.W. 1983. Ultrastructure, development, and moulting of the aesthetascs of Neomysis integer and
Halcrow, K., and E.L. Bousfield. 1987. Scanning electron microscopy of surface microstructures of some
gammaridean amphipod crustaceans. Journal of Crustacean Biology 7:274–287.
Hallberg , E., and B.S. Hansson. 1999. Arthropod sensilla: Morphology and phylogenetic considerations.
Microscopy Research and Technique 47:428 –439.
Hallberg , E., K.U.I. Johansson, and R. Elofsson. 1992. The aesthetasc concept: Structural variations of puta-
tive olfactory receptor cell complexes in Crustacea. Microscopy Research and Technique 22:325–335.
Hallberg , E., K.U.I. Johansson, and R. Wallén. 1997. Olfactory sensilla in crustaceans: Morphology,
sexual dimorphism, and distribution patterns. International Journal of Insect Morphology and
Embryology 26:173–180.
Hallberg , E., and M. Skog. 2011. Chemosensory sensilla in crustaceans. Pages 103–121 in T. Breithaupt and
M. Thiel, editors. Chemical communication in crustaceans. Springer, New York.
Harris, R.A. 1979. A glossary of surface sculpturing. Entomology Occasional Papers No. 28. California
Department of Food and Agriculture Laboratory Services, Sacramento.
Hatt, H. 1986. Responses of a bimodal neuron (chemo- and vibration-sensitive) on the walking legs of the
crayfish. Journal of Comparative Physiology A 159:611–617.
Haug , T., and H. Altner. 1984a. A cryofixation study of a subcuticular receptor organ in the antennular
tip of the terrestrial isopod, Porcellio scaber Latr. (Crustacea). Journal of Ultrastructure Research
87:62–74.
Haug , T., and H. Altner. 1984b. A cryofixation study of presumptive hygroreceptors on the antennule of a
terrestrial isopod. Tissue and Cell 16:377–391.
Hinton, H.E. 1970. Some little known surface structures. Pages 41–58 in A.C. Neville, editor. Insect
ultrastructure. Royal Entomological Society, London .
Hipeau-Jacquotte, R. 1986. A new cephalic type of presumed sense organ with naked dendritic ends in
the atypical male of the parasitic copepod Pachypygus gibber (Crustacea). Cell and Tissue Research
245:29 –35.
Høeg , J.T., E.S. Karnick , and A. Frølander. 1994 . Scanning electron microscopy of mouth appendages in
six species of barnacles (Crustacea: Cirripedia: Thoracica). Acta Zoologica 75:337–357.
Holdich, D.M. 1984 . The cuticular surface of woodlice: A search for receptors. Symposia of the
Zoological Society of London 53:9 –48.
Holmquist, J.G. 1989. Grooming structure and function in some terrestrial Crustacea. Pages 95–114 in B.
Felgenhauer , L. Watling , and A.B. Thistle, editors. Functional morphology of feeding and groom-
ing in Crustacea. Balkema, Rotterdam.
Hunt, M.J., H. Winsor, and C.G. Alexander. 1992. Feeding by the penaeid prawns: The role of the anterior
mouthparts. Journal of Experimental Marine Biology and Ecology 160:33–46.
Hunter, D.A., and R.F. Uglow. 1998. Setal development at moult staging in the shrimp Crangon crangon
(L.) (Crustacea: Decapoda: Crangonidae). Ophelia 49:195–209.
Jacques, F. 1989. The setal system of crustaceans: Types of setae, groupings, and morphology. Pages 1–13
in B. Felgenhauer, L. Watling , and A.B. Thistle, editors. Functional morphology of feeding and
grooming in the Crustacea. Crustacean Issues 6. A.A. Balkema, Rotterdam.
Johnston, D.J. 1999. Functional morphology of the mouthparts and alimentary tract of the slipper lobster
Thenus orientalis (Decapoda: Scyllaridae). Marine and Freshwater Research 50:213–223.
Keil, T.A. 1997. Comparative morphogenesis of sensilla: A review. International Journal of Insect
Morphology and Embryology 26:151–160.
Keil, T.A. 1998. The structure of integumental mechanoreceptors. Pages 385–404 in F.W. Harrison and
M. Locket, editors. Insecta, Vol. 2B. Wiley-Liss, New York.
Klepal, W., and R.T. Kastner. 1980. Morphology and differentiation of non-sensory cuticular structures
in Mysidacea, Cumacea, and Tanaidacea (Crustacea, Peracarida). Zoologica Scripta 9:271–281.
Kohlhage, K., and J. Yager. 1994 . An analysis of swimming in remipede crustaceans. Philosophical
Transactions of the Royal Society of London Series B 346:213–221.
Lagersson, N.C., A. Garm, and J.T. Høeg. 2003. Notes on the ultrastructure of the setae on the fourth
antennulary segment of the Balanus amphitrite cyprid (Crustacea: Cirripedia: Thoracica). Journal
of the Marine Biological Association 83:361–365.
Lang , A.W., P. Motta, P. Hidalgo, and M. Westcott. 2008. Bristled shark skin: A microgeometry for
boundary layer control. Bioinspiration and Biomimetics 3:1–9.
Lavalli, K., and J. Factor. 1995 . The feeding appendages. Pages 349–393 in J. Factor, editor. Biology of the
lobster. Academic Press, New York.
Longmuir, E. 1983. Setal development, moult-staging and ecdysis in the banana prawn Penaeus merguien-
sis. Marine Biology 77:183–190.
Martin, J.W. 1989. Morphology of the feeding structures in the Conchostraca with special reference to
Lynceus . Pages 123–136 in B. Felgenhauer, L. Watling , and A.B. Thistle, editors. Functional morphol-
ogy of feeding and grooming in Crustacea. Balkema, Rotterdam.
Martin, J.W., and C.E. Cash-Clark 1995 . The external morphology of the onychopod “cladoceran” genus
Bythotrephes (Crustacea, Branchiopoda, Onychopoda, Cercopagidae) with notes on the morphol-
ogy and phylogeny of the order Onychopoda. Zoologica Scripta 24:61–90
Mellon, D., Jr. 1963. Electrical responses from dually innervated tactile receptors on the thorax of the
crayfish. Journal of Experimental Biology 40:137–148.
Meyer-Rochow, V.B. 1980. Cuticular surface structures in Glyptonotus antarcticus—a marine isopod from
the Ross Sea (Antarctica). Zoomorphologie 94:209 –216.
Mü ller, K.J., and D. Walossek. 1987. Morphology, ontogeny, and life habit of Agnostus pisiformis from the
upper Cambrian of Sweden. Fossils and Strata 19:1–124.
Mü ller, K.J., and D. Walossek. 1988. External morphology and larval development of the Upper Cambrian
maxillopod Bredocaris admirabilis. Fossils and Strata 23:1–70.
Mü ller, M., M. Olek , M. Giersig , and H. Schmitz. 2008. Micromechanical properties of consecutive lay-
ers in specialized insect cuticle: The gula of Pachnoda marginata (Coleoptera, Scarabaeidae) and
the infrared sensilla of Melanophila acuminata (Coleoptera, Buprestidae). Journal of Experimental
Biology 211:2576 –2583.
Nickell, L.A., J.A. Atkinson, and E.H. Pinn. 1998. Morphology of thalassinidean (Crustacea: Decapoda)
mouthparts and pereiopods in relation to feeding, ecology and grooming. Journal of Natural
History 32:733–761.
Nicol, E.A.T. 1932. The feeding habits of the Galatheidea. Journal of the Marine Biological Association
18:87–106.
Niederegger, S., and N.G. Stanislav. 2006. Friction and adhesion in the tarsal and metatarsal scopulae of
spiders. Journal of Comparative Physiology A 192:1223–1232.
Olesen, J. 2001. External morphology and larval development of Derocheilocaris remanei
Delamare-Deboutteville and Chappuis 1951 (Crustacea, Mystacocarida), with a comparison of
crustacean segmentation and tagmosis patterns. Biologiske Skrifter 53:1–59.
Paffenhöfer, G.A., and P.A. Loyd. 2000. Ultrastructure of cephalic appendage setae of marine planktonic
copepods. Marine Ecology Progress Series 203:171–180.
Pohle, G. 1989. Gill and embryo grooming in lithodid crabs: Comparative functional morphology based
on Lithodes maja . Pages 75–94 in B. Felgenhauer, L. Watling , and A.B. Thistle, editors. Functional
Praetorius, H., J. Frokiaer, S. Nielsen, and K. Spring. 2003. Bending of the primary cilium opens
Ca2+-sensitive intermediate-conductance K+ channels in MDCK cells. Journal of Membrane
Biology 191:193–200.
Reaka, M.L. 1975 . Molting in stomatopod crustaceans. 1. Stages of the molt cycle, setagenesis, and mor-
phology. Journal of Morphology 146:55–80.
R ützler, M., and L.J. Zweibel. 2005 . Molecular biology of insect olfaction recent progress and conceptual
models. Journal of Comparative Physiology A 191:777–790.
Schembri, P.J. 1982 . Functional morphology of the mouthparts and associated structures of Pagurus
rubricatus (Crustacea: Decapoda: Anomura) with special reference to feeding and grooming.
Schmidt, M., and C.D. Derby. 2005 . Non-olfactory chemoreceptors in asymmetric setae activate anten-
nular grooming behavior in the Caribbean spiny lobster Panulirus argus. Journal of Experimental
Biology 208:233–248.
Schmidt, M., and W. Gnatzy. 1984 . Are the funnel-canal organs the “campaniform sensilla” of the
shore crab Carcinus maenas (Decapoda: Crustacea)? II. Ultrastructure. Cell and Tissue Research
237:81–97.
Snow, P.J. 1973. Ultrastructure of the aesthetasc hairs of the littoral decapod, Paragrapsus gaimardii .
Zeitschrift fuer Zellforschung und Mikroskopische Anatomie 138:489 –502.
Stamhuis, E.J., B. Dauwe, and J.J. Videler. 1998. How to bite the dust: Morphology, motion pattern and
function of the feeding appendages of the deposit-feeding thalassinid shrimp Callianassa subterra-
nea. Marine Biology 132:43–58.
Stange, G., and S. Stowe. 1999. Carbon-dioxide sensing structures in terrestrial arthropods. Microscopy
Research and Technique 47:416 –427.
Steele, V.J., and D.H. Steele. 1999. Cellular organization and fine structure of type II microtrich sensilla
in gammaridean amphipods (Crustacea). Canadian Journal of Zoology 77:88 –107.
Steele, V.J., and D.H. Steele. 1997. Type II microtrich sensilla of amphipods: Variations in external
morphology and distribution patterns. Canadian Journal of Zoology 75:1155–1165.
Steinbrecht, R.A. 1997. Pore structure in insect olfactory sensilla: A review of data and concepts.
International Journal of Insect Morphology and Embryology 26:229 –245.
Steinbrecht, R.A. 1998. Bimodal thermo- and hygrosensitive sensilla. Pages 405–422 in F.W. Harrison and
M. Locket, editors, Insecta, Vol. 2B. Wiley-Liss, New York.
Steullet, P., H.S. Cate, and C.D. Derby. 2000a . A spatiotemporal wave of turnover and functional matura-
tion of olfactory receptor neurons in the spiny lobster Panulirus argus. Journal of Neuroscience
20:3282–3294.
Steullet, P., H.S. Cate, W.C. Michel, and C.D. Derby. 2000b. Functional units of a compound nose:
Aesthetasc sensilla house similar populations of olfactory receptor neurons on the crustacean
antennule. Journal of Comparative Neurology 418:270–280.
Steullet, P., and C.D. Derby. 1997. Coding of blend ratios of binary mixtures by olfactory neurons in the
Florida spiny lobster, Panulirus argus. Journal of Comparative Physiology A 180:123–135.
Talarico, G., J.G. Palacios-Vargas, M.F. Silva, and G. Alberti. 2006. Ultrastructure of tarsal sensilla
and other integumental structures of two Pseudocellus species (Ricinulei, Arachnida). Journal of
Morphology 267:441–463.
Tautz , J., M. Masters, B. Aicher, and H. Mark. 1981. A new type of water vibration receptor on the crayfish
antenna. Journal of Comparative Physiology A 144:533–541.
Tazaki, K. 1975 . Sensory units respond to osmotic stimuli in the antennae of the spiny lobster Panulirus
japonicus. Comparative Biochemistry and Physiology A 51:647–653.
Thomas, W.J. 1970. The setae of Austropotamobius pallipes (Crustacea: Astacidae). Journal of Zoology
160:91–142.
Thompson, H., and B.W. Ache. 1980. Threshold determination for olfactory receptors of the spiny lob-
ster. Marine Behaviour and Physiology 7:249 –260.
van der Ham, J.L., and B.E. Felgenhauer. 2008. Ultrastructure and functional morphology of glandular
setae and distal claws of cephalic appendages of Speleonectes tanumekes (Crustacea: Remipedia).
Vedel, J.P. 1985 . Cuticular mechanoreception in the antennal flagellum of the rock lobster Panulirus
vulgaris. Comparative Biochemistry and Physiology A 80:151–158.
Vedel, J.P., and F. Clarac. 1976. Hydrodynamic sensitivity by cuticular organs in the rock lobster Panulirus
vulgaris. Morphological and physiological aspects. Marine Behaviour and Physiology 3:235–251.
Voigt, R., and J. Atema. 1992. Tuning of chemoreceptor cells of the second antenna of American lobster
(Homarus americanus) with a comparison of four of its other chemoreceptor organs. Journal of
Comparative Physiology A 171:673–683.
Walossek , D. 1993. The upper Cambrian Rehbachiella and the phylogeny of Branchiopoda and Crustacea.
Fossils Strata 32:1–202.
Watling , L. 1989. A classification system for crustacean setae based on the homology concept. Pages 15–26
in B. Felgenhauer, L. Watling , and A.B. Thistle, editors. Functional morphology of feeding and
grooming. Balkema, Rotterdam.
Wiese, K. 1976. Mechanoreceptors for near-field water displacement in crayfish. Journal of
Neurophysiology 39:816 –833.
Ziegler, A., and H. Altner. 1995 . Are the numerous sensilla of terrestrial isopods hygroreceptors?
Ultrastructure of the dorsal tricorn sensilla of Porcellio scaber. Cell and Tissue Research 282:135–145.
The author has requested enhancement of the downloaded file. All in-text references underlined in blue are linked to publications
7
ANTENNULES AND ANTENNAE IN THE CRUSTACEA
Geoff Boxshall and Damià Jaume
Abstract
The remarkable diversity in form and function of the antennules and antennae of crustaceans
is reviewed. The basic form of the crustacean antennule is a single-axis segmented limb, but in
malacostracans it is typically biflagellate, and in remipedes it comprises a dorsal segmented axis
and ventral flagellum. The form of the antenna is also compared across the major crustacean
taxa. It is plesiomorphically biramous, with a multisegmented exopod and up to four-segmented
endopod; the segmentation of the protopodal part is variable.
The antennules are primarily sensory and form a major sensory interface with the envi-
ronment. The distribution patterns of chemosensors, mechanosensors, and bimodal ele-
ments along the antennules are compared across major taxa. The structure of selected
sensors is brief ly described, and their roles in feeding, mating, and predator detection
behavior are discussed. Crustaceans also use their antennules for such purposes as holding
food, grasping a mate, and attaching to a host or other substrate. Morphological adaptations
exhibited by these multifunctional limbs are described. Antennae are used for a wide range
of tasks. They often perform a sensory role but are used in swimming, attachment, feeding,
mating, brooding, and respiration. The manner in which this multifunctionality is ref lected
in morphology is outlined.
The balance among the different functional roles performed by antennules and anten-
nae changes during development. In crustaceans with planktotrophic nauplii, for example,
the antennal coxa bears one or two feeding endites that are subsequently lost during devel-
opment as the mandibular gnathobase takes over their function. The ontogenetic develop-
ment of both limbs is brief ly reviewed. The enhancement of the chemosensory array on the
antennules of males as they attain sexual maturity is found to be common to many different
crustacean groups.
199
ANTENNULES AND ANTENNAE IN THE CRUSTACEA
The spectacular adaptive radiation of crustaceans is reflected in the diversity of morphology,

behavior, and mode of life they exhibit. The traditional definition of a crustacean usually refers
to the possession of a mandible in combination with two pairs of antennae. This serves to dis-
tinguish them from chelicerates and fossil taxa such as trilobites, megacheirans, and marrel-
lomorphs, which lack mandibles, and from hexapods and myriapods, which have mandibles
but only a single pair of antennae. While in many different crustaceans the antennae provide
the primary sensory interface with the environment, they can also be involved in locomotion,
attachment, feeding, and mating behavior. The morphology of the antennae differs from group
to group, reflecting their different functional roles, and it can vary during development, as the
balance of functional roles changes from larva to adult. The patterns of antennal morphology
and their relationships are explored here.
ANTENNULES
The anteriormost paired limb on the head of arthropods goes by a variety of names: in crus-
taceans either antennule or first antenna is used, according to group or personal preference,
whereas in the other mandibulatan groups (hexapods and myriapods) and in the trilobites it
is most commonly referred to as the antenna. In modern chelicerates, the anteriormost limbs
on the prosoma are the paired chelicerae, which, on the basis of Hox gene expression patterns
(Telford and Thomas 1998, Damen et al. 1998), can be interpreted as positional homologues of
the antennules in these other arthropods (Akam 2000), but they are not considered here. In
some Paleozoic fossil arthropods of uncertain affinity, such as Leanchoilia superlata, the first
limb is simply termed the “great appendage” (Bruton and Whittington 1983). We use antennule
here for the anteriormost limb pair arising from the deuterocerebral somite of the head of crus-
taceans and their mandibulatan relatives (see Scholtz and Edgecombe 2005).
Structure
The typical arthropodan antennule comprises a single proximodistal axis composed of few to
multiple subdivisions, which have been referred to variously as antennulomeres, podomeres,
f lagellomeres, segments, articles, annuli, or annulations. The terminology for the subdivi-
sions is dependent upon their anatomy. An antennule is segmented if it consists of a linear
series of true segments, as defined by the presence of intrinsic muscles that insert or attach
at each intersegmental articulation. Each articulation is typically provided with a hoop of
arthrodial membrane that allows slight telescoping of the proximal rim of the more distal seg-
ment within the distal rim of the more proximal segment. Segmented antennules, therefore,
have segmentally arranged intrinsic musculature, typically along the entire length of the limb
(see Boxshall 2004).
The other type of single-axis antennule is f lagellate. At least two different types of f lagel-
late antennules are found within recent arthropods: those with terminal f lagella formed by
annulation of the distal segment, as in some collembolans, ectognathan insects, and mala-
costracan crustaceans, and those with nonterminal or intercalary annulations, such as scu-
tigeromorph centipedes and some crustacean larvae (see Boxshall 2004). Terminal f lagella
are by far the most common. Flagella are also composed of few to multiple external subdivi-
sions of the axis, but they lack intrinsic musculature. These subdivisions are referred to here
as annuli .
Antennules and Antennae in the Crustacea 201
Interpreting the nature of the antennules of fossil arthropods can be problematic since infor-
mation on intrinsic musculature is usually lacking. Without evidence derived from knowledge
of the internal anatomy, the subdivisions of the limb cannot be identified as either segments
or annuli, and descriptive terms such as antennulomeres should be used. Whether segmented
or flagellate, antennules are essentially modular in construction, and this modularity confers
important functional attributes, permitting, for example, the enhancement of a sensory array by
the addition of extra modules or by the specialization of individual modules.
Single-Axis Antennules
Single-axis antennules are found in the great majority of fossil arthropod taxa from the early
Paleozoic, as exemplified by the Cambrian arthropods of the Burgess and Maotianshan Shale
faunas. Single-axis, segmented antennules are found in the Myriapoda (with the exception of
the Pauropoda), in some basal Hexapoda (Diplura and Collembola only) (Imms 1939), and in
the Crustacea, with the exception of the Remipedia and the Malacostraca only (see Boxshall
et al. 2010).
In the Crustacea, the maximum number of segments expressed varies with taxon. In recent
Branchiopoda, the antennules are either one- or two-segmented, although the spinicauda-
tan Caenestheriella australis has a distal flagellar section comprising a linear series of lobes
that resemble segments (Boxshall 2004). Fossil branchiopods have more antennulary segments:
the Devonian lipostracan Lepidocaris has short, three-segmented antennules (Scourfield 1926,
1940), but in the Kazacharthra (fossil relatives of the Notostraca) up to 15 antennulomeres have
been reported in Almatium gusevi (McKenzie et al. 1991). In Cambrian branchiopods such as
Rehbachiella and Bredocaris, the antennules comprise a proximal zone of incomplete annuli and
a distal zone of cylindrical segments (Walossek 1993). The presence of proximal annuli is pos-
sibly indicative of intercalary annulation (sensu Boxshall 2004), but the absence of data on mus-
culature makes it impossible to interpret these fossils unequivocally.
In the Cephalocarida the single-axis antennule comprises only six segments in
Hutchinsoniella macracantha (Hessler 1964), and no segments are added during development
(Sanders 1963). In the Mystacocarida the maximum number of segments is eight (Hessler and
Sanders 1966), and this is constant throughout larval development in Derocheilocaris rema-
nei (Olesen 2001). In any extant copepod species, a maximum of 27 antennulary segments is
found, although Huys and Boxshall (1991) demonstrated that a total of 28 different segments
are expressed within the Copepoda as a whole. These multisegmented antennules are not flag-
ellate—all segments are primitively provided with intrinsic musculature (Fig. 7.1). Reductions
in antennulary segmentation are common across the Copepoda and are primarily a result of
failure of expression of intersegmental articulations during development rather than secondary
fusion of segments that were expressed earlier in ontogeny (Boxshall and Huys 1998).
The antennule of Myodocopa is a single axis with up to eight segments, as found in extant
forms and in fossil taxa from the Silurian (Siveter et al. 2003, 2007). Podocopan ostracods have
single-axis antennules, and a maximum of eight segments is expressed, although most recent
taxa have fewer (Maddox 2000). Developmental data indicate that reductions in segmentation
in adults result primarily from failures of expression of intersegmental articulations rather than
secondary fusions (Smith and Tsukagoshi 2005, Smith and Kamiya 2008). It has been suggested
that a reduced exopod, represented by a setose marginal expansion, is present in some podo-
copans (e.g., Kesling 1951, Rossetti and Martens 1996, Karanovic 2005), but a recent review of
developmental and other studies found no evidence to support this interpretation (Boxshall
et al. 2010).
Fig. 7.1.
Proximal part of the antennule of a female Euaugaptilus (Copepoda: Calanoida) showing intrinsic muscles
making intermediate attachments on the proximal rim of each segment. Modified from Boxshall (1985),
with permission from the Royal Society of London.
In the bivalved Cambrian phosphatocopines, the antennules are small and comprise a single
axis with a maximum of 13 irregular subdivisions (in Waldoria), referred to by Maas et al. (2003)
as annuli. Setae are present on the two or three distal annuli only, and the setation pattern does
not change during development.
Antennules of Thecostraca consist of a maximum of six expressed segments, as found in some
Ascothoracida. In adults the prehensile antennule terminates in a clawlike subchela mechanism
that secures attachment to the host. Developmental studies show that the ascothoracidan claw
originates on the fourth segment of the six-segmented naupliar antennule, with the distal two
segments becoming incorporated into the compound apical segment of the adult (Grygier 1984).
A total of eight different segments are therefore expressed during development. In the Cirripedia,
including the parasitic Rhizocephala, the antennules (Fig. 7.2) are short and four-segmented, but
the apical segment is offset at an angle to the main axis that terminates in the attachment disc
carried on the third segment. This disc is responsible for securing the larva to the substrate dur-
ing settlement. A standardized terminology for the segments and their setae was proposed by
Bielecki et al. (2009).
The antennule of the branchiuran fish lice comprises a two-segmented basal part armed with
curved, hooklike outgrowths and a two-segmented distal part, bearing setae (Rushton-Mellor
and Boxshall 1994). The Tantulocarida lack antennules in the tantulus larva stage (indeed, this
larva lacks all cephalic limbs), and in adult males the antennules are represented only by paired
clusters of aesthetascs arising anteriorly on the ventral surface of the cephalothorax (Boxshall
and Lincoln 1987). In the adult sexual female, a pair of unsegmented antennules is present (Huys
et al. 1993).
Double-Axis Antennules
Antennules with two proximodistal axes are found in adult malacostracans and remipedes.
The malacostracan antennule typically comprises a robust basal part, the peduncle, bearing two
multiannulate flagella. The antennulary peduncle in malacostracans is not homologous with
the protopod of the postantennulary biramous limb—there is no evidence that the crustacean
antennule is derived from a fundamentally biramous structure (Boxshall 2004). The peduncle
Fig. 7.2.
Scanning electron micrograph of distal segments (s2, s4) of antennule of cypris larva of Megabalanus rosea
(Thecostraca: Cirripedia) showing offset apical segment (s4) with complex setal armature, and attach-
ment disc (ad) on third segment. Photo courtesy of J. Høeg.
is the proximal segmented zone that contains intrinsic musculature and carries the flagella. It
can be two-, three-, or four-segmented and houses the flagellar flexor and extensor muscles that
insert inside the proximal rim of the basal annulus of each flagellum (Fig. 7.3). All malacostracan
antennules thus far investigated lack intrinsic musculature in the annulated flagellar parts. In
the terrestrial anomuran Birgus latro, the peduncle segments are long and slender, and the distal
flagella are relatively short.
This biflagellate antennule is an autapomorphy of the Malacostraca (Richter and Scholtz
2001, Jenner et al. 2009) and is present in the earliest unequivocal fossil malacostracan,
Cinerocaris magnifica, an archaeostracan phyllocarid from the Silurian (Briggs et al. 2003). The
two flagella are sometimes referred to as inner and outer rami (Richter and Scholtz 2001) or,
specifically, as exopod and endopod (e.g., Bruce 1986 for isopods, Clark et al. 1998 for decapods,
and Perrier et al. 2006 for palaeocarid syncarids), but this terminology is inappropriate (see
review in Boxshall et al. 2010). The flagella are also referred to as outer and inner (Jaume and
Bréhier 2005), as medial and lateral (e.g., Goldman and Patek 2002, Reidenbach et al. 2008),
or as primary and accessory (Jaume et al. 2006). The terms primary and accessory flagella are
used here.
The biflagellate antennule comprises a laterally located primary flagellum, the annuli of
which each typically carry one or two rows of aesthetascs, and an accessory flagellum. The
more medially positioned accessory flagellum can be as long as or longer than the primary
flagellum, but it never carries aesthetascs and typically appears later in development than the
pd1
pd2
pd3
pf
af
Fig. 7.3.
Antennule of the male of Montucaris (Peracarida: Bochusacea) showing intrinsic musculature within
three-segmented peduncle (pd1–pd3) and inserting on the proximal rim of an accessory flagellum (af). No
musculature is observed going to the base of the primary flagellum (pf) in the male. Modified from Jaume
et al. (2006), with permission from Blackwell Publishing.
primary flagellum. Given the presence of aesthetascs only on the primary flagellum, we infer
that it is homologous with the dorsal axis in remipedes and with the sole axis in other nonmala-
costracans. Most malacostracans, including the anaspidacean and palaeocaridacean Syncarida,
Euphausiacea, Amphionidacea, Decapoda, and members of the peracaridan groups Mysidacea,
Lophogastrida, Cumacea, and Spelaeogriphacea, primitively have two multiannulate flagella.
Both flagella can be reduced; in the Mictacea and Bochusacea, for example, both consist of just
a few annuli. The accessory flagellum is reduced and often absent in isopods, amphipods, and
tanaidaceans. In oniscoidean isopods, perhaps as an adaptation to a terrestrial mode of life, the
entire antennule can be reduced to one to three subdivisions, with subsequent loss of clear sepa-
ration between the peduncle and flagellum (Vandel 1960). In the cirolanid isopod Bathynomus
giganteus, the “scale” carried on the third antennulary segment has been interpreted as repre-
senting the reduced accessory flagellum, as indicated by the retained cluster of setal elements at
its tip (Brusca and Wilson 1991).
In the Leptostraca, the antennule consists of a three-segmented peduncle bearing a flagel-
lum and an articulated scale. The externally located scale of the Leptostraca was interpreted
by Richter and Scholtz (2001) as the “outer ramus” (presumably the homologue of the later-
ally located primary flagellum). It is probably independently derived within the Phyllocarida,
since the archaeostracan phyllocarid Cinerocaris magnifica carries two long antennulary flagella
dx
vf
Fig. 7.4.
Antennule of Speleonectes (Remipedia) with details showing musculature within protopodal part extend-
ing into segmented dorsal axis (dx) and inserting on proximal rim of annulate ventral flagella (vf).
Modified from Boxshall (2004), with permission from Wiley and Sons, Ltd.
(Briggs et al. 2003). We consider that the leptostracan outer scale is derived from the accessory
flagellum despite its lateral origin. The evidence supporting this inference is the relatively late
appearance of the scale after the main axis (the primary flagellum) during development (Olesen
and Waloßek 2000) and the absence of aesthetascs, which are found only on the primary flagel-
lum. In the Bathynellacea there is an antennulary scale carried internally, and it has been inter-
preted as a rudiment of the accessory flagellum (Siewing 1959, Richter and Scholtz 2001, as the
“inner ramus”).
When first discovered, the Remipedia were described as having biramous antennules
(Yager 1981), but Boxshall (2004) revealed that the dorsal branch is the primary axis consist-
ing of segments defined by intrinsic muscles, and the ventral branch lacks intrinsic muscula-
ture and is weakly annulated (Fig. 7.4). The ventral branch is not segmented and should not
have been interpreted as a ramus: it is a flagellum. During development the primary axis only
is present in the metanaupliar phase, and the ventral flagellum first appears in the postlarva,
initially as a single “segment” lacking annulations (Koenemann et al. 2007). The remipede
antennule therefore comprises the segmented primary axis typical of other Crustacea such
as the Cephalocarida and Copepoda plus a ventral flagellum and differs from the biflagellate
antennule of malacostracans. The common basal part of the remipede antennule is referred to
as the peduncle. It is not homologous with the protopod of a biramous limb because, as for the
Malacostraca, there is no evidence that the crustacean antennule is derived from a biramous
limb (Boxshall 2004).
Multiple-Axis Antennules
A triflagellate antennule occurs in the Stomatopoda and in their Paleozoic relatives belong-
ing to the hoplocaridan orders Aeschronectida and Palaeostomatopoda (Schram 1986). The
triflagellate condition of the stomatopod antennule is an autapomorphy (Richter and Scholtz
2001). In stomatopods the ventrally located accessory flagellum is subdivided into two subflag-
ella (Kunze 1983), but only the primary flagellum carries aesthetascs (Mead and Koehl 2000),
as in other malacostracans.
A B C
af
pf
pf
pf
pd pd pd
Fig. 7.5.
Development of antennule of Pleoticus muelleri (Decapoda) showing single-axis state in protozea I stage
(A) and protozoea III stage (B), consisting of peduncle (pd) and primary flagellum (pf), and biflagellate
condition of mysis II stage (C), after first appearance of accessory flagellum (af) at mysis I stage. Redrawn
from de Calazans (1992).
Within the Caridea (Decapoda), some representatives of at least three families (Palaemonidae,
Alpheidae, and Hippolytidae) also have the accessory flagellum divided to form two subflagella
(see Bacescu 1967). Given current estimates of relationships, we infer that this condition has
arisen independently in the Caridea, probably more than once.
Development
Studies on postembryonic development of crustaceans provide additional evidence support-

ing the secondary derivation of the bif lagellate antennule (e.g., Scholtz 2000, Gruner and
Scholtz 2004, Koenemann et al. 2007). The orthonauplius represents a primordial phylo-
typic stage for the Crustacea, and the naupliar antennule always comprises a single primary
axis (Fig. 7.5A,B). Any additional f lagellar structures present in malacostracans (e.g., the
accessory f lagellum) and remipedes (the ventral f lagellum) develop at a subsequent, post-
naupliar stage (Fig. 7.5C).
In segmented antennules, development follows a distal-to-proximal pattern. Articulations
separating the more distal segments are typically expressed earlier than those separating the
more proximal ones, and segmental setation is typically complete earlier on more distally
located segments than on proximal ones (Boxshall and Huys 1998, Smith and Tsukagoshi
2005). The ground-plan development pattern from nauplius to adult was modeled by Boxshall
and Huys (1998) for a hypothetical ancestral copepod (Fig. 7.6). The metamorphic molt from
I V X XV XX XXV
N VI
CoI
CoII
CoIII
CoIV
CoV
Fig. 7.6.
Schematic showing hypothetical development of segmentation and setation through the copepodid stages
of Copepoda. The scale at the top indicates the presumed 28 segments of the ancestral copepod. Setae are
shown as lines, and aesthetascs, as solid elements. A segment carrying a seta not present at the preceding
stage is shaded with vertical stripes if the newly added seta is anterodistal or with stippling if the new seta
is anteroproximal. The basal segment is shown with horizontal stripes when its second and third setae
appear. Aesthetascs are shown stippled when they first appear, and then in black. Abbreviations: CoI–
CoV, copepodid stages I–V; F, female; NVI, nauplius VI stage. Adapted from Boxshall and Huys (1998)
with permission from the Royal Society of London.
the sixth and final nauplius stage to the first copepodid stage was marked by the subdivision of
the apical segment of the nauplius to form the distal eight segments of the adult antennule. No
further divisions occur in this distal section of the antennule throughout the five copepodid-
phase molts to adult. During the copepodid phase, the two proximal antennulary segments of
the nauplius undergo a sequence of subdivisions to form segments 1–20 of the adult. Antennules
with fewer expressed segments are envisaged as being generated by early cessation of the proc-
ess of subdivision (Boxshall and Huys 1998, Schutze et al. 2000), a pedomorphic process.
Proximal annulation is expressed transiently during the naupliar phase of development of
some podoplean copepods but is lost by the first copepodid stage (e.g., Dahms 1992). The pro-
tozoeal larvae of penaeid decapods similarly exhibit transient annuli in the proximal part of
the antennule (Fig. 7.5A), which are lost by the end of the zoeal phase. The proximal annulated
part of the antennule of Rehbachiella and Bredocaris may be interpreted as additional evidence
of their larval status but may also indicate that a proximal annulated zone is plesiomorphic for
the Crustacea.
In decapod malacostracans such as Panulirus argus and Cherax destructor, the primary
antennulary flagellum develops by the production of new annuli at the base of the flagellum,
in a meristematic zone (Sandeman and Sandeman 1996, Steullet et al. 2000). In both species
subdivision takes place in annuli distal to the basal meristematic annulus. Few details are avail-
able but the basic process seems similar to that described for the antennal flagellum in isopods
(see “Development,” below).
ANTENNAE
The second limb in arthropods, the one immediately posterior to the antennule, has two main
names: in Crustacea, it is the second antenna or just antenna; in Chelicerata, it is the pedipalp. We
use the term antenna here. In Hexapoda and Myriapoda this limb is missing; its absence serv-
ing as a diagnostic character of the taxon Atelocerata (Heymons 1901). However, the antennal
segment is represented by the limbless intercalary segment. The expression pattern of the gene
engrailed in the epidermal and neural cells of hexapods unequivocally marks the intercalary seg-
ment, and its existence is further supported by the expression pattern of the Hox gene labial in
insects (Diederich et al. 1989, Peterson et al. 1999).
The Silurian arthropod Tanazios was described by Siveter et al. (2007) as a possible
stem-lineage crustacean. Boxshall (2007) reinterpreted the antenna of Tanazios as missing in
the adult—its absence is indicated by the marked gap in the limb series between the antennule
and the mandible. He concluded that the lack of differentiation in the postmandibular limbs of
Tanazios excludes it from the Eucrustacea. Boxshall (2007, 322) considered the lack of anten-
nae in a Silurian marine arthropod to be “of immense significance both to our understanding
of deep mandibulate phylogeny, and to the emerging, but as yet unstable, picture of hexapod
origins within the Pancrustacea.”
Structure
The basic postantennulary limb of arthropods is widely regarded to be biramous (see Walossek
1993, Hou and Bergström 1997, Boxshall 2004), comprising a proximal stem, the protopod, bear-
ing an inner endopod and outer exopod. These rami are major limb axes and are carried dis-
tally on the protopod. They are plesiomorphically supplied with intrinsic muscles originating
within the protopod and are commonly segmented. The antenna of crustaceans is plesiomor-
phically biramous: the protopod is two-segmented, comprising coxa and basis; the exopod is
usually multisegmented, and the endopod typically comprises only four expressed segments. In
malacostracans the protopod may be three-segmented (Fig. 7.7), but there is no evidence for the
existence of a precoxa in the antenna of cephalocaridans, remipedes, branchiopods, copepods,
mystacocaridans, podocopan ostracods, myodocopans, or branchiurans. The Tantulocarida
lack antennae at all stages of the described life cycle (Huys et al. 1993). The nonfeeding plank-
tonic adults of monstrilloid copepods lack all cephalothoracic limbs from antennae to maxil-
lipeds, inclusive. The infective nauplius phase, however, has biramous antennae with a setose,
natatory exopod and an endopod that carries a terminal clawlike seta (Grygier and Ohtsuka
1995). The antennal endopod together with the clawed mandible are used to grasp the host sur-
face during infection.
The antenna of Cambrian phosphatocopines is biramous: the protopod is unsegmented or
subdivided into coxa and basis, the endopod is two- or three-segmented, and the exopod is
described as multiannulate (Maas et al. 2003). When undivided, the protopod forms an entire
gnathobase; when divided, both coxa and basis are drawn out medially into a spine-bearing
endite (Siveter at al. 2001). The number of “annuli” in the exopod ranges from about 8 up to 24,
and these typically carry a single seta each, with two at the apex (Maas et al. 2003).
In the Anostraca, the antennae exhibit extreme sexual dimorphism. In adult males they may
be modified as enormous grasping structures, often with species-specific basal outgrowths
A B
en3
en2
ex
en1 en3
pr3
pr2
pr1
en2
pr1
en1
pr3
pr2
Fig. 7.7.
(A) Biramous antenna of Hemimysis (Peracarida: Mysidacea) showing intrinsic musculature within
three-segmented protopod (pr1–pr3), within the proximal three endopodal segments (en1–en3) insert-
ing on the proximal rim of the endopodal flagellum and within the exopod (ex). (B) Uniramous antenna
of Typhlocirolana (Peracarida: Isopoda) showing intrinsic musculature within three-segmented proto-
pod (pr1–pr3) and proximal three endopodal segments (en1–en3), inserting on the proximal rim of the
endopodal flagellum. The exopod is absent.
and elaborate ornamentation, whereas in females they are typically smaller and simpler in
construction (Linder 1941). In conchostracan branchiopods the antenna is biramous, and
both of the large rami appear to be f lagellate, but both exopod and endopod comprise numer-
ous segments as defined by the presence of intrinsic muscles (Shakori 1968, Boxshall 2004).
The multisegmented nature of the endopod was interpreted as secondarily derived within
the Conchostraca by Boxshall (2004). In cladocerans the number of exopodal and endopo-
dal segments does not exceed three in Anomopoda, Onychopoda, and Ctenopoda or four in
Haplopoda and the fossil order Cryptopoda. In Holopedium , the antenna is uniramous due to
loss of the endopod.
The cephalocaridan antenna is biramous, comprising a protopod divided into coxa and basis,
a short two-segmented endopod, and a well-developed, multisegmented exopod (Sanders 1963).
The number of exopodal segments and associated setal elements increases during ontogeny;
Hutchinsoniella, for example, has 13 segments bearing 15 setae at the metanauplius stage, rising
to 19 and about 70 setae in the adult (Elofsson and Hessler 1991). The setae are structurally simi-
lar, with the lumen of each containing 6–12 unbranched outer dendritic segments surrounded
by two layers of sheath cells. All the setae were interpreted as chemosensors by Elofsson and
Hessler (1991), who remarked on the lack of mechanoreceptors, not having found scolopale bod-
ies associated with any of the setal sensory cells (see chapter 6).
In mystacocarids, cirripedes, and copepods, the antenna is typically biramous, comprising

coxa and basis, which bears the exopod and endopod. The endopod is apparently six-segmented
in mystacocarids, but in copepods it is typically only three-segmented, although traces of an
ancestral four-segmented condition are retained in some basal calanoids (Huys and Boxshall
1991). It is only two-segmented in cirripede nauplii. The exopod has at most nine segments
in mystacocarids and cirripede nauplii and ten segments in copepods. However, within the
Thecostraca, ascothoracid metanauplii have antennal exopods of 12 or more segments (Boxshall
and Böttger-Schnack 1988).
In malacostracans the protopod has typically been regarded as two-segmented, comprising
coxa and basis, but we find in Tulumella (Thermosbaenacea), Hemimysis (Fig. 7.7A), Stygiomysis
(Mysidacea), and Typhlocirolana (Isopoda) (Fig. 7.7B) that the protopod is three-segmented.
The coxa articulates proximally with a precoxa that may have been interpreted as a pedestal, but
the presence of muscles inserting at this joint indicates that it is a segment. The antennal endo-
pod in malacostracans is well developed, consisting of up to three defined segments proximally,
plus a terminal flagellum representing a subdivided fourth segment. The proximal endopodal
segments are usually referred to as peduncle segments, so the six-segmented peduncle of some
peracaridans comprises a combination of three protopodal and three endopodal segments (Fig.
7.7), whereas in other peracaridans and euphausiaceans the peduncle is five-segmented, consist-
ing of two protopodal and three endopodal segments. Muscles are present only in the peduncle
segments (Fig. 7.7). In the syncarid Anaspides the peduncle is only four-segmented, comprising
coxa, basis, and two defined endopodal segments plus the flagellum.
In leptostracans the exopodal scale is absent, and the antenna is uniramous, but in the
archaeostracan phyllocarid Cinerocaris the antenna is biramous with two slender flagellate rami
(Briggs et al. 2003). In eumalacostracans the exopod is reduced to a scale, although in stomato-
pods the scale has a well-defined proximal segment (Schram and Hof 1998). The exopodal scale,
also referred to as the scaphocerite, is greatly enlarged in the Amphionidacea and in decapod
shrimps but can be reduced or lost in anomurans and brachyurans. In asellote isopods and in
the thermosbaenacean Tulumella, there is also a scalelike exopod, but other members of these
orders, as well as members of the Cumacea and Amphipoda, have uniramous antennae lack-
ing any trace of the exopod (Fig. 7.7B). The flattened, platelike antenna of scyllarid lobsters is
derived from the flagellum, not from the exopodal scale.
Extreme development of the antennal flagellum is exhibited in penaeidean decapods, in which
it can attain a total length more than three times that of the body. In these penaeideans, the flagel-
lum comprises a relatively rigid proximal section and a long whiplike distal section, separated by
a flexure zone. During normal swimming, the proximal section is held out from the body, and the
flexible distal part trails out parallel to and at a distance from the animal (Foxton 1969). Distal
to the flexure zone, each annulus typically carries a pair of arched, plumose setae that together
effectively form a tube running the entire length of the distal section. Within this “tube” a linear
array of finely plumose setae can be present, although there is not necessarily one per annulus.
This system allows the detection of near-field vibrating sources and can indicate the direction of
the source because the near-field effect attenuates rapidly (i.e., along the length of the flagellum)
(Denton and Gray 1986).
The stiffness of the flagellum is nonuniform. In Cherax destructor, the flagellum is tapered
and consists of 220–250 annuli that increase in length and decrease in diameter toward the tip
(Sandeman 1989). The flagellum is oval in cross section and exerts the greatest mechanical
resistance against medial deflection and the lowest against dorsal deflection. Medial mechani-
cal resistance decreases markedly toward the tip. When bent passively, curvature is confined to
a small part of the flagellum, but with increasing force, the apex of the bend moves toward the
base. Sensing curvature at several locations along the flagellum is likely to provide sufficient
information to enable the crayfish to distinguish whether the bending is caused by the flow
fields in the surrounding medium or by physical contact with an obstacle (Barnes et al. 2001).
Development
During the early naupliar phase, the antenna bears one or two feeding endites, referred to as
the naupliar or antennal processes , on the proximal segment (the coxa) of the two-segmented
protopod. These naupliar processes are found in copepods, mystacocarids (Fig. 7.8A),
cephalocarids (Fig. 7.8B), and branchiopods—taxa that retain nonlecithotrophic nauplii.
They decrease in size during later development and are lost at or before the molt to the post-
naupliar phase.
In dendrobranchiate decapods, the antenna of the naupliar and protozoeal phases has a mul-
tisegmented exopod that gradually ceases to express segmentation during development until,
by the megalope phase (= mysis I stage), the exopod has transformed into the unsegmented
antennal scale (Fig. 7.9) so characteristic of the adult caridoid facies (Hessler 1983). This transi-
tion from segmented naupliar ramus to unsegmented scale is unique to these malacostracans. It
is accompanied by a change in form of the endopod, from a two-segmented ramus (Fig. 7.9A) to
an annulate flagellum (Fig. 7.9C).
A B
np
np
Fig. 7.8.
(A) Antenna of first stage metanauplius of Derocheilocaris (Mystacocarida) showing large feeding nau-
pliar processes (np) on coxa (redrawn from Hessler and Sanders 1966). (B) Antenna of first stage nau-
plius of Hutchinsoniella (Cephalocarida) showing developing naupliar process on coxa (redrawn from
Sanders 1963).
A B C
en en en
ex ex ex
Fig. 7.9.
Developmental of the antenna of Pleoticus muelleri (Decapoda) showing transition in form of exopod (ex)
and endopod (en) from protozoea III stage (A) to mysis I stage (B), and megalopa stage (C). Redrawn from
de Calazans (1992).
The isopod Asellus aquaticus is a useful model for the development of the endopodal flagel-
lum, which consists of a single segment divided into annuli that are devoid of intrinsic muscu-
lature (Wege 1911). The antennal flagellum comprises a proximal meristematic region, a central
region composed of quartets (sets of four annuli, each having a specific arrangement of setae),
and an apical complex consisting of the apical annulus plus the four preceding annuli with spe-
cific setal patterns. The number of quartets in the central region is variable in Asellus aquaticus
since this species never ceases molting and continues to add annuli throughout life (Maruzzo
et al. 2007). The proximal meristematic annulus divides into a copy of itself (the meristem) and
a distal annulus that is effectively an incomplete quartet and divides following a set pattern to
produce the complete quartet.
SENSORS
In most crustaceans, the antennules are primarily sensory in function and carry rich arrays
of sensory receptors that play a role in almost every aspect of their behavior. The main setal
receptor types can be defined by their sensory modality, and although the sensitivity and func-
tional responses of most setal elements have not been experimentally investigated, compara-
tive studies allow for putative functions to be inferred. Setal elements with a sensory function
are commonly referred to as sensilla (see Hallberg and Skog 2011), but the terminology has not
yet stabilized (see chapter 6). In some taxa, such as copepods, aesthetascs are regarded as dis-
tinct from setae rather than as a setal subtype.
Various terminologies are employed to discuss crustacean sensory modalities, and this can
generate confusion. Chemosensors that mediate perception of a remote chemical are referred
to as olfactory. Olfaction (sense of smell) is distance chemoreception and usually involves the
detection of a gradient of chemical entrained within a plume originating at its source, such
as a pheromone produced by congeneric females or amino acids originating from food items.
Chemosensors that mediate perception of a chemical stimulus at extremely close range, or
when in direct physical contact, are often referred to as gustatory or taste receptors. This is con-
tact chemoreception (Atema 1977). Distance and contact chemoreceptors represent extremes
in sensitivity along a continuous spectrum, so the separation is somewhat artificial although

widely adopted (see Hallberg and Skog 2011).
There is a similar functional division in mechanoreceptors. Mechanosensors that mediate
remote perception of hydrodynamic signals, such as disturbances in flow fields caused by par-
ticles suspended in the water column or by the swimming motions of a live prey, are distance
mechanosensors. Sensors that detect the presence of objects only when they come into direct
physical contact with a surface are tactile sensors. Again, distance and tactile sensors repre-
sent extremes in sensitivity along a continuous spectrum of mechanosensors. Displacement of a
mechanosensory setal shaft in its socket or the bending of a seta in direct contact with an object
can both constitute a stimulus.
The Aesthetasc
Aesthetascs are the most studied crustacean chemosensor. They are typically elongate, thin-
walled, cylindrical elements (Fig. 7.10), which lack internal enveloping cells in their outer part
(Hallberg and Skog 2011). They are innervated by sensory cells that vary in number from a few to
hundreds, for example, 400 in Pagurus hirsutiusculus (Ghiradella et al. 1968a). The sensory cells
are surrounded by enveloping cells basally. They have dendrites from which cilia emerge, usu-
ally two cilia in malacostracans, sometimes only one, sometimes more. The cilia typically, but
not always, branch dichotomously and repeatedly to form a dense mass of outer branches called
outer dendritic segments (Laverack 1964, Hallberg et al. 1992). Gr ü nert and Ache (1988) reported
8,000–10,000 such outer dendritic segments per aesthetasc in Panulirus argus.
Aesthetascs’ function as a chemoreceptor has been confirmed experimentally by direct neu-
rophysiological studies in various decapod malacostracans (Anderson and Ache 1985, Michel
et al. 1993, Steullet et al. 2000). The permeability of the thin cuticle allows water-borne com-
pounds to enter over the entire surface area, but the cuticle remains sufficiently impermeable to
prevent loss of physiologically important molecules (Derby et al. 1997).
The aesthetasc can vary in external form: curved aesthetascs can be found, for example, in
some isopods (Ka ï m-Malka et al. 1999) and some cavernicolous copepods (Boxshall and Jaume
2000). They vary in size with taxa: body size is a factor influencing aesthetasc length. Aesthetascs
in Cancer productus can attain a length of >1700 μ m, one of the longest in the Crustacea, whereas
those of small cladocerans or interstitial copepods may reach only 10–12 μ m in length (Hallberg
et al. 1992, Boxshall et al. 1993). Aesthetascs increase in size during development in the stomat-
opod Gonodactylus mutatus (Mead 2002). As well as varying in size with species, aesthetascs
can be sexually dimorphic, with males carrying larger aesthetascs than conspecific females
(Boxshall and Huys 1998).
Terrestrial crustaceans retain functional aesthetascs (Ghiradella et al. 1968b). In the robber
crab Birgus latro, the antennules consist of an elongate, three-segmented peduncle bearing two
short distal flagella, and the aesthetascs are arrayed in rows across the central groove of the pri-
mary flagellum. They differ from those of aquatic relatives in being relatively short and blunt.
In addition, they have an asymmetric profile, with the side nearest the surface of the annulus
being thickened and the exposed surface being thin and wrinkled (Stensmyr et al. 2005). The
thickened surface and flattened profile presumably enhance the rigidity of the aesthetasc out
of water.
The arrangement of aesthetascs on the antennule varies but is normally taxon specific and
relatively highly conserved within a higher taxon. Cephalocarids, for example, carry just a sin-
gle terminal aesthetasc. In adult Hutchinsoniella the aesthetasc is located in a terminal tuft,
together with 11 other setae, and a further 11 setae are distributed over the more proximal seg-
ments (Elofsson and Hessler 1991). In anostracan and cladoceran branchiopods the aesthetascs
ae
ods
cut
isc
osc
ods
bb
osc
ids
isc isc
Fig. 7.10.
Fine structure of typical malacostracan aesthetasc. The aesthetasc (ae) has a short stalk attached to the
cuticle (cut), and its lumen is filled with a mass of branching outer dendritic segments (ods), which arise
from inner dendritic segments (ids) within the antennule. Just proximal to the origin of the outer dendritic
segments are the 9 × 2 + 0 ciliary basal bodies (bb). The array of dendritic segments is sheathed with mul-
tiple layers formed by inner (isc) and outer (osc) sheath cells. Schematic shown with reduced numbers of
components, there are multiple dendrites and a variable number of sheath cells. Adapted from Heimann
(1984), with permission from Springer.
are typically found in a tuft on the apex of the antennule, whereas in the Notostraca and most
Spinicaudata they are arrayed along the margin (Martin 1992). In mystacocarids, there is a
single aesthetasc located subterminally on the apical segment (Olesen 2001). The sensory
tubes described from the antennules of the myodocopan Conchoecia spinirostris are probably
aesthetascs, although they differ from the typical decapod aesthetasc (Heimann 1979). In the
remipede Speleonectes tanumekes the antennule carries several dozen aesthetascs arranged in
parallel rows on the peduncle (van der Ham and Felgenhauer 2006).
In planktonic copepods, Giesbrecht (1893) observed that, with the exception of the basal and
a few distal segments, all antennule segments carry a trithek of setal elements (one aesthetasc
and two setae). Traces of this pattern can be identified in all copepods, whether planktonic, ben-
thic, or parasitic (Huys and Boxshall 1991). Giesbrecht also noted that males in some calanoid
families possess two aesthetascs per segment, giving a quadrithek arrangement (two setae plus
two aesthetascs) compared with the trithek of the female. Quadritheks occur on one or more
segments of the male antennules in many calanoids (Huys and Boxshall 1991). In its extreme
form, double aesthetascs are present along almost the entire length of the male antennules
(from segments II to XXIV in Eucalanus attenuatus), whereas in other calanoid families they are
restricted to the proximal part of the antennule.
In malacostracans aesthetascs are found only on the primary (= lateral) flagellum. They are
typically aligned in regular rows, either one or two rows per annulus, and the number of aes-
thetascs per row varies with taxon (Table 7.1). The rows may be distributed along the length of
the flagellum or restricted to the more proximal part. In some amphipods, the proximal annuli
are completely or partially fused and bear multiple transverse rows of aesthetascs, forming an
organ referred to as the callynophore by Lowry (1986). Similarly, in the isopod Idotea baltica,
aesthetascs are carried in six or seven rows on the distal antennulary “segment” (Guse 1983), but
this is undoubtedly a compound unit representing several annuli that failed to separate during
Table 7.1. Arrangement of aesthetascs on the primary flagellum of malacostracans.
Higher taxon Species No. rows per No. aes- Reference

annulus thetascs per
row
Stomatopoda Gonodactylus 1 3 Mead 2002
mutatus
Decapoda Panulirus argus 2 8–12 Daniel et al.
2008
Decapoda Orconectes virilis 2 3–4 Mead 2008
Decapoda Homarus 2 ~12 Derby 1982
americanus
Decapoda Typhlatya arfeae 1 1–3 Jaume and
Bréhier 2005
Decapoda Lysmata boggessi 2 4–5 Zhang et al.
2008
Decapoda Birgus latro 2 ~12–14 Stensmyr
et al. 2005
Lophogastrida Lophogaster 2 1–2 (30–40 in Johansson
typicus males) et al. 1996
Isopoda Bathynomus pelor 1 4–5 Thomson
et al. 2009
Isopoda Natatolana 1 10 Ka ï m-Malka
borealis et al. 1999
Isopoda Asellus aquaticus 1 1 Heimann 1984
Isopoda Idotea baltica — 2 Guse 1983
Amphipoda Metacrangonyx 1 1–2 Jaume and
dominicanus Christenson
2001
Amphipoda Bathymedon 2 4–5 Jaume et al.
longirostris 1998
development. Fusion of proximal annuli and subsequent concentration of aesthetasc rows occur
elsewhere in eucaridan and peracaridan malacostracans. In the Brachyura, the aesthetascs are
arrayed in a dense tuft on the ventral surface at the tip of the flagellum.
The fine scale arrangement of aesthetascs, such as the precise angle at which they are carried
relative to the segment, can have functional significance (Mead and Weatherby 2002, Thomson
et al. 2009). The guard setae located on either side of the aesthetasc rows in Panulirus argus have
a dual function: protecting the array from damage and conditioning the flow to allow for the
correct leakiness during a flick and return sequence (Reidenbach et al. 2008).
Unimodal Nonaesthetasc Chemosensors
Several different morphologies of nonaesthetasc chemosensory setae are found in the

Crustacea (Hallberg and Skog 2011). The presence of a terminal pore on a setal element is
often taken as an indication of a chemoreceptive function. Such setae often have their outer
dendritic segments shielded by a dendritic sheath of enveloping cells, so their sensory surfaces
are exposed only near the tip. This setal type probably functions as a contact chemoreceptor.
Several are present on the antennule of the cirripede cyprid larva (see Bielecki et al. 2009) that
carry a single terminal setal element (TS-D in terminology of Bielecki et al. 2009) identified
as an aesthetasc on the basis of external morphology. However, at least in Megabalanus rosa ,
seta TS-D has a terminal pore, which is typically absent from true aesthetascs, and Bielecki
et al. (2009) preferred to call it “aesthetasc-like.” Its inferred function was detection of water-
borne chemicals along its entire length.
The setae on the cephalocaridan antennule all share a similar structure: each contains an
outer dendritic segment that arises from a single ciliary body (9 × 2 + 0 microtubule pattern),
which in turn arises from a basal body connected to the sensory cell via the inner dendritic
segment. All the setae lack scolopale bodies and display features suggesting chemoreception
(Elofsson and Hessler 1991).
In two superfamilies of Podocopa (Cypridoidea and Pontocypridoidea), a modified seta
known as “aesthetasc Y” is carried on the first endopodal segment of the antenna. Its internal
structure was studied in detail by Andersson (1975), who inferred that it is a chemoreceptor.
Kaji and Tsukagoshi (2008) compared the development and structure of “aesthetasc Y” and the
linear array of so-called grouped setae located in a similar position on the first endopodal seg-
ment on five other ostracod superfamilies. They suggested that “aesthetasc Y” is derived from
grouped setae.
In cypridoidean ostracods, the Wouters organ is found on the dorsal surface of the first
antennulary segment, and the Rome organ is found on the ventral side of the second moveable
segment of the antennule in cypridoideans (Smith and Matzke-Karasz 2008). Both the Rome
and Wouters organs vary in form from buttonlike to tubular and may be derived from setae.
They were presumed to be chemosensors by Smith and Matzke-Karasz (2008).
Unimodal Mechanosensors
Mechanosensory setae are rigid structures with relatively thick cuticles, and in copepods each
is usually innervated by two dendrites, sometimes only one (Gresty et al. 1993a). The struc-
ture and innervation of the mechanosensory seta of Pleuromamma xiphias (Fig. 7.11), a calanoid
copepod, was described in detail by Weatherby and Lenz (2000). A pair of long dendritic proc-
esses extends from the paired sensory cell bodies (the somata), located in the antennule itself,
to the seta. Distal to each soma, the basal body is located within the dendrite about at the level
where the scolopale begins. The scolopale tube extends almost to the socket at the base of the
se cut
ods
isc
osc
tsc
mt tsc
bb
ac
scc
ids
scb
ax
Fig. 7.11.
Schematic of typical copepod mechanosensory seta. The seta (se) articulates basally with the cuticle (cut).
It is innervated by a pair of mechanosensory dendrites which pass from the cell bodies, through the tubular
scolopale (tsc) contained within the scolopale cell (scc) sensory cell body (scb) before entering the base
of the seta and inserting on its inner wall. The whole structure is enclosed by inner (isc) and outer (osc)
sheath cells and is anchored to the cuticle by microtubules (mt) within the anchor cell (ac). At the level
where the dendrite enters the scolopale are the 9 × 2 + 0 ciliary basal bodies (bb), marking the division
of the dendrite into inner (ids) and outer segments (ods). The nerve cell connects to the central nervous
system via an axon (ax). Adapted from Weatherby and Lenz (2000), with permission from Elsevier.
setal shaft. More distal dendrites become densely packed with a regular array of proliferating
microtubules. Distally the microtubule array and surrounding dendrites bend and enter the
lumen of the seta, inside which the dendrites are enveloped by inner and outer sheath cells. The
dendrites and their microtubules terminate at attachments to the setal cuticle.
The scolopale cell is typical of arthropodan mechanosensors, and many of the cuticular
setae in decapods are scolopidial in structure (Ball and Cowan 1977). The copepod mech-
anoreceptor described above (from Weatherby and Lenz 2000) differs from a typical scolo-
pidial organ, which is characterized by the possession of a ciliary body with very large rootlets.
These are in close contact with the dendritic membrane that itself makes desmosomal con-
nections to the scolopale, firmly anchoring it to the scolopale (Schmidt and Gnatzy 1984). In
Pleuromamma , dendrite anchoring appears to occur by the tight fit of the microtubule-packed
dendrites within the tubular scolopale. In many crustaceans there is an extracellular den-
dritic sheath or cap that ensheathes the distal dendrites (Guse 1978), but none is present in
Pleuromamma .
Transduction in a mechanosensor is the process by which a mechanical stimulus—a force
acting to displace the seta—is transformed into a cellular physiological response. Weatherby and
Lenz (2000) suggest a likely mechanism for mechanotransduction involving linkages between
individual microtubules and mechanogated channels in the dendritic membrane. The scolopale
increases the rigidity of the system, and this rigidity probably contributes to high-frequency
sensitivity. The attachment of the distal dendrites within the setal lumen instead of at the base
probably enhances the physical displacement at the transduction site, promoting high sensitiv-
ity. The highly specialized receptor allows this planktonic copepod to detect the hydrodynamic
disturbances generated by an incoming predator.
It is almost always the movement of the shaft in its socket that serves as the stimulus, but
during molting in Panulirus argus the scolopale body is briefly located in the basal region of the
setal shaft, and Schmidt and Derby (2005) suggested that, in this configuration, bending of the
setal shaft itself could serve as an adequate stimulus.
Bimodal Chemo- and Mechanosensors
Antennulary setal elements that are bimodal—with both mechanosensory and chemosensory
function—are well known in decapods and other malacostracans (Schmidt and Ache 1996,
Ka ï m-Malka et al. 1999). They have also been reported from cirripede cyprid larvae (Lagersson
et al. 2003), in copepods (Laverack and Hull 1993, Weatherby et al. 1994), and in anostracan
Branchiopoda (Tyson 1980), and they are probably widespread in the Crustacea.
In the model decapod Panulirus argus, the aesthetasc rows on the antennulary annuli are
accompanied by setal elements, including guard setae, companion setae, and asymmetric setae.
Guard setae flank the distal row of aesthetascs, and one or two companion setae are located
lateral to each guard seta. The asymmetric seta is located between the end of the aesthetasc
row and the guard seta. Only the asymmetric seta has been studied both ultrastructurally and
electrophysiologically (Schmidt and Derby 2005). The asymmetric seta of Panulirus argus is
bimodal. It has a terminal pore at the tip of the setal shaft, indicative of a chemosensory func-
tion, plus an associated scolopale body located in the annulus below its base, indicative of a
mechanosensory function. Its position on the annulus provides for a loose mechanical coupling
with the aesthetasc row.
The hooded sensillum of decapods is another bimodal element. In Panulirus argus the
hooded sensillum is the second most abundant setal type on the antennulary f lagella
after the aesthetascs. Each has a porous cuticle and is innervated by nine or ten chemo-
sensory and three mechanosensory neurons whose dendrites project to the tip (Cate and
Derby 2002). The chemosensory neurons respond to waterborne chemical stimuli, while
the mechanosensory neurons respond to direct tactile stimulation, not to distant hydro-
dynamic signals. Similarly, the pocilliform seta on the antenna of the scavenging isopod
Natatolana borealis has a subapical pore and is probably a chemosensor (Ka ï m-Malka
et al. 1999).
Statocysts
Statocysts are paired equilibrium organs that contain mechanosensory setae responsive to
changes in spatial orientation. In dendrobranchiate, caridean, and reptantian Decapoda,
they are carried in the basal segment of the antennulary peduncle. They are also present
in Anaspides and in the mysid Hansenomysis , according to Siewing (1956). In decapods,
each statocyst consists of an invaginated cavity containing a statolith formed from sand
grains cemented together by a secretion from integumental glands in the f loor of the cyst
(Prentiss 1901). Cysts are closed to the external environment and house two circular canals,
one vertical and one horizontal, formed by compression of the cyst walls. Three groups of
Fig. 7.12.
Scanning electron micrograph of calceolus from antenna of Eusirus perdentatus (Amphipoda). Photo
courtesy of R. Lincoln.
mechanosensory setae are located in the f loor of the statocyst and support the statolith. The
setae, known as “statolith hairs,” form concentric rows and are stimulated by shearing force
created by movement of the statolith or by f luid movement within the circular canals. As the
animal changes its orientation relative to gravity, the statolith is displaced creating a shear-
ing force on the “statolith hairs.” Responses of receptors within the decapod statocyst con-
trol ref lexive compensatory and righting movements of the animal (see references in Cate
and Roye 1997).
The Calceolus
Calceoli are enigmatic setal elements found in gammaridean amphipods (Lincoln and Hurley
1981). Each calceolus (Fig. 7.12) typically consists of a cup-shaped proximal element and a
transversely banded distal element, both supported by a main receptacle and attached to the
antenna by a short stalk. They can occur singly or in small groups on the f lagellar annuli, and
occasionally also on the peduncle. They frequently occur in males only, sometimes in both
sexes, but never in females only. They can occur on the peduncle and f lagellum of the anten-
nule and antenna but are often confined to the antenna only. Dahl et al. (1970) inferred that
calceoli are chemoreceptors, functioning as pheromone detectors, but Lincoln and Hurley
(1981) concluded that they were mechanosensors despite being unable to confirm the pres-
ence of a nerve supply.
FUNCTIONAL MORPHOLOGY AND BEHAVIOR
The antennules of recent crustaceans are primarily sensory in function and form an important
sensory interface with the environment. However, the hallmark of the arthropodan limb is its
multifunctional potential, and antennules may play a role in many other behaviors, including
locomotion, attachment, feeding, and mating. Performance of multiple functions is usually
reflected in morphological adaptations, but in addition, comparative studies have revealed
numerous examples of adaptive fine-tuning of the sensory array, by changes in the number of
modular sets of sensory elements, by increasing or decreasing annulation, or by changes in the
size or density of receptors. The antennae often perform a sensory role but can be similarly
involved in a variety of other behaviors, including swimming, attachment, respiration, feeding,
and brooding.
Swimming
Nauplii have only three pairs of limbs that perform a range of functions. The antennules already
fulfill the sensory role that continues through to the adult, but in addition they may be involved
in swimming and feeding in certain taxa. In cirripede nauplii, for example, the antennules are
typically held directed forward while the paired antennae and mandibles generate the swim-
ming motions (Rainbow and Walker 1976). In such cases, the role of antennules is presumably
mainly sensory, whereas in calanoid copepods the antennules are often paddle shaped and setose
and can contribute significantly to swimming (Bjørnberg 1986). The antennae are important
locomotory limbs in all swimming nauplii.
Pelagic myodocopans such as Conchoecia swim almost continuously in the laboratory,
using their antennal exopods, and begin sinking as soon as swimming motions cease dur-
ing feeding episodes (Lochhead 1968). In podocopan Ostracoda, the antennules often have
a locomotory function. This includes swimming in the Cypridoidea and crawling or digging
in many Cytheroidea and in Darwinuloidea. Podocopans, such as Cypridopsis vidua, use both
antennules and antennae in swimming. The motions of thrust-producing limbs are uniquely
coordinated with the power strokes synchronized diagonally so that the left antennule and
right antenna start together and end just as the right antennule and left antenna commence
their power stroke (Hunt et al. 2007). During the power stroke, the long setae located on the
four distal segments of the antennule and the array of setae on segment 3 of the antenna splay
out into a fanlike configuration that accounts for >75% and about 50%, respectively, of the
surface area in contact with the medium. During the recovery stroke, these natatory setae col-
lapse back against the limb shaft. Swimming in this species is smoothly continuous because
power strokes occur throughout the stroke cycle, in contrast to other small crustaceans, such
as Daphnia, which exhibit rapid accelerations and decelerations due to the alternate power and
recovery strokes of the antennae (the swimming limbs).
Cladocerans propel themselves through the water by the swimming motions of the paired
antennae that have robust protopods housing powerful muscles. The zone of conspicuously
folded cuticle at the base of each antenna (Fig. 7.13) functions to increase the angle through
which the limb can swing during swimming. They carry arrays of long plumose natatory setae
that are typically splayed out to maximize their surface area in contact with the water during the
swimming power stroke. The antennae are folded toward the body to minimize their contribu-
tion to drag during the recovery stroke (Zaret and Kerfoot 1980). The predatory haplopodan
branchiopod Leptodora kindti swims continuously in the water column using its large anten-
nae to attain speeds up to 28 mm/s (Browman et al. 1989). The large, powerful antennae are
also important swimming limbs in the Laevicaudata and Spinicaudata. The long antennules of
planktonic copepods are folded back against the body during swimming, but evidence that they
contribute to swimming itself is lacking.
Many malacostracans use their abdomen to perform a powerful tail-flip swimming action.
This is an energetically expensive behavior and is usually employed as a startle escape response
from an attacking predator. Tail-flip swimming in shrimps such as Crangon involves motions
of a head fan, formed by the antennal scales, as well as the tail fan, formed from telson and uro-
pods. The antennal scales pivot laterally during body flexion to form an expanded propulsive
Fig. 7.13.
Scanning electron micrograph of male Moina (Branchiopoda) in lateral view, showing the curved form
of antennules (a1) and a large biramous antenna (a2) with a robust protopod and proximal zone of highly
folded cuticle (arrow).
surface, the head fan, which assists in the generation of thrust during tail-flips (Arnott et al.
1998). In the heavily armored scyllarid lobsters, lift is created during tail-flips, and changes in
orientation of the transformed, platelike antennal flagella are used to alter the distribution of
this lift to create pitching and rolling movements during maneuvers.
Attachment
Attachment to Substratum
The cyprid larva of cirripedes is a transitional stage marking the end of the planktonic dispersal
phase of the life cycle and the beginning of the sessile adult phase. The highly mobile cyprid
is specialized for settlement: the task of selecting a site for permanent attachment and meta-
morphosis, mediated by specific environmental cues (Crisp and Meadows 1962). The paired
antennules play a key role in settlement behavior in free-living cirripedes. Cyprid larvae explore
surfaces by walking across the substratum in a bipedal fashion, using alternate movements of
their antennules (Nott and Foster 1969). The antennules are equipped with an attachment disc
and cement gland for temporary adhesion to the substratum during walking, and they also carry
an array of sensory elements (Nott and Foster 1969, Walker 1971), almost all of which were con-
sidered to be bimodal by Lagersson et al. (2003).
The attachment disc, carried on the third segment of the four-segmented antennule, is a
disc-shaped pad, the surface of which is densely covered with cuticular villi (Fig. 7.14). The pad
is surrounded by a membranous velum and also contains the opening of the cement gland duct.
The cement gland is located in the head, close to the brain, and a long duct with a muscular sac
located proximally carries the glycoproteinaceous cement down the antennule into the disc.
The mechanism that allows rapidly reversible, temporary attachment via the discs is poorly
understood, but a preliminary study of the footprints left by a walking cyprid led Phang et al.
(2007) to suggest that a solely viscoadhesive mechanism, with the cement functioning as an
adhesive, could not generate sufficient adhesive force to explain the real attachment tenacity of
the cyprids.
Fig. 7.14.
Scanning electron micrograph of attachment disc on antennule of cypris larva of Megabalanus (Cirripedia),
showing cuticular villi covering the surface. Photo courtesy of J. Høeg.
In parasitic cirripedes, the Rhizocephala, the antennules play a major role in the unique host
invasion process. As with other cirripedes, rhizocephalans typically hatch as a nauplius larva
that, after four or five stages, metamorphoses into the cyprid larva. In the Kentrogonida, female
cyprids attach to the surface of their crustacean hosts using their antennular cement glands and
undergo a postsettlement molt into a flask-shaped, infective kentrogon stage that becomes firmly
attached to the host. Internally, the kentrogon forms a stylet that it uses to penetrate the host cuti-
cle and inoculate the next stage, the vermigon larva, into the host. This vermigon develops to form
the adult body comprising the interna (the rootlet system within the host) and the externa (the
external reproductive body). In the Lernaeodiscidae and Peltogastridae, the release of supplemen-
tary cement from the cement gland secures the kentrogon larva onto the host, and the stylet is
evaginated through its midventral surface. In contrast, in the Sacculinidae, the kentrogon remains
attached only by the cyprid antennules, and the stylet penetrates the host cuticle either via one
of the antennules or between the antennules (see Glenner 2001). Again, the host is inoculated
with the vermigon larva via the stylet. As do females, male cyprids attach using their antennules,
but their postsettlement metamorphosis produces a motile larva, the trichogon, which escapes
from the cyprid via one of its antennules at the distal break zone (Høeg 1987) and enters the female
externa via its mantle aperture.
Penetration has been observed in only three akentrogonid rhizocephalans. The “female”
cyprid of Clistosaccus uses its long antennules to permanently attach to the host (Høeg 1990),
and then one antennule penetrates the host cuticle. The method of penetration is unknown. The
distal region of the penetrating antennule breaks off, allowing the embryonic cells within the
cyprid to pass into the host and commence interna formation. The male cyprid uses its anten-
nules in a similar way to inject male generative cells either into the host adjacent to a developing
female interna or directly into a newly emerged externa (Høeg 1985).
Fig. 7.15.
Scanning electron micrograph of Argulus (Branchiura) showing base of antennule (a1) with hooked claw
(hc) and spinous processes (sp), and base of antenna (a2) with spinous process (sp). Both limbs have slen-
der, cylindrical distal segments carrying sensory elements.
Attachment to Host
Many crustaceans are parasitic, and several others, in addition to the rhizocephalans, attach to
the host using modified antennules. In the Ascothoracida, for example, the antennule is prehen-
sile and used for attachment to the invertebrate host (Grygier 1984). In the majority of parasitic
copepods, it is the antennae that form the grasping mechanism by which attachment to the host
surface is secured (Huys and Boxshall 1991). They are typically subchelate structures, with a
robust protopodal part housing the main musculature, and a clawlike distal subchela that grasps
the host. The exopod is typically lost.
In the branchiuran fish lice, the basal part of the antennule is robust, heavily sclerotized, and
armed with curved hooklike processes on the segmental margins (Fig. 7.15). In Argulus the first
segment is drawn out into a hooklike process medially, and the more elongate second segment
carries spinous processes anteriorly and posteriorly and terminates in a robust ventral hook.
Adduction by extrinsic muscles originating on the dorsal cephalic wall brings these hooks into
contact with the host surface (Gresty et al. 1993b). These hooks form part of the multilimb mech-
anism employed by these ectoparasites to attach to their fish hosts. In branchiurans, the coxa of
the five-segmented antenna is heavily sclerotized and carries a stout hooked process proximally.
However, since no adduction-abduction motions of the coxa are possible, this process probably
only assists in securing the attachment of the parasite by preventing it from being dislodged
(Gresty et al. 1993b).
Mating
Sexual dimorphism in antennule morphology reflects differing behavioral roles of the sexes in
mating, although the functional significance of structures is not always well understood. For
example, in the male of the mysid Mesopodopsis slabberi, the third segment of the antennulary
peduncle carries, in addition to the two flagella, a large setose lobe referred to as the appendix
B A
ae
pf
af
pd3
pd2
pd1
Fig. 7.16.
(A) Antennule of male Leptostylis longimana showing three-segmented peduncle (pd1–pd3) bearing pri-
mary (pf) and accessory (af) flagella. The proximal annulus of the primary flagellum is flared at its base
and carries a dense array of aesthetascs; this flagellum also carries a pair of aesthetascs (ae) distally, as in
the female. (B) Isolated aesthetasc from the basal array.
masculine plus an accessory appendix, which is an elongate lobe with a single long apical seta
(Tattersall and Tattersall 1951). The function of these lobes is unknown.
Mate Location
In many groups of crustaceans, males actively locate sexually receptive females using chem-
osensory-mediated behavior based on the detection and localization of pheromone plumes
produced by the female (e.g., Doall et al. 1998, Yen et al. 1998, Johnson and Atema 2005).
Ref lecting this sexual difference in behavioral roles, males commonly carry an enhanced
array of aesthetascs compared with conspecific females (Hallberg et al. 1997). For example,
the male of the mysid Neomysis integer has additional specialized setae on the antennulary
peduncle (Guse 1983, Johansson and Hallberg 1992). In some male cumaceans, the proximal
annulus of the primary f lagellum carries a spectacular array of long aesthetascs (Fig. 7.16)
on a f lared basal swelling. In the male of Lophogaster typicus , the primary f lagellum carries
several hundred additional slender “male-specific sensilla” in regular arrays on each annulus
in the middle and distal parts of the f lagellum. Although considerably smaller, these male-
specific sensilla do not differ significantly from aesthetascs in fine structure. In decapods,
only aesthetascs, not the nonaesthetasc chemosensors, are involved in processing pherom-
ones (Johnson and Atema 2005).
In copepods, the array of chemosensors on the antennules of adult males is often enhanced
relative to that of the female (Boxshall and Huys 1998). Enlargement of aesthetascs in the male,
rather than higher numbers of aesthetascs, is found in some planktonic copepods such as
Fig. 7.17.
Dorsal view of head of male Eubranchipus grubii (Anostraca) showing species-specific form of antenna that
is used for grasping the female during mating. Redrawn from Daday (1910).
Pontoeciella abyssicola. The female carries two aesthetascs; the male has a third located proxi-
mally, but the middle aesthetasc is grossly enlarged (1.12 mm long) in an animal with a body
length of only 1.10 mm. Outspread, this pair of aesthetascs spans more than 2.2 mm, providing
an enormous surface area and enhanced ability to scan the water passing across the antennules
for pheromonal signals.
Copulation
Male anostracans clasp onto females during mating using their antennae. In all anostracan fam-
ilies except the Streptocephalidae, the basal and apical parts of the male antennae flex against
each other to form a prehensile mechanism that enables them to grasp the female around the
genital segment (Linder 1941). The basal part of the antenna carries an array of spinous or digi-
tiform processes and smaller warts, and in some anostracans large elaborate frontal processes
form as outgrowths of the basal part (Fig. 7.17). This ornamentation and the frontal processes
may function as part of a species-specific mate recognition system (Belk 1984).
All neocopepodan orders primitively have geniculate antennules in adult males that
are used for grasping the female during precopulatory and postcopulatory mate guarding,
as well as during mating (Boxshall 1990). The specialized geniculation lies between ances-
tral segments XX and XXI, either side of which there is usually segmental fusion and setal
modifications.
Siphonostomatoid copepods exhibit precopulatory mate guarding behavior in which adult
males grasp developing females using modified antennae (Boxshall 1990). The dimorphism
in antennal form and structure reflects the different behavior patterns during mating. Sexual
dimorphism in antennule morphology can also reflect gender differences in feeding biology in
copepods with dwarf parasitic males or with nonfeeding adult males. These are reflected in the
number and size of sensors on the antennules (Boxshall et al. 1997, Boxshall and Huys 1998).
Offspring Brooding
Some arcturid isopods of the genera Astacilla and Arcturus provide extended parental care for
their developing young by carrying their first stage juveniles on their long antennae (Sars 1899).
Similar behavior has been reported for the caprellid amphipod Pseudoprotella phasma, in which
the mother lifts the young out of the marsupium and places them on her antennae (and gnatho-
pods), where they remain for up to three weeks, until the third instar (Harrison 1940).
Feeding
As a major sensory interface, the antennules function to identify and locate potential food items
for many crustaceans. Chemosensors along the antennules allow the animal to detect odorant
molecules (often amino acids) emanating from their food, and mechanosensors allow the ani-
mal to detect the presence of particles nearby.
Decapods and stomatopods use their antennules to track the chemical signatures of their
food (Goldman and Patek 2002). The chemosensors are carried on the primary f lagellum
(aesthetascs) and on the accessory f lagellum (nonaesthetasc chemosensors), and both are
involved in detecting food odors (Keller et al. 2003). Antennulary f licking is a well-studied
behavior pattern (Schmitt and Ache 1979). The primary f lagellum is f licked through the
water, a process of sampling the surrounding medium that has been likened to sniffing. In
Panulirus argus , water f lows through the aesthetasc array during the rapid f lick downstroke
and is retained there during the slower return stroke (Koehl et al. 2001). Intermittent f licking
possibly enables the lobsters to take discrete samples of odor-containing f luid (Reidenbach
et al. 2008).
Antennae can be used mechanically in deposit and suspension feeding. The amphipod
Corophium, for example, is a deposit feeder that uses its long antennae to rake surface sediment
into the entrance of its burrow, from where it is drawn down to the setose gnathopods by a water
current generated by the beating pleopods. Some Caprella also use their antennae for scraping
food particles from the substrate. The mole crab Emerita is a swash rider, burrowing into the
sediment repeatedly as it follows the tide up and down the beach. It uses its large setose anten-
nae for suspension feeding on phytoplankton during each wave cycle. Podocerid amphipods are
also known to sieve seston from the water using their setose antennae.
The planktonic copepod Euchaeta is a specialist predator that detects the presence of prey
by means of a three-dimensional array of long setae on the antennules (Yen and Nicoll 1990).
It feeds only on live prey, typically other copepods, which it detects by responding to distur-
bance (shear) in the water column generated by the swimming motions of the prey. The setal
array develops through the copepodid stages and reaches the peak of development in the adult
female but is atrophied in the adult male, which is a nonfeeding stage with vestigial mouthparts
(Boxshall et al. 1997). Small-particle-feeding copepods beat their antennae in opposition to the
maxillipeds to create the flow fields that bring food particles within range, so they can be cap-
tured by the maxillae (Price et al. 1983).
Excretion
The antennal gland is the primary excretory gland in early crustacean larval stages, but in
the adults of most taxa the paired maxillary glands take over this role during development.
However, in the Mystacocarida, Eucarida, Amphipoda, Mysidacea, some Myodocopa, and miso-
phrioid copepods, the antennal glands are retained in the adults as the sole functional excretory
gland (Hessler and Elofsson 2007, Boxshall 1982). The gland is typically located within the head,
and only the excretory duct passes into the antenna. In amphipods, the exit pore of the anten-
nal gland is typically carried at the tip of a conical process located at the base of the antenna. In
Derocheilocaris typica, the antennal excretory gland is, uniquely, located entirely within the coxa
of the limb. It comprises only eight cells and has an excretory duct that opens via a pore on the
posterior surface of the coxa (Hessler and Elofsson 2007).
a1
Fig. 7.18.
Lateral view of Bosmina longispina (Branchiopoda) showing elongate spinous form of antennules (a1).
Redrawn from Lilljeborg (1900).
Defense
Predator Deterrence
The antennules of some cladocerans take the form of curved spinous processes (Fig. 7.18) that,
together with carapace spines and crests, help to protect them against predators. Long features,
including long antennules, may be selected to reduce predation risk from grasping predators
such as copepods and Leptodora (Kerfoot 1978). Such long-featured morphs may be replaced by
short-featured morphs when predation pressure declines (Kerfoot and Peterson 1980, Tollrian
and Dodson 1999). In Bosmina coregoni gibbera, feature length seems to be determined by fit-
ness trade-offs between increased protection afforded by the better developed antennules
and spines and negative hydrodynamic effects of these structures on swimming performance
(Lord et al. 2006).
Migrating spiny lobsters (Panulirus argus) exhibit collective defensive behavior when
attacked by predatory fish. Under threat, they cluster into outward-facing, rosettelike groups
and defend themselves using their spinous antennae. This behavior is effective, with per cap-
ita mortality declining with increasing lobster group size. Panulirus also produces sound by
stridulation. The antenna has an area of ridged membrane, the stridulatory membrane, on a
medial process on the proximal antennal segment. When the antennae are raised, the stridula-
tory membrane moves over the toothed ridge on the adjacent margin of the carapace, generat-
ing a rasping sound or a slow rattle. Bouwma and Herrnkind (2009) showed that stridulation
in P. argus improved the chances of escape from attacking predators such as Octopus.
Detection of Incoming Predators
The array of setae on the eight distal (ancestral) segments of copepod antennules is highly
conservative (Boxshall and Huys 1998) throughout the copepodid phase of development.
This underlying conservatism of the distal array of sensors through ontogeny indicates
a requirement for functional continuity. Electrophysiological studies by Yen et al. (1992)

demonstrated that these antennulary setae are mechanosensors and that ablation of the
distal tip of the antennule in Pleuromamma and Euchaeta deprives the copepod of its rapid
escape response to mechanical signals (Lenz and Yen 1993). The distal array of setae forms
the mechanosensory early warning system and is involved in detecting incoming predators.
In the water column, the copepod represents a potential prey item for many predators, and
the possession of a functional approaching-predator warning system is highly advantageous.
The setae of the distal array are already present in late nauplii of planktonic calanoids. This
mechanosensory system is operational very early in ontogeny, and functional continuity is
maintained throughout the copepodid phase.
Grooming
Antennular grooming behavior is a distinctive and stereotyped behavior in decapods in which

the antennulary flagella are repeatedly brought down to the third maxillipeds and drawn
through pads of densely packed specialized setae on the endopods (Bauer 1989). In Panulirus
argus, this behavior is elicited by stimulation with L-glutamate (Barbato and Daniel 1997), and
Schmidt and Derby (2005) concluded that it is mediated through the chemoreceptors within
the asymmetric setae on the flagella. The long antennal flagellum of most dendrobranchiate,
stenopodidean, and caridean shrimps is groomed by specialized brushes of setae located either
side of the carpus-propodus articulation of the first pereopod, whereas in most other decapods
antennal grooming is performed by the third maxillipeds (Bauer 1989).
Respiration
In the burrowing crab Corystes, the long antennae carry linear arrays of setae that interlock
when the antennae are closely apposed, thus forming a breathing tube, the tip of which extends
to the surface. Inhalant water is filtered and drawn down this tube into the branchial chamber
(Hartnoll 1972).
WIDER COMPARISONS
The variation in form and function of the antennules and antennae within the Crustacea is
remarkable. The other mandibulatans, hexapods, and myriapods, all lack antennae, but their
antennules can also perform a range of roles. With the exception of the Protura, which lack
them, the antennules of hexapods and myriapods function primarily as sense organs. The
flagellate antennules of insects (winged hexapods) typically carry an array of sensilla that can
serve as olfactory receptors, mechanoreceptors, or thermohygroreceptors (Zacharuk 1985).
As in the Malacostraca, the modular construction of the antennule provides a basic flexibility
since the numbers of modules expressed during development can be adapted to suit changing
requirements. Very long antennules, as found in cockroaches, for example, may have a tactile
role analogous to that of the long antennal flagellum in Cherax.
Even in insects, the antennules can perform additional functions in mating, respiration,
or feeding behavior. The terminal annuli of the flagellum in the water beetle Hydrophilus are
covered in hydrophobic hairs and are involved in the formation of a funnel that carries air
down to the layer of trapped air on the ventral surface. Male fleas grasp their mates using their
antennules, which are provided with stalked discs, and many male collembolans exhibit simi-
lar clasping behavior during mating. The plasticity of form, as it reflects different functional
priorities, is apparent in all arthropod limbs, but the sheer structural diversity of the antennules
and antennae of the Crustacea is more spectacular than in any other arthropod group.
ACKNOWLEDGMENTS
We thank the editors for their constructive suggestions and improvements to the manuscript.
Paul Clark pointed us to important references on decapod morphology. We are grateful to Jens
Høeg and Roger Lincoln for providing photographic illustrations.
REFERENCES
Akam, M. 2000. Arthropods: Developmental diversity within a (super) phylum. Proceedings of the
National Academy of Sciences of the USA 97:4438 –4441.
Anderson, P.A., and B.W. Ache. 1985 . Voltage- and current-clamp recordings of the receptor potential in
olfactory receptor cells in situ. Brain Research 338:273–280.
Andersson, A. 1975 . The ultrastructure of the presumed chemoreceptor aesthetasc “Y” of a cypridid
ostracode. Zoologica Scripta 4:151–158.
Arnott, S.A., D.M. Neil, and A.D. Ansell. 1998. Tail-flip mechanism and size-dependent kinemat-
ics of escape swimming in the brown shrimp Crangon crangon. Journal of Experimental Biology
201:1771–1784.
Atema, J. 1977. Functional separation of smell and taste in fish and Crustacea. Pages 165–174 in
J. Le Magnen and P. MacLeod, editors. Olfaction and taste, Vol. 6. Information Retrieval,
London .
Bacescu, M. 1967. Decapoda. Fauna Republicii Socialiste Romania (Crustacea), Vol. 4, Fasicle 9. Editura
Academiei R.S.R., Bucharest .
Ball, E.E., and A.N. Cowan. 1977. Ultrastructure of the antennal sensilla of Acetes (Crustacea, Decapoda,
Natantia, Sergestidae). Philosophical Transactions of the Royal Society of London Series B
277:429 –457.
Barbato, J.C., and P.C. Daniel. 1997. Chemosensory activation of an antennular grooming behav-
ior in the spiny lobster, Panulirus argus, is tuned narrowly to L-glutamate. Biological Bulletin
293:107–115.
Barnes, T.G., T.Q. Truong , G.G. Adams, and N.E. McGruer. 2001. Large deflection analysis of a biomi-
metic lobster antenna due to contact and flow. ASME Journal of Applied Mechanics 68:948 –951.
Bauer, R.T. 1989. Decapod crustacean grooming: Functional morphology, adaptive value and phy-
logenetic significance. Pages 49–73 in B.E. Felgenhauer , L. Watling , and A.B. Thistle, editors.
Functional morphology of feeding and grooming in Crustacea. Balkema, Rotterdam.
Belk , D. 1984 . Antennal appendages and reproductive success in the Anostraca. Journal of Crustacean
Biology 4:66 –71.
Bielecki, J., B.K.K. Chan, J.T. Høeg , and A. Sari. 2009. Antennular sensory organs in cyprids of bal-
anomorph cirripedes: Standardizing terminology using Megabalanus rosea. Biofouling 25:203–214.
Bjørnberg , T.S. 1986. The rejected nauplius: A commentary. Syllogeus 58:232–236.
Bouwma, P.E., and W.F. Herrnkind. 2009. Sound production in Caribbean spiny lobster Panulirus argus
and its role in escape during predatory attack by Octopus briareus. New Zealand Journal of Marine
and Freshwater Research 43:1–13.
Boxshall, G.A. 1982. On the anatomy of the misophrioid copepods, with special reference to
Benthomisophria palliata Sars. Philosophical Transactions of the Royal Society of London Series B
297:125–181.
Boxshall, G.A. 1985 . The comparative anatomy of two copepods, a predatory calanoid and a particle feed-
ing mormonilloid. Philosophical Transactions of the Royal Society of London Series B 311:303–377.
Boxshall, G.A. 1990. Precopulatory mate guarding in copepods. Bijdragen tot de Dierkunde 60:209 –213.
Boxshall, G.A. 2004 . The evolution of arthropod limbs. Biological Reviews 79:253–300.
Boxshall, G.A. 2007. Crustacean classification: On-going controversies and unresolved problems.
Zootaxa 1668:313–325.
Boxshall, G.A., and R. Böttger-Schnack. 1988. Unusual ascothoracid nauplii from the Red Sea. Bulletin of
the British Museum (Natural History), Zoology Series 54:275–283.
Boxshall, G.A., D.L. Danielopol, D.J. Horne, R.J. Smith, and I. Tabacaru. 2010. A critique of biramous
interpretations of the crustacean antennule. Crustaceana 83:153–167.
Boxshall, G.A., T.D. Evstigneeva, and P.F. Clark. 1993. A new interstitial cyclopoid copepod from a sandy
beach on the western shore of Lake Baikal, Siberia. Hydrobiologia 268:99 –107.
Boxshall, G.A., and R. Huys, 1998. The ontogeny and phylogeny of copepod antennules. Philosophical
Boxshall, G.A., and D. Jaume. 2000. Discoveries of cave misophrioids (Crustacea: Copepoda) shed new
light on the origin of anchialine faunas. Zoologischer Anzeiger 239:1–19.
Boxshall, G.A., and R.J. Lincoln. 1987. The life cycle of the Tantulocarida (Crustacea). Philosophical
Boxshall, G.A., J. Yen, and J.R. Strickler. 1997. Functional significance of the sexual dimorphism in the
cephalic appendages of Euchaeta rimana Bradford. Bulletin of Marine Science 61:387–398.
Briggs, D.E.G., M.D. Sutton, D.J. Siveter, and D.J. Siveter. 2003. A new phyllocarid (Crustacea:
Malacostraca) from the Silurian Fossil-Lagerstätte of Herefordshire, UK. Proceedings of the Royal
Browman, H.I., S. Kruse, and W.J. O’Brien. 1989. Foraging behavior of the predaceous cladoceran,
Leptodora kindti, and escape responses of their prey. Journal of Plankton Research 11:1075–1088.
Bruce, N. 1986. Cirolanidae (Crustacea: Isopoda) of Australia. Records of the Australian Museum,
Brusca, R.C., and G.D.F. Wilson. 1991. A phylogenetic analysis of the Isopoda with some classificatory
recommendations. Memoirs of the Queensland Museum 31:143–204.
Bruton, D.L., and H.B. Whittington. 1983. Emeraldella and Leanchoilia, two arthropods from the Burgess
Shale, Middle Cambrian, British Columbia. Proceedings of the Royal Society of London Series B
300:553–585.
Cate, H.S., and C.D. Derby. 2002. Ultrastructure and physiology of the hooded sensillum, a bimodal
chemo-mechanosensillum of lobsters. Journal of Comparative Neurology 442:293–307.
Cate, H.S., and D.B. Roye. 1997. Ultrastructure and physiology of the outer row statolith sensilla of the
blue crab Callinectes sapidus. Journal of Crustacean Biology 17:398 –411.
Clark , P.F., D.K. Calazans, and G.W. Pohle. 1998. Accuracy and standardisation of brachyuran larval
descriptions. Invertebrate Reproduction and Development 33:127–144.
Crisp, D.J., and P.S. Meadows. 1962. The chemical basis of gregariousness in cirripedes. Philosophical
Transactions of the Royal Society of London Series B 156:500 –520.
Daday, E. 1910. Monographie systématique des Phyllopodes Anostracés. Annales des Sciences Naturelle,
Zoologie, Series 9, 9:91–489.
Dahl, E., H. Emanuelsson, and C.V. Mecklenburg. 1970. Pheromone reception in the males of the amphi-
pod Gammarus duebeni Lilljeborg. Oikos 21:42–47.
Dahms, H.-U. 1992. Metamorphosis between naupliar and copepodid phases in the Harpacticoida.
Damen, W.G.M., M. Hausdorf, E.A. Seyfarth, and D. Tautz. 1998. A conserved mode of head segmenta-
tion in arthropods revealed by the expression patterns of Hox genes in a spider. Proceedings of the
National Academy of Sciences of the USA 95:10665–10670.
Daniel, P.C., M. Fox , and S. Mehta. 2008. Identification of chemosensory sensilla mediating antennular
flicking behavior in Panulirus argus, the Caribbean spiny lobster. Biological Bulletin 215:24–33.
De Calazans, D.K. 1992. Taxonomy, distribution and abundance of protozoea, mysis and megalopa stages
of Penaeidean decapods from the southern Brazilian coast. PhD dissertation, University of London.
Denton, E., and J.A.B. Gray. 1986. Lateral-line-like antennae of certain of the Penaeidea (Crustacea,
Decapoda, Natantia). Proceedings of the Royal Society of London Series B 226:249 –261.
Derby, C.D. 1982. Structure and function of cuticular sensilla of the lobster Homarus americanus. Journal
Derby, C.D., H.S. Cate, and L.R. Gentilcore. 1997. Perireception in olfaction: Molecular mass sieving
by aesthetasc sensillar cuticle determines odorant access to receptor sites in the Caribbean spiny
lobster Panulirus argus. Journal of Experimental Biology 200:2073–2081.
Diederich, R.J., V.K.L. Merrill, M.A. Pultz , and T.C. Kaufman. 1989. Isolation, structure and expression
of labial, a homeotic gene of the Antennapedia complex involved in Drosophila head. Genes and
Development 3:399 –414.
Doall, M.H., S.P. Colin, J.R. Strickler, and J. Yen. 1998. Locating a mate in 3D: The case of Temora longi-
cornis. Philosophical Transactions of the Royal Society of London Series B 353:681–689.
Elofsson, R., and R.R. Hessler. 1991. Sensory morphology in the antennae of the cephalocarid
Hutchinsoniella macracantha. Journal of Crustacean Biology 11:345–355.
Foxton, P. 1969. The morphology of the antennal flagellum of certain of the Peneidea (Decapoda,
Natantia). Crustaceana 16:33–43.
Ghiradella, H.T., J. Case, and J. Cronshaw. 1968a . Fine structure of the aesthetasc hairs of Pagurus hirsu-
tiusculus Dana. Protoplasma 66:1–20.
Ghiradella, H.T., J. Case, and J. Cronshaw. 1968b. Structure of aesthetascs in selected marine and terres-
trial decapods: Chemoreceptor morphology and environment. American Zoologist 8:603–621.
Giesbrecht, W. 1893. Systematik und Faunistik der pelagischen Copepoden des Golfes von Neapel und
der angrenzenden Meeres-Abschnitte. Fauna und Flora des Golfes von Neapel 19:1–831 (text), pls.
1–54 (atlas).
Glenner, H. 2001. Cypris metamorphosis, infection and earliest internal development of the rhizocepha-
lan Loxothylacus panopaei (Gissler). Crustacea: Cirripedia: Rhizocephala: Sacculinidae. Journal of
Morphology 249:43–75.
Goldman, J.A., and S.N. Patek. 2002. Two sniffing strategies in panulirid lobsters. Journal of
Gresty, K.A., G.A. Boxshall, and K. Nagasawa. 1993a . Antennulary sensors of the infective copepodid
larva of sea lice (Copepoda: Caligidae). Pages 83–98 in G.A. Boxshall and D. Defaye, editors.
Pathogens of wild and farmed fish: Sea lice. Ellis Horwood, Chichester, UK .
Gresty, K.A., G.A. Boxshall, and K. Nagasawa. 1993b. The fine structure and function of the cephalic
appendages of the branchiuran parasite, Argulus japonicus Thiele. Philosophical Transactions of the
Royal Society of London Series B 339:119 –135.
Gruner, H.-E., and G. Scholtz , 2004 . Segmentation, tagmata, and appendages. Pages 13–57 in J. Forest,
J.C. von Vaupel Klein and F.R. Schram, editors. The Crustacea. Brill, Leiden, The Netherlands.
Gr ü nert, U., and B.W. Ache. 1988. Ultrastructure of the aesthetasc (olfactory) sensilla of the spiny lobster,
Panulirus argus. Cell and Tissue Research 251:95–103.
Grygier, M.J. 1984 . Comparative morphology and ontogeny of the Ascothoracida, a step towards a phyl-
ogeny of the Maxillopoda. PhD dissertation, University of California, San Diego.
Grygier, M.J., and S. Ohtsuka. 1995 . SEM observation of the nauplius of Monstrilla hamatapex, new
species, from Japan and an example of upgraded descriptive standards for monstrilloid copepods.
Guse, G.-W. 1978. Antennal sensilla of Neomysis integer (Leach). Protoplasma 95:145–161.
Guse, G.-W. 1983. Ultrastructure, development and moulting of the aesthetascs of Neomysis integer and
Hallberg , E., K.U.I. Johansson, and R. Elofsson. 1992. The aesthetasc concept: Structural variations of puta-
tive olfactory receptor cell complexes in Crustacea. Microscopy Research and Technique 22:325–335.
Hallberg , E., K.U.I. Johansson, and R. Wallén . 1997. Olfactory sensilla in crustaceans: Morphology,
Hallberg , E., and M. Skog. 2011. Chemosensory sensilla in crustaceans. Pages 103–121 in T. Breithaupt and
M. Thiel, editors. Chemical communication in crustaceans. Springer, New York.
Harrison, R.J. 1940. On the biology of the Caprellidae. Growth and moulting in Pseudoprotella phasma
Montagu. Journal of the Marine Biological Association of the UK 24:483–493.
Hartnoll, R.G. 1972. The biology of the burrowing crab, Corystes cassivelaunus. Bijdragen tot de
Dierkunde 42:139 –155.
Heimann, P. 1979. Fine structure of sensory tubes on the antennule of Conchoecia spinirostris (Ostracoda,
Crustacea). Cell and Tissue Research 202:461–477.
Heimann, P. 1984 . Fine structure and molting of aesthetasc sense organs on the antennules of the isopod,
Asellus aquaticus (Crustacea). Cell and Tissue Research 235:117–128.
Hessler, R.R. 1964 . The Cephalocarida. Comparative skeletomusculature. Memoirs of the Connecticut
Academy of Arts and Sciences 16:1–97.
Hessler, R.R. 1983. A defense of the caridoid facies, wherein the early evolution of the Eumalacostraca.
Pages 145–164 in F.R. Schram, editor. Crustacean phylogeny. Balkema, Rotterdam.
Hessler, R.R., and R. Elofsson. 2007. An excretory organ in the Mystacocarida (Crustacea). Arthropod
Hessler, R.R., and H.L. Sanders. 1966. Derocheilocaris typicus Pennak and Zinn (Mystacocarida) revis-
ited. Crustaceana 11:141–155.
Heymons, R. 1901. Die Entwicklungsgeschichte der Scolopender. Zoologica 33:1–33, pls. I–VIII.
Høeg , J.T. 1985 . Male cypris settlement in Clistosaccus paguri Lilljeborg (Crustacea: Cirripedia:
Rhizocephala). Journal of Experimental Marine Biology and Ecology 89:221–235.
Høeg , J.T. 1987. Male cypris metamorphosis and a new male larval form, the trichogon, in the parasitic
barnacle Sacculina carcini (Crustacea: Cirripedia: Rhizocephala). Philosophical Transactions of the
Royal Society of London Series B 317: 47–63.
Høeg , J.T. 1990. “Akentrogonid” host invasion and an entirely new life cycle in the rhizocephalan parasite
Clistosaccus paguri (Thecostraca: Cirripedia). Journal of Crustacean Biology 10:37–52.
Hou, X., and J. Bergström. 1997. Arthropods of the Lower Cambrian Chengjiang fauna, southwest China.
Hunt, G., L.E. Park , and M. Labarbera. 2007. A novel crustacean swimming stroke: coordinated
four-paddled locomotion in the Cypridoidean ostracode Cypridopsis vidua (Mü ller). Biological
Bulletin 212:67–73.
Huys, R., and G.A. Boxshall. 1991. Copepod evolution. Ray Society, London .
Huys, R., G.A. Boxshall, and R.J. Lincoln. 1993. The tantulocaridan life cycle: The circle closed? Journal
Imms, A.D. 1939. On the antennal musculature in insects and other arthropods. Quarterly Journal of the
Microscopical Society 81:273–320.
Jaume, D., G.A. Boxshall, and R.N. Bamber. 2006. A new genus of Hirsutiidae from the continental slope
off Brazil and the discovery of the first males in the Bochusacea (Crustacea: Peracarida). Zoological
Journal of the Linnean Society 148:169 –208.
Jaume, D., and F. Bréhier. 2005 . A new species of Typhlatya (Crustacea: Decapoda: Artyidae) from
anchialine caves on the French Mediterranean coast. Zoological Journal of the Linnean Society
144:387–414.
Jaume, D., J.E. Cartes, and J.-C. Sorbe. 1998. A new species of Bathymedon Sars, 1892 (Amphipoda:
Oedicerotidae) from the western Mediterranean bathyal floor. Scientia Marina 62:341–356.
Jaume, D., and K. Christenson. 2001. Amphi-Atlantic distribution of the subterranean amphipod family
Metacrangonyctidae (Gammaridea). Contributions to Zoology 70:99 –125.
Jenner, R. A., C. Ní Dhubhghaill, M.P. Ferla, and M.A. Wills. 2009. Eumalacostracan phylogeny and total
evidence: Limitations of the usual suspects. BMC Evolutionary Biology 9:21.
Johansson, K.U.I., L. Gefors, R. Wallén, and E. Hallberg. 1996. Structure and distribution patterns of
aesthetascs and male-specific sensilla in Lophogaster typicus (Mysidacea). Journal of Crustacean
Biology 16:45–53.
Johansson, K.U.I., and E. Hallberg. 1992. Male-specific structures in the olfactory system of mysids
(Mysidacea: Crustacea). Cell and Tissue Research 268:369 –368.
Johnson, M.E., and J. Atema. 2005 . The olfactory pathway for individual recognition in the American
lobster Homarus americanus. Journal of Experimental Biology 208:2865–2872.
Ka ï m-Malka, R.A., S. Maebe, C. Macquart-Moulin, and C. Bezac. 1999. Antennal sense organs of
Natatolana borealis (Lilljeborg, 1851) (Crustacea: Isopoda). Journal of Natural History 33:65–88.
Kaji, T., and A. Tsukagoshi. 2008. Origin of the novel chemoreceptor Aesthetasc “Y” in Ostracoda:
Morphological thresholds and evolutionary innovation. Evolution and Development 10:228 –240.
Karanovic , I. 2005 . Comparative morphology of the Candoninae antennula, with remarks on the ances-
tral state in ostracods and a proposed new terminology. Spixiana 28:141–160.
Keller, T.A., I. Powell, and M.J. Weissburg. 2003. Role of olfactory appendages in chemically mediated
orientation of blue crabs. Marine Ecology Progress Series 261:217–231.
Kerfoot, W.C. 1978. Combat between predatory copepods and their prey: Cyclops, Epischura and Bosmina.
Limnology and Oceanography 23:1089 –1102.
Kerfoot, W.C., and C. Peterson. 1980. Predatory copepods and Bosmina: Replacement cycles and further
influences of predation upon prey reproduction. Ecology 61:417–431.
Kesling , R.V. 1951. The morphology of ostracod molt stages. III. Biological Monographs 21:1–324.
Koehl, M.A.R., J.R. Koseff, J.P. Crimaldi, M.G. McCay, T. Cooper, M.B. Wiley, and P.A. Moore. 2001.
Lobster sniffing: Antennule design and hydrodynamic filtering of information in an odor plume.
Science 294:1948 –1951.
Koenemann, S., F.R. Schram, A. Bloechl, T.M. Iliffe, M. Hoenemann, and C. Held, 2007. Post-embryonic
development of remipede crustaceans. Evolution and Development 9:117–121.
Kunze, J. K., 1983. Stomatopoda and the evolution of the Hoplocarida. Pages 165–188 in F.R. Schram, edi-
tor. Crustacean phylogeny. Crustacean Issues, Vol. 1. Balkema, Rotterdam.
Lagersson, N.C., A. Garm, and J.T. Høeg. 2003. Notes on the ultrastructure of the setae on the fourth
antennulary segment of the Balanus amphitrite cyprid (Crustacea: Cirripedia: Thoracica). Journal
of the Marine Biological Association of the UK 83:361–365.
Laverack , M.S. 1964 . The antennulary sense organs of Panulirus argus. Comparative Biochemistry and
Laverack , M., and M.Q. Hull. 1993. Sensory innervation of the antennule of the preadult male Caligus
elongatus . Pages 114–122 in G.A. Boxshall and D. Defaye, editors. Pathogens of wild and farmed fish:
Sea lice. Ellis Horwood, Chichester, UK .
Lenz , P.H., and J. Yen. 1993. Distal setal mechanoreceptors of the first antennae of marine copepods.
Bulletin of Marine Science 53:170–179.
Lilljeborg , W. 1900. Cladocera Sueciae oder Beträge zur Kenntniss der in Schweden lebenden
Krebsthiere von der Ordnung der Branchiopoden und der Unterordnung der Cladoceren.
Akademischen Buchdruckerei, Upsala.
Lincoln, R.J., and D.E. Hurley. 1981. The calceolus, a sensory structure of gammaridean amphipods
(Amphipoda: Gammaridea). Bulletin of the British Museum (Natural History), Zoology Series
40:103–116.
Linder, F. 1941. Contributions to the morphology and the taxonomy of the Branchiopoda Anostraca.
Zoologiska Bidrag frå n Uppsala 20:101–302.
Lochhead, J.H. 1968. The feeding and swimming of Conchoecia (Crustacea, Ostracoda). Biological
Bulletin 134:456 –464.
Lord, H., R. Lagergren, J.-E. Svensson, and N. Lindqvist. 2006. Sexual dimorphism in Bosmina: The role
of morphology, drag, and swimming. Ecology 87:788 –795.
Lowry, J.K. 1986. The callynophore, a eucaridan/peracaridan sensory organ prevalent among the
Amphipoda (Crustacea). Zoologica Scripta 15:333–349.
Maas, A., D. Waloszek , and K.J. Mü ller. 2003. Morphology, ontogeny and phylogeny of the
49:1–238.
Maddox , R.F. 2000. The antennule in podocopid Ostracoda: Chaetotaxy, ontogeny and morphometrics.
Micropaleontology 4(suppl 2):1–72.
Martin, J. 1992. Branchiopoda. Pages 25–224 in F.W. Harrison, editor. Microscopic anatomy of inverte-
brates, Vol. 9, Crustacea. John Wiley and Sons, New York.
Maruzzo, D., A. Minelli, M. Ronco, and G. Fusco. 2007. Growth and regeneration of the second anten-
nae of Asellus aquaticus (Isopoda) in the context of arthropod antennal segmentation. Journal of
McKenzie, K.G., P.-J. Chen, and S. Majoran. 1991. Almatium gusevi (Chernyshev 1940): Redescription,
shield-shapes, and speculations on the reproductive mode (Branchiopoda, Kazacharthra).
Paläontologische Zeitschrift 65:305–317.
Mead, K.S. 2002. From odor molecules to plume tracking: An interdisciplinary, multilevel approach to
olfaction in stomatopods. Integrative and Comparative Biology 42:258 –264.
Mead, K.S. 2008. Do antennule and aesthetasc structure in the crayfish Orconectes virilis correlate with
flow habitat? Integrative and Comparative Biology 48:823–833.
Mead, K.S., and M.A.R. Koehl. 2000. Stomatopod antennule design: The asymmetry, sampling effi-
ciency and ontogeny of olfactory flicking. Journal of Experimental Biology 203:3795–3808.
Mead, K.S., and T.M. Weatherby. 2002. Morphology of stomatopod chemosensory sensilla facilitates
fluid sampling. Invertebrate Zoology 121:148 –157.
Michel, W.C., H.G. Trapido-Rosenthal, E.T. Chao, and M. Wachowiak. 1993. Stereoselective detec-
tion of amino acids by lobster olfactory receptor neurons. Journal of Comparative Physiology A
171:705–712.
Nott, J.A., and B.A. Foster. 1969. On the structure of the antennular attachment organ of the cypris larva
of Balanus balanoides (L.). Philosophical Transactions of the Royal Society of London Series B
256:115–134.
Olesen, J. 2001. External morphology and larval development of Derocheilocaris remanaei
Delamare-Deboutteville and Chappuis, 1951 (Crustacea, Mystacocarida), with a comparison of
crustacean segmentation and tagmosis patterns. Biologiske Skrifter 53:1–59.
Olesen, J., and D. Waloßek. 2000. Limb ontogeny and trunk segmentation in Nebalia species (Crustacea,
Malacostraca, Leptostraca). Zoomorphology 120:47–64.
Perrier, V., J. Vannier, P.R. Racheboeuf, S. Charbonnier, D. Chabard, and D. Sotty. 2006. Syncarid crusta-
ceans from the Montceau Lagerstätte (Upper Carboniferous; France). Palaeontology 49:647–672.
Peterson, M., B.T. Rogers, A. Popadić , and T.C. Kaufman. 1999. The embryonic expression pattern
of labial, posterior homeotic complex genes and the teashirt homologue in an apterygote insect.
Development, Genes and Evolution 209:77–90.
Phang , I.Y., N. Aldred, A.S. Clare, and G.J. Vancso. 2007. Towards a nanomechanical basis for temporary
adhesion in barnacle cyprids (Semibalanus balanoides). Interface 5:397–402.
Prentiss, C.W. 1901. The otocyst of decapod Crustacea. Bulletin of the Museum of Comparative Zoology
36:167–251.
Price, H.J., G.-A. Paffenhöfer, and J.R. Strickler. 1983. Modes of cell capture in calanoid copepods.
Rainbow, P.S., and G. Walker. 1976. The feeding apparatus of the barnacle nauplius larva: A scanning
electron microscope study. Journal of the Marine Biological Association of the UK 56:321–326.
Reidenbach, M.A., N. George, and M.A.R. Koehl. 2008. Antennule morphology and flicking kinemat-
ics facilitate odor sampling by the spiny lobster, Panulirus argus. Journal of Experimental Biology
211:2849 –2858.
Rossetti, G., and K. Martens. 1996. Redescription and morphological variability of Darwinula stevensoni
(Brady and Robertson, 1870) (Crustacea, Ostracoda). Bulletin de l’Institute Royal des Sciences
Naturelles de Belgique, Biologie 66:73–92.
Rushton-Mellor, S., and G.A. Boxshall. 1994 . The developmental sequence of Argulus foliaceus. Journal of
Sandeman, D.C. 1989. Physical properties sensory receptors and tactile reflexes of the antenna of the
Australian freshwater crayfish Cherax destructor. Journal of Experimental Biology 141:197–218.
Sandeman, R.E., and D.C. Sandeman. 1996. Pre- and postembryonic development, growth and
turnover of olfactory receptor neurones in crayfish antennules. Journal of Experimental Biology
199:2409 –2418.
Sanders, H.L. 1963. The Cephalocarida. Functional morphology, larval development, comparative exter-
nal anatomy. Memoirs of the Connecticut Academy of Arts and Sciences 15:1–80.
Sars, G.O. 1899. Isopoda. An account of the Crustacea of Norway. Bergen Museum 2:1–270.
Schmidt, M., and B.W. Ache. 1996. Processing of antennular input in the brain of the spiny lobster,
Panulirus argus. I. Non-olfactory chemosensory and mechanosensory pathway of the lateral and
median antennular neuropils. Journal of Comparative Physiology A 178:579 –604.
Schmidt, M., and C.D. Derby. 2005 . Non-olfactory chemoreceptors in asymmetric setae activate anten-
nulary grooming behaviour in the Caribbean spiny lobster Panulirus argus. Journal of Experimental
Biology 208:233–248.
Schmidt, M., and W. Gnatzy. 1984 . Are the funnel-canal organs the campaniform sensilla of the shore
crab Carcinus maenas (Crustacea, Decapoda). 2. Ultrastructure. Cell and Tissue Research
237:81–93.
Schmitt, B.C., and B.W. Ache. 1979. Olfaction: Responses of a decapod crustacean are enhanced by flick-
ing. Science 205:204–206.
Systematics and Evolutionary Research 38:175–187.
Scholtz , G., and G.D. Edgecombe. 2005 . Heads, Hox and the phylogenetic position of trilobites. Pages
139–165 in S. Koenemann and R.A. Jenner, editors. Crustacea and arthropod relationships.
Crustacean Issues, Vol. 16. Taylor and Francis, Boca Raton, FL.
Schram, F.R. 1986. Crustacea. Oxford University Press, New York.
Schram, F.R., and C. Hof. 1998. Fossils and the interrelationships of major crustacean groups. Pages
233–302 in G.D. Edgecombe, editor. Arthropod fossils and phylogeny. Columbia University Press,
New York.
Schutze, M.L.M., C.E.F. da Rocha, and G.A. Boxshall. 2000. Antennular development during the cope-
podid phase in the family Cyclopidae (Copepoda, Cyclopoida). Zoosystema 22:749 –806.
Scourfield, D.J. 1926. On a new type of crustacean from the Old Red Sandstone (Rhynie Chert Bed,
Aberdeenshire)—Lepidocaris rhyniensis, gen, et sp. nov. Philosophical Transactions of the Royal
Scourfield, D.J. 1940. Two new complete specimens of young stages of the Devonian fossil crustacean
Lepidocaris rhyniensis. Proceedings of the Linnean Society 152:290 –298.
Shakori, A.R. 1968. Morphology and skeletomusculature of Caenestheria propinqua (Sars)
(Conchostraca; Branchiopoda; Crustacea). Bulletin of the Department of Zoology University of
the Panjab 2:1–48.
Siewing , R. 1956. Untersuchungen zur Morphologie der Malacostraca. Zoologische Jahrbücher,
Abteilung f ü r Anatomie 75:39 –176.
Siewing , R. 1959. Syncarida. Pages 1–121 in H.-E. Gruner, editor. Dr. H. G. Bronns Klassen und
Ordnungen des Tierreiches, Vol. 5, Band 1. Akademische-Verlagsgesellschaft Geest, Leipzig.
Siveter, David J., Derek J. Siveter, M.D. Sutton, and D.E.G. Briggs. 2007. Brood care in a Silurian ostra-
cod. Proceedings of the Royal Society of London Series B 274:465–469.
Siveter, David J., M.D. Sutton, D.E.G. Briggs, and Derek J. Siveter. 2003. An ostracode crustacean with
soft parts from the Lower Silurian. Science 302:1749 –1751.
Siveter, David J., M. Williams, and D. Waloszek. 2001. A phosphatocopid Crustacean with appendages
from the Lower Cambrian. Science 293:479 –481.
Smith, R.J., and T. Kamiya. 2008. The ontogeny of two species of Darwinuloidea (Ostracoda, Crustacea).
Zoologischer Anzeiger 247:275–302.
Smith, R.J., and R. Matzke-Karasz. 2008. The organ on the first segment of the cypridoidean (Ostracoda,
Crustacea) antennule: Morphology and phylogenetic significance. Senckenbergiana Lethaea
88:127–140.
Smith, R.J., and A. Tsukagoshi. 2005 . The chaetotaxy, ontogeny and musculature of the antennule of
podocopan ostracods (Crustacea). Journal of Zoology 265:157–177.
Stensmyr, M.C., S. Erland, E. Hallberg, R. Wallén, P. Greenaway, and B.S. Hansson. 2005 . Insect-like
olfactory adaptations in the terrestrial giant robber crab. Current Biology 15:116 –121.
Steullet, P., H.S. Cate, W.C. Michel, and C.D. Derby. 2000. Functional units of a compound nose:
Aesthetasc sensilla house similar populations of olfactory receptor neurons on the crustacean
antennule. Journal of Comparative Neurology 418:270–280.
Tattersall, W.M., and O.S. Tattersall. 1951. The British Mysidacea. Ray Society, London .
Telford, M.J., and R.H. Thomas. 1998. Expression of homeobox genes shows chelicerate arthropods
retain their deutocerebral segment. Proceedings of the National Academy of Sciences of the USA
95:10671–10675.
Thomson, M., K. Robertson, and A. Pile. 2009. Microscopic structure of the antennulae and antennae on
the deep-sea isopod Bathynomus pelor. Journal of Crustacean Biology 29:302–316.
Tollrian, R., and S.I. Dodson. 1999. Inducible defenses in Cladocera: Constraints, costs, and multipreda-
tor environments. Pages 177–202 in R. Tollrian and C.D. Harvell, editors. The ecology and evolu-
tion of inducible defenses. Princeton University Press, Princeton, NJ.
Tyson, G.E. 1980. Fine structure of the type 2 antennular sensilla of the brine shrimp, Artemia salina.
American Zoologist 20:816 –000.
Vandel, A. 1960. Isopodes terrestres (Première partie). Faune de France 64:1–416.
Van der Ham, J.L., and B.E. Felgenhauer. 2006. Ultrastructure of the peduncular aesthetascs of
Speleonectes tanumekes (Crustacea, Remipedia) in comparison with crustaceans from stressful
environments. Invertebrate Biology 125:256 –264.
Walker, G. 1971. A study of the cement apparatus of the cypris larva of the barnacle Balanus balanoides.
Marine Biology 9:205–212.
Weatherby, T.M., and Lenz , P.H. 2000. Mechanoreceptors in calanoid copepods: Designed for high
sensitivity. Arthropod Structure and Development 29: 275–288.
Weatherby, T.M., K.K. Wong , and P.H. Lenz. 1994 . Fine structure of the distal sensory setae on the
first antenna of Pleuromamma xiphias Giesbrecht (Copepoda). Journal of Crustacean Biology
14:670–685.
Wege, W. 1911. Morphologische und experimentelle Studien an Asellus aquaticus. Zoologische
Jahrbücher, Abteilung f ü r Allgemeine Zoologie und Physiologie der Tiere 30:217–320.
Yager, J. 1981. Remipedia, a new class of Crustacea from a marine cave in the Bahamas. Journal of
Crustacean Biology 1:328 –333.
Yen, J., P.H. Lenz , D.V. Gassie, and D.K. Hartline. 1992. Mechanoreception in marine copepods:
Electrophysiological studies on the first antennae. Journal of Plankton Research 14:495–512.
Yen, J., and N.T. Nicoll. 1990. Setal array on the first antennae of a carnivorous marine copepod, Euchaeta
norvegica. Journal of Crustacean Biology 10:218 –224.
Yen, J., M.J. Weissberg , and M.H. Doall. 1998. The fluid physics of signal perception by mate-tracking
copepods. Philosophical Transactions of the Royal Society of London Series B 353:787–804.
Zacharuk , R.Y. 1985 . Antennae and sensilla. Pages 1–69 in G.A. Kerkut and L.I. Gilbert, editors.
Comprehensive insect physiology, biochemistry and pharmacology, Vol. 6. Pergamon Press,
Oxford.
Zaret, R.E., and W.C. Kerfoot. 1980. The shape and swimming technique of Bosmina longirostris.
Zhang , D., S. Cai, H. Liu, and J. Lin. 2008. Antennal sensilla in the genus Lysmata (Caridea). Journal of
8
FEEDING AND DIGESTIVE SYSTEM
Les Watling
Abstract
Following food capture, the process of digestion in all animals involves breaking down the
food material into ever smaller components that, under the action of digestive enzymes,
results in molecules small enough to be absorbed by specialized cells in the digestive tract.
Crustaceans eat a wide variety of items, from capture of particles a few micrometers in diam-
eter to taking bites from organisms much larger than themselves. Since the crustacean body is
completely covered in an exoskeleton of chitin, and no cilia are present externally, the process
of ingestion must utilize other means. Some crustaceans have evolved mechanisms to obtain
particles by using the viscous properties of water, while others have modified appendages pos-
terior to the head to aid in food procurement. Expansion of the esophagus and foregut creates
a suction effect that causes food to enter the esophagus and then the foregut, where there may
be some predigestion. Contractions of the foregut push the food material into the midgut,
where the last stages of breakdown and absorption occur. Non-malacostracans generally have
a relatively simple foregut and a large, saclike midgut. On the other hand, most malacostra-
cans are characterized by having a strongly elaborated foregut, which in the simplest forms
involves a series of infoldings and ridges but in decapods may be armored with a series of cal-
careous ossicles. The addition of enzymes along with the maceration action of the armature
on the ridges produces a soupy mixture that is pressed against one or more filters in the f loor
of the foregut. The filter size is very small, assuring that only colloidal-size material passes
into the midgut, which in malacostracans is developed into a series of caeca. The main chemi-
cal digestion and uptake of digested food take place in the midgut. Undigested material, along
with some water absorption and binding of material into fecal pellets, occurs in the hindgut.
Most non-malacostracans ingest simple foods that can easily be handled by their relatively
simple guts, but the elaboration of the gut, combined with the diversity of mouth appendages,
has undoubtedly led to exploitation of a wide variety of food types by malacostracans.
© 2013 Oxford University Press. Published 2013 by Oxford University Press. 237
INTRODUCTION
Being clothed in a hard exoskeleton, devoid of cilia, and with limited ability to produce mucus
but with seemingly limitless capacity to mold and reconfigure the features of their mouth
appendages, crustaceans have evolved so that they can feed on almost anything. Very small
particles, from either the sediment or the water column, are trapped on plumose setae, while
larger particles are handled using large clusters of pappose and serrate setae. Mandibles can be
deployed for tearing flesh as well as for crushing larger objects.
Whatever is being fed upon is sucked into the foregut, where predigestion prepares the
food for its eventual transport to the cells of the midgut. It is important to think of the feeding
appendages and structures of the foregut as a single integrated system. No matter what is taken
into the mouth, the food material must be broken down into units sufficiently small to be taken
up by the cells of the digestive gland, where the final steps of digestion and absorption occur.
Undigested and partially digested material that cannot pass through the foregut filters or other-
wise is not absorbed will make its way out the hindgut as fecal material.
THE FEEDING APPENDAGES
All crustaceans have five pairs of head appendages: from anterior to posterior, the antennules
(also called first antennae), antennae (or second antennae), mandibles, maxillules (or first max-
illae), and maxillae (or the second maxillae). In front of the mandibles, attached to the lower
part of the front of the head, is the labrum (or upper lip), and behind the mandibles is the labium
(or lower lip, also paragnaths). The mandibles and both pairs of maxillae are often referred to as
the mouth appendages, or mouthparts. In many crustacean groups, one or more segments of the
thorax may be incorporated into the posterior part of the head. The appendages on those seg-
ments are called maxillipeds, as are other modified thoracic appendages used for feeding (Fig.
8.1). The maxillipeds are often used in food procurement and so are also part of the mouthpart
complement.
Depending on the type of food eaten and its source, there are two basic pathways that food
items can take en route to the mouth. Small particles generally travel mid-ventrally, passing
between the pairs of mouth appendages. In this case, the appendages are usually very setose
along their medial margins. On the other hand, larger food items first come in contact with the
distalmost extensions of the mouthparts and are then passed inward, eventually reaching the
atrium oris, the opening to the mouth itself. In some cases, for example, in the decapods, the
mouthpart appendages are arranged so that any food items will first be handled by the outer
(third) pair of maxillipeds before passing the more typical mouthpart appendages. In other
cases, as in predatory or scavenging amphipods, pieces of flesh are cut by the incisors of the
mandibles, and the other mouthparts are used in various ways to hold the prey or larger cut
pieces.
The mandibles (Fig. 8.1) are the central feeding appendage and to a large extent determine
either what an animal can ingest or the condition of the ingested material. Crustacean man-
dibles are of two basic types: the rolling crushing model and the dual-purpose rolling cutting
model (see Manton 1977 for details of musculature, etc.). Rolling crushing mandibles are the
simplest, consisting of a large mandibular body to which the promotor-remotor (forward and
back) muscles are attached and a distal curved crushing surface, the gnathobase, which meets
its opposite member at the midline just below the mouth. This type of mandible is found in
most non-malacostracans and some malacostracans. The gnathobase may end in molar ridges
of varying strength and complexity, for example, in the branchiopods, or teeth (cusps), as
Feeding and Digestive System 239
A eye-
stalk
4 3
C
2 antennule
lateral groove
posterior mandibular UL
apodeme antenna
pleural fold
maxillule anterior margin of
labrum Md
1st thoracic leg mandible mandibular
palp
mandible incisor process
left molar lobe right molar lobe
B
right spine row
left spine row right lacinia mobilis Mxp
left lacinia mobilis

right incisor
process
200 μm
left incisor process

left labral setae right labral setae
D E
Md
Gastric mill
Mx1
Mx2
Gut
Mxp
Mouth
Mx1 Lb Mp
Mx2 Md
Mxp1
Mxp2
Mxp3
TH
BEYERHOL
M-
100 μ
BE 99
5 mm
Fig. 8.1.
The crustacean mandible is the central feeding appendage. In higher crustaceans, it is designed to both
cut and crush food items in one motion. (A) Primitively, the mandible has a rolling motion, as exemplified
in the freshwater genus Anaspides. In peracarids, as well as many decapods, the rolling motion has been
lost, and the mandible is operated by muscles connected to apodemes (muscles 2–4) (from Manton 1977,
with permission from Oxford University Press). (B) Food particles cut by the incisors are moved toward
the molars by the seta row, sometimes also called lifting setae , after which they pass to the mouth (from
Manton 1977, with permission from Oxford University Press). (C) Frontal view of the mouthparts of an
undescribed new genus of amphipod showing upper lip (UL), mandibles (Md), and maxilliped (Mxp). (D)
Side view of mouthpart field of Munida sarsi; note the arrangement of maxillipeds (Mxp1–3) and maxillae
(Mx1, Mx2) ventral to the mouth. Mp, mandible palp; Lb, labrum (from Garm and Hoeg 2000, with per-
mission from Springer). (E) Anchistrotos laqueus, a poecilostomatoid copepod ectoparasitic on the gills of
serranid fishes; mouthparts are simple and reduced. Abbreviations: Md, mandible; Mx1, Mx2, maxillae 1,
2; Mxp, maxilliped (from Kabata 1979, with permission from the Ray Society).
seen in cephalocarids, copepods, and ostracods. The dual-purpose rolling cutting mandible is
formed by adding a cutting process, the incisor, to the body of the mandible far from the axis of
swing. Such mandibles thus consist of (1) a large or small mandible body to which the muscles
responsible for the movement of the appendage are attached, either directly or by means of
chitinous extensions called apodemes; (2) a molar process proximal to the mouth and some-
times extending into the atrium oris; (3) a row of setae variously referred to as “lifting setae,”
“raker setae,” or simply the “seta row”; and (4) a distal incisor process, which may or may not
have an accessory tooth on one or both members of the mandibular pair, referred to as a “lac-
inia mobilis” (Watling 1993). Both mandible types may also bear a “palp,” generally of three
articles, that is not involved in feeding but might have functions as diverse as generation of
respiratory currents or cleaning of the front of the head and base of the antennae.
Anterior to the mouth and forming the anterior margin of the atrium oris is the labrum,
sometimes called the upper lip (Fig. 8.1C). It often contains glands that secrete mucus for bind-
ing of particles to aid in transport to the mouth; no enzymes seem to have been found in any
of these secretions (e.g., Zeni and Franchini 1990). Posterior to the mouth and often dorsal or
posterior to the mandibles is a set of fleshy lobes referred to variously as the paragnaths, labium,
or lower lip. The upper and lower lips function to seal the anterior and posterior spaces between
the mandibles and keep food items from escaping the mouth region. As suction is applied by
expansion of the foregut, the paragnaths help to form a barrier that keeps food moving in the
direction of the mouth.
Posteriorly, but in close proximity to the mandibles and paragnaths, are the two pairs of
maxillae. Crustacean maxillae are of nearly the same basic design in all groups except those
specialized for parasitism. In their basic form, both the maxillule and maxilla consist of a proxi-
mal protopod that bears one or more endites (medial setose extensions of the limb article), an
endopod of several articles also bearing setae on the medial margin, and an exopod. Both sets
of maxillae undergo significant reduction in number of articles, usually losing the exopod and
reducing in extent the endopod, especially in the various malacostracan orders. Extreme spe-
cialization of the maxillae, where the appendage has been reduced to a stylet-like structure, is
seen in the external parasitic forms of ascothoracicans, branchiurans, and some ostracods (e.g.,
Watling 1972).
Maxilliped (Fig. 8.1C,D,E) is a term used to describe an appendage posterior to the maxil-
lae that is used to help procure food. Embryologically, they are thoracic appendages, but there
are two modes of formation of maxillipeds. In most cases, as the animal develops, one or more
thoracic somites are incorporated (“fused,” in the old terminology) into the posterior margin
of the head. This seems to be the result of the action of the Hox gene Ultrabithorax (Ubx), the
expression of which begins in the second thoracic segment in isopods and contracts to the third
thoracic segment in decapods, resulting in the development of one and three pairs of maxil-
lipeds, respectively (Abzhanov and Kaufman 2003). The second type of maxilliped does not
involve developmental sequences; rather, the appendage is simply modified to help move food
items to the mouth, sometimes taking on aspects of the morphology of the maxillae but located
on the anteriormost “unfused” thoracic somite. For example, in mysids, the first and sometimes
the second thoracopod can be modified so they function more in food gathering than as loco-
motory appendages.
FEEDING: THE CAPTURE OF FOOD PARTICLES
Food for crustaceans encompasses a nearly continuous range of sizes from a few microm-
eters to many centimeters. For convenience, ecologists have divided the food spectrum into
categories, labeling animals as suspension feeders, deposit feeders, detritivores, and carni-
vores, to name a few. Of importance to understanding crustacean feeding mechanisms, how-
ever, is being able to relate the milieu of the food items to the manner in which these animals
have modified their mouthparts in order to take advantage of a particular food source. From
this perspective, there are perhaps only three major feeding modes: feeding on small particles
at low and high density, and feeding on large morsels that need to be cut and “chewed.” For
this discussion, we do not deal in depth with specializations related to parasitism and invasion
of host tissues.
Both suspension feeders and deposit feeders ingest small particles, usually <100 μm in the
longest dimension. The former encounter particles that are widely dispersed in water and so
have to be concentrated in some way by the mouth appendages, whereas the latter encounter
particles surrounded by very little water, with the result that water may need to be introduced
into the feeding area in order to help particle sorting and ingestion. As we will see, there is most
likely a continuum of particle densities that some crustaceans can exploit but above or below
which others cannot. Crustaceans that cut food into pieces will have evolved very different fea-
tures in their mouth appendages, especially with respect to the setae that are present. Here, too,
however, there is a continuity of features, culminating in the simplification of feeding structures
in those animals that eat only meat.
Adaptations for Feeding on Suspended Particles
Food particles collected by suspension feeders are highly variable and dependent on the habi-
tat of the animal. These particles may be small living organisms such as unicellular algae, lar-
vae of invertebrates, eggs, or bacteria. Nonliving particles are also collected for the attached
bacteria and organic matter. Collectively, these particles are called seston—they range in
size from 1 μm to 1 mm, and they generally occur at relatively low densities so that they may
be handled one or a few at a time. There is a vast literature on suspension feeders and their
relationship to water f low and particle capture (e.g., Wildish and Kristmanson 1997), but for
this chapter we will deal only with the mechanics of particle capture, that is, how small par-
ticles are moved from the surrounding water to the vicinity of the mouth where they can be
ingested.
Among crustaceans, details of particle capture so far are best known for calanoid copep-
ods. Mathematical and physical models have been generated for the second maxilla (Fig. 8.2A)
of three species of copepods (e.g., Koehl 1993, 1995, 2001, 2004, Koehl and Strickler 1981).
Central to understanding how this appendage works, and most likely others, one needs to
know the Reynolds number, Re , of both the appendage and the setae. Re is a ratio of the iner-
tial to viscous forces for the movement of a structure relative to the f luid in a particular situa-
tion: Re = UL/ν, where U is the velocity of the water passing the structure, L is the diameter of
the seta or the linear dimension of the structure, and ν is the kinematic viscosity of the water.
As water moves over the surface of a body or structure, some of the fluid sticks to and moves
with the surface of the body, resulting in a velocity gradient from the body outward to the free
stream (ambient) flow. Very small organisms or structures have very low Re values and so carry
with them a thick (relative to the size of the body or structure) layer of fluid as they move (see
chapter 11 in this volume). For a crustacean appendage, each seta will carry a layer of water with
it as it is moved, so the Re of the seta will determine the thickness of that layer of water. Since Re
is partly a function of velocity, the Re of a seta can vary, depending on how fast the seta is moved
through the water.
Most crustacean appendages have arrays of setae along their margin; consequently, the spac-
ing of the setae will determine whether water flows around the setal array, that is, functions as
1.0
Re=0.5
A C
0.8 Re=10–1
0.6
Re=10–2
0.4
Re=10–3
0.2 Re=10–4
Re=10–5
Leakiness
10 20 30 40 50
25
Water velocity through M2 (mm/s)
B 1.0 Re=0.5
20
Re=10–1 Re=10–2
0.8
15
10 0.6
Re=10–3
5 0.4 Re=10–4
Re=10–5
0
0.2
–5
0 50 100 150 200 250
10 20 30 40 50
Distance along M2 from base of seta (μm) Spacing (µm)
Fig. 8.2.
Copepods feed by “catching” particles floating in water. The primary appendage used is the second max-
illa (M2). This appendage works by becoming either a “rake” or a “paddle,” depending on the spacing and
movement speed of the setae. (A) As the M2 are moved outward, water rushes in to fill the space. Any
entrained particles are moved to the mouth as the M2 close (from Koehl 2004, with permission from
Elsevier). (B) Setae are long and thin structures. As the seta is moved by the appendage, the velocity of
the water moving past the seta will vary with distance along the seta, depending on the action being per-
formed (e.g., in the copepod Eucalanus pileatus): while rejecting particles (triangles), making a single 70°
fling-and-squeeze motion to capture large particles (squares), and during one of a series of 30° out-and-in
motions to move water containing small particles toward the mouth (diamonds) (from Koehl 2004, with
permission from Elsevier). (C) The degree to which the setae will become “leaky,” thus acting less like a
paddle and more like a rake, is a function of the spacing of the setae relative to the seta diameter; setae in
the upper graph are 1 μm in diameter, and those in the lower graph are 0.1 μm diameter. Numbers at the
ends of the lines are Reynolds (Re) values calculated for cylinders in a constant flow; as Re increases, so
does leakiness, so groups of setae with low Re operate much more like paddles, whereas at high Re, the seta
group acts more like a rake (from Cheer and Koehl 1987, with permission from Elsevier).
a “paddle,” or whether there is some “leakiness” and the setal array functions as a sieve (Koehl
1993). At Re < 1, there is slight leakiness as the gap between the setae increases to more than five
times the seta diameter. As Re increases to about 3, leakiness of the setal array is complete at
gaps about 10 times the seta diameter. However, at such low Re values and gaps up to 45 times
the seta diameter, the setal array never becomes completely leaky (Hansen and Tiselius 1992,
Koehl 1995). Clearly, setal spacing, along with movement speed of the appendage, will deter-
mine whether the appendage functions as a paddle, a sieve, or something in between.
Copepod second maxillae (M2) intercept the feeding current generated by the second
antennae and maxillipeds (Koehl and Strickler 1981). When algal cells are detected, the M2 of
Euclanaus pileatus move rapidly (“fling”) outward (Fig. 8.2A), creating a gap between adjacent
M2 that is immediately filled by water containing the algal cell. Koehl and Strickler (1981), using
high-speed micro-cinematography, determined the speed of this inrushing water to be about
32 mm/s. The adductor movement of the M2 then traps the algal cell, and it is moved along to the
mouth by the endites of the maxillules. Rejection of particles was accomplished by spreading of
the M2 setae combined with a rapid movement inward.
Crustacean setae can be so long that the tips of the setae can be moving at speeds that
are quite different from those measured at the base (Fig. 8.2B). In Eucalanus pileatus, for
example, during the rejection movement of M2, the speed of the water passing the seta 100
μm from the base was 5 mm/s, whereas at the tip 250 μm from the base, the water velocity
was 20 mm/s. During the f ling motion for food capture, water was moving by the tip of the
seta at only 5 mm/s, compared with about 2 mm/s 100 μm from the base. Since copepod M2
can be armored with setae of varying length , Re and thus the leakiness of the appendage may
vary with the spacing (Fig. 8.2C), as well as with movement speed of the appendage (Koehl
2004). In fact, Koehl (2004) showed that E. pileatus and Temora stylifera M2 setae operate at
Re ~ 10 –2, so the appendage functions as a slightly leaky paddle. On the other hand, the M2 of
Centropages velificatus are lined with very elongate setae that operate at Re = 1, so the append-
age functions as a “leaky sieve” (Koehl 2004).
Re values for other crustacean feeding appendages have not been calculated very frequently.
Porter et al. (1983) used measurements of intersetule distance, setule diameter, appendage
beat rate, and arc of appendage movement (from which setule speed through the water was
estimated) to calculate the order of magnitude of Re for the filtering combs on the third tho-
racic appendages. The Re of the setules on these appendages varied from 10 –3 to 10 –5 over the
four species examined. The boundary layer of water associated with the setules at these low Re
values was calculated as d × Re 0.5, where d is the diameter of the setule. In all cases, the bound-
ary layer was one to two orders of magnitude larger than the setule, suggesting that the filter-
ing comb on this appendage was not very leaky and was probably acting more like a paddle.
McClatchie and Boyd (1983) used measurements of intersetule distance of the thoracopod
setae forming the filter basket of the krill Euphausia superba to determine whether krill feed by
filtration, that is, using the setae to capture particles by direct interception as the animal moves
through the water propelled by the pleopods, or by flailing movements of the thoracic legs.
Assuming the water velocity moving past the setae and setules to be equal to the swimming
speed of the animal, they found the setules to be operating at Re < 1 and so concluded that flow
around the setules was highly viscous. Further, each setule was surrounded by a boundary layer of
attached water that blocks flow through the setule mesh. Consequently, they concluded that the
krill filter basket acts more like a series of paddles, at least when the thoracopods are not moving or
are moving slowly. Food particle capture occurs as a result of what they describe as “metachronal
flailing motions” of the thoracopods. As the thoracopods move outward, a large parcel of water
moves into the ventral area between the legs. By moving the thoracopods toward the midline of
the body at a slightly faster rate, water is forced through the mesh of setules, resulting in higher Re
and decreased setule boundary layer thickness. Particle capture finally occurs by direct intercep-
tion on the setules of the filter basket.
Bednarska and Dawidowicz (2007) suggested that Daphnia longispina could alter the Re of
their filtering appendages in the face of large numbers of cyanobacteria. This was done either
by descending to a deeper, colder part of the lake where the viscosity of the water was higher,
thus altering the Re of the appendage; by reducing the intersetule distance, presumably through
some phenotypic plasticity; or by changing the movement speed of the appendage.
For the most part, studies on other suspension feeders have dealt primarily with the distri-
bution of various setal types on the feeding appendages, paying only scant attention to their
spacing, a detail that can be used to make inferences about how the animal feeds and perhaps
about particles that the animal will have available for ingestion. Marshall and Orr (1955), for
example, thought that spacing of the setae, by itself, could be used to determine the smallest size
of particles that could be retained by the setae of a copepod maxilla. It is clear now, however, that
by combining information on spacing of setules with knowledge of the speed of movement of
the appendage, one can show that some species can feed effectively on particles of much smaller
size than seta spacing alone would have predicted.
Once particles have been successfully captured, they then need to be transferred to the
mouth. In copepods, this appears to be accomplished by the short setae on the endites of the
maxillule (Koehl and Strickler 1981, Boxshall 1985), which pass the food particles on to the gna-
thobase (incisor process) of the mandible. Itoh (1970) defined an “edge index” for copepod man-
dibles, noting that the teeth on the cutting edge were generally smaller and more widely spaced
in herbivores and omnivores that also consumed phytoplankton cells (see also, e.g., Giesecke
and Gonzalez 2004). Schnack (1982) showed that Itoh’s edge index could be related to the spac-
ing of the setae on the maxillae, but she noted that the cutting edges of the omnivorous species
varied considerably. Schnack also illustrated a wide range of second maxilla morphologies for
the copepods of Kiel Bay; using what we now know about the design of these appendages and the
Re at which they operate, we can propose alternative hypotheses about the major food sources
these species might be exploiting.
Decapods, especially porcelain crabs, aeglids, and atyid prawns, engage in suspension feed-
ing using large tufts of long setae on their third maxillipeds or first and sometimes second
pereopods. Atyids, for example, can filter particles from stream currents by spreading the long
plumose setae of the chelipeds (first and second pereopods) to form large fans that are directed
into the current (Fryer 1977). Nicol (1932) noted that the porcellanids, for example, Porcellana
longicornis, had abandoned the sediment feeding habits of the Galatheidae in favor of using the
water currents set up by the motion of the antennae and scaphognathites. This agitated water is
intercepted by sweeping motions of the third maxilliped armed with long plumose setae. Most
porcellanid species, though, utilize currents and simply extend their third maxillipeds into the
water, thus feeding in a passive manner by exploiting the natural water flow (e.g., Valdivia and
Stotz 2006). Regardless of whether they feed actively or passively, the particles captured on the
setae of the third maxilliped are transferred to the mouth by a combing motion of the distal part
of the second maxilliped.
Adaptations for Feeding on Sediment
Feeding on sediment, referred to as deposit feeding, is quantitatively, but not qualitatively, dif-
ferent from feeding on suspended particles. As with suspension feeding, water is often used to
help move particles toward the mouth, the particles will be captured using setae lining the feed-
ing appendages, and a certain fraction of the particles captured will not be digestible. In con-
trast to suspension feeding, deposit feeders will handle many more particles, often in lumps, and
may ingest a much higher proportion of indigestible material. As a result, feeding appendages
of deposit feeders may have a lower proportion of plumose setae and a higher complement of
denticulate or plumodenticulate setae, used to break up compacted sediment parcels.
Marine and freshwater sediments comprise a complex array of mineral particles bound
together in a matrix of organic polymers (Watling 1988). While most of the organic matter in
sediment is in the form of indigestible humic substances, various potential food particles may
be quite common. For example, in shallow lakes, in estuaries, and in shallow marine bays,
nestled among or attached to the sediment grains will be very small algal cells, collectively
termed microphytobenthos, such as diatoms and single-celled green algae. Shallow marine sed-
iments also contain >109 bacteria per gram wet weight and extensive fungal hyphae (Watling
1988). In deeper waters, where there is no sunlight to drive photosynthesis, phytoplankton
cells derived from the overlying photic zone may form the bulk of ingestible particles, but
even in very deep water there may be 107 bacteria per gram of sediment. In addition, within
the pore water of most sediments, amino acids, proteins, and lipids may be present in the
form of dissolved organic matter (DOM). The DOM will be ingested along with the sedi-
ment and organic particles and may form an additional nutrient source for sediment feed-
ers (although this remains to be tested using labeled compounds). The use of DOM could
be especially important to crustaceans since, as described below, what is finally sent to the
hepatopancreas for the final stages of digestion is essentially a soup of liquids with DOM and
colloidal particles.
To obtain nutrition from sediment, deposit-feeding crustaceans may either (a) ingest bulk
sediment and use their guts to sort and extract the digestible portion or (b) engage in some sedi-
ment sorting activity using the setae on the mouthparts to remove some fraction of the digest-
ible particles from the larger nondigestible mineral grains and detritus. In both cases, a large
number of mineral grains are likely to be ingested, so additional sorting and some predigestion
in the gut will be required.
The best-studied deposit-feeding crustaceans are the thalassinidean decapods (e.g., Nickell
et al. 1998, Coelho and Rodrigues 2001) and corophioid amphipods (e.g., Miller 1984, Shillaker
and Moore 1987). In both groups, thoracic appendages (chelipeds in the decapods, gnathopods
in the amphipods) are used to gather large boluses of sediment. Within their burrows or tubes,
pleopod beating sets up a strong anterior-posterior water current that is used to facilitate a rough
sorting of the sedimentary particles. A “filter basket” made up of long plumose setae is present
on the gnathopods of the corophioid amphipods and on the second and third maxillipeds in the
thalassinids. Movement of these appendages, in concert with the water current, tends to slightly
suspend the particles, allowing the smaller ones to pass through a setal filter and the larger ones
to be retained. Particles retained on the setae are transferred via mouth appendages for inges-
tion. In both groups of animals, suspension feeding was also observed, suggesting there might
be times when it is more efficient for the animal to simply filter particles from the water than to
try to sort particles from the sediment.
A similar mechanism is used by the sand bubbler crab Scopimera inflata (Zimmer-Faust
1987). The crab lifts particles from the sediment surface to the mouth area with its chelae and
then uses water stored in the gill chambers to float the lighter organic material from the heavier
sand grains. The organic particles are moved to the mouth by setae on the mouth appendages,
and the sand grains are aggregated into a pellet that is deposited back on the surface of the sedi-
ment (Zimmer-Faust 1987). Presumably, the deposition of the pellet assures the crab that energy
will not be wasted reprocessing previously sorted material.
Bulk sediment ingestion has been seen in some amphipods. Coleman (1989a) noted that
even though Antarctic species of Paraceradocus had very large gnathopods, the amphipods
were never observed to prey on anything. Rather, they constructed burrows under large stones
and used the gnathopods to push sediment toward the mouthparts. A similar mode of feed-
ing was observed in Casco bigelowi, which lives in a burrow in very soft mud (Thiel et al. 1997).
Large “handfuls” of compacted mud were taken from the burrow wall and brought to the
mouthparts by the gnathopods. When young were present, the female manipulated the mud
bolus, effectively adding water, so the juveniles could more easily ingest the particles.
Adaptations for Feeding on Plants
Feeding on plant matter involves both cutting and crushing: snipping off a piece of plant and
then crushing the piece to help release intracellular nutrients. Algivorous crabs often have
spoon-tipped chelae that they use to scrape algae from the surfaces of rocks (Fig. 8.3). Feeding
involves using first one cheliped and then the other, and the material scraped and ingested will
Fig. 8.3.
The crab Leptograpsus variegatus feeding on algae in intertidal zone of Chile. Inset shows spoon-tipped
chelae of the cheliped. Photo by Ivá n A. Hinojosa.
most likely be a mix of algae, small invertebrates, and sedimentary detritus. There may be some
sorting of food bits by the setae lining the edges of the mouth appendages (Warner 1977).
Crabs feeding on vascular plants, whether terrestrial or aquatic, have to deal with structur-
ally tougher material. As a consequence, the chelae are shorter and have sharper cutting edges
(Warner 1977). Pieces to be ingested may be cut further by the mandibles, but most of the work
breaking down the material will be done by the ossicles of the foregut.
In the deep sea, at almost 5000 m depth, Barnard (1961) found the lysianassid Onesimoides
chelatus living inside coconuts, which they were in the process of excavating. Pirlot (1933) noted
that O. chelatus ate wood that had sunk to the seafloor. Not much is unusual about the mouth-
parts of this species except that the mandible incisors are bladelike and oriented to bite in the
frontal plane, as is typical of several groups of lysianssids. A standard rolling crushing molar is
also present, presumably to help move the fragments of woody material into the mouth.
Several species of amphipods and isopods burrow either into the stipes of kelp (e.g., Najna
conciliorum, Limnoria algarum) or into pieces of wood (e.g., Limnoria lignorum). Species of the
amphipod genus Najna have greatly enhanced toothed mandible incisors and an elongate molar
surface. The mandible palp is absent. In the isopod Limnoria, the mandible is also modified, but
in this case the incisor surfaces are constructed as a “rasp and file” system, with one incisor lined
with a series of small bumps forming a rasp and the other a series of parallel grooves constituting
the file (Menzies 1957).
Adaptations for Feeding on Animal Tissue
Predation and scavenging are functionally similar, with predation requiring involvement of addi-
tional appendages for prey capture. Once the prey has been subdued, however, both predators
and scavengers will ingest whole pieces of animal tissue, usually by cutting or tearing pieces
of tissue from the larger body mass to be ingested or by tearing open the body wall of the prey
and ingesting fluids and soft interior tissues. In addition, because animal tissue usually does not
require much preparation before ingestion, that is, sorting or crushing, the mouth appendages of
predators and scavengers may be armed with a more uniform set of setae than found in suspen-
sion and deposit feeders.
Some small crustaceans are capable of preying on or scavenging larger animals. For example,
the ostracod Vargula hilgendorfi and a few other cypridinids were seen to attack large polychaete
worms in aquaria. The body wall of the worm, or any wound, was opened by a ripping action of
the caudal furca (Parker 1997, Vannier et al. 1998). The furca, which bears two rows of robust,
serrate setae increasing in length distally, is also used to hold the food item. Clawlike setae on
the fourth limbs (maxillules) help to tear open the cuticle of the worm and to remove parts of
the body contents. Further breakdown of the food pieces is facilitated by setae on the exopod of
the fifth limbs (maxillae), which then pass the food to the endites of the mouth appendages and
eventually to the atrium oris.
A substantial number of amphipod species from the families Eusiridae (e.g., Klages and Gutt
1990), Lysianassidae (e.g., Sainte-Marie 1984, Steele and Steele 1993), Stegocephalidae (Moore
and Rainbow 1989), Acanthonotozomatidae (e.g., Coleman 1989b, 1989c), and Phoxocephalidae
(Oliver et al. 1982), among others, are active predators and often scavengers. Unlike ostracods,
amphipods use their mandibles as the primary biting and cutting appendages and use the tho-
racic appendages, such as the gnathopods, merely to hold the food item. Several adaptations
to predation can be seen in the modification of amphipod mandibles (Watling 1993) from the
basic microphagous form where the toothed biting incisor leads to a row of lifting setae and
then to a rolling crushing molar. Phoxocephalids, for example, which are known to prey on
juvenile polychaetes, copepods, and other small invertebrates from the sediment, tend to have
a reduced molar and few or no lifting setae. Species that take large bites of tissue, for example,
Parandania boecki (feed on scyphozoans) (Moore and Rainbow 1989), Echiniphimedia hodgsoni
(feed on sponges), and Maxilliphimedia longipes (feed on anthozoans or hydrozoans) (Coleman
1989b), have an enlarged incisor cutting blade, usually with very small or no teeth, and a reduced
or small, soft molar. Sainte-Marie (1984) showed that scavenging lysianassids had similarly
designed mandible incisors.
Adaptations for Parasitism
Several crustacean groups have become parasites of other crustaceans, other invertebrates, or
fish. Feeding on body tissue or fluids requires modifications of the mouthparts of the parasite
for piercing the host epidermis or for invading the host body cavity. Branchiurans, for exam-
ple, have modified the maxillules as suckers that they use in concert with hooked antennae and
maxillae to attach themselves to their fish host (Gresty et al. 1993). The mandibles are small and
rasplike and nestled within the elongate labrum and labium that form the mouth tube.
Copepods exhibit some of the most amazing and diverse modifications of the head and some-
times also of the whole body (Boxshall 2005). In some cases, only the anterior appendages are
modified with hooks or suckers to hang onto the host, but in others, especially those parasit-
izing fishes, the head is modified to form rootlike processes for penetrating the body cavity of
the host. Monstrilloid copepods hatch and develop as perfectly normal copepod nauplii. When
the nauplius contacts the polychaete or molluscan host, it burrows into the body wall. Further
naupliar and copepodid stages develop within the body of the host, with progressively longer
rootlike processes replacing the normal appendages of the head. The last copepodid stage exits
the host and molts to the adult reproductive stage with fully formed swimming appendages but
no mouthparts. The most highly modified of all copepod parasites are those occupying the body
cavities of nudibranchs and chitons—the body of the copepod becomes a series of elongate tubu-
lar processes.
Other crustacean parasites include several families of isopods, a few ostracods (e.g., Watling
1972), tantulocarids, two orders of cirripedes (Ascothoracida and Rhizocephala), and cyamid as
well as some hyperiid amphipods. These groups exhibit, to varying degrees, many of the modi-
fications developed in the copepods. Mouthparts are modified for tissue piercing or biting, and
when the parasite evolves to occupy the internal body cavity of the host, all normal external
form is lost, and mouthparts are absent.
FROM INGESTION TO ABSORPTION
The Process of Ingestion
The mouthpart appendages can deliver particles, large or small, to the vicinity of the mouth, but
those particles then need to be ingested. Considering that the mouth and the foregut are lined
with chitin, the process of ingestion would seem to be mechanically difficult. The most likely
mechanism involves expansion of the foregut to create suction, thus pulling food items into the
esophagus and then further into the foregut. In decapods, the latter has both circular and longi-
tudinal muscle layers, ostensibly to keep from regurgitating ingested items (Ceccaldi 2006). In
other groups, the entrance to the foregut is blocked by large valvelike plates that move inward
and so keep material from sliding back down the esophagus.
The Design of the Digestive Tract
The crustacean digestive tract (Fig. 8.4) begins with a relatively short esophagus that leads
to a foregut, or stomach, that varies in complexity and may be divided into anterior (car-
diac) and posterior (pyloric) sections, which together are also occasionally referred to as
the proventriculus. The esophagus and foregut are derived from ectoderm and so are lined
with chitin. The ectodermal origin of the foregut allows the development of setae and other
cuticular features, resulting in a structure that can be adapted to process a wide variety of
food types before passage to the midgut, where final digestion and absorption occurs. The
midgut is of endodermal origin and is not lined with chitin. In larger crustaceans, the midgut
is usually elaborated into a system of narrow tubules lined with cells that secrete enzymes
or absorb digestive products (Fig. 8.4B). Undigested material not passed into the midgut
tubules is moved directly into the hindgut, where some additional, but often minor, diges-
tion and absorption may occur. If the animal produces fecal pellets, the binding and dewa-
tering of the material to be voided occurs here.
Functional Mechanics of the Foregut
Foreguts in crustaceans vary from the simplest sacs (e.g., in copepods) to very complex struc-
tures designed for reduction and partial digestion of ingested material. The best-studied and
most complicated and elaborated foreguts are those of decapods. To understand the decapod
foregut, we will need first to examine the simpler designs.
In barnacles, the foregut consists of a shorter or longer esophagus and short or absent ven-
triculus, leading to the rather enlarged midgut (Rainbow and Walker 1977, Johnston et al. 1993,
Anderson 1994). The esophagus may be muscular, with circular, longitudinal, and dilatory
A B
mg FG MG
fg hg
OE HG
mo
0.25 mm
CDL
cardiac stomach
C pyloric stomach
D
HG
LF
CSP PTS
IMA
OE 0.5 cm
IMP
dorsal
VIII IX II I VII V VI IV III XXIX XIX XX
F
E XXIa
XXI
XXXIII
XXXI
XXXII
XXVIII
XVI XVII XXX
OE XVIII XXIV
XII Xa X XIII XIV XV XXIII XXII XXV XXVI XXVII
Fig. 8.4.
The crustacean foregut. (A) The foregut of the copepod is relatively simple, with a small foregut and large
midgut (from Briggs 1977, with permission from the Zoological Society of London). (B) In malacostracans,
the foregut is much more elaborate, and the midgut is developed into a series of caeca (from Sars 1900). (C)
The foregut of a mysid showing the interior elaborations of the foregut wall into a series of ridges, which may
be armed with large or small spines, and filters through which the gut contents are strained before passage
to the midgut ceaca (modified from Kobusch 1998, with permission from the Royal Society of London). (D)
Predatory malacostracans generally do not have these ridges, and the foregut is often large and distensible to
accommodate large volumes of food (from Kunze 1981, with permission from the Royal Society of London).
(E) The foregut ridges may be calcified into a series of ossicles, which, as shown here for a decapod, are given
numbers so their homology can be traced (modified from Maynard and Dando 1974, with permission from
the Royal Society of London). (F) The movement of the esophagus and foregut is accomplished by contrac-
tions of a large number of extrinsic muscles (modified from Maynard and Dando 1974, with permission from
the Royal Society of London). Abbreviations: CDL, dorsolateral fold of cardiac stomach; CSP, spines of the
pyloric secondary filter; fg, FG, foregut; hg, HG, hindgut; IMA, inferomedianum anterius or anteromedi-
anum, midventral cardiac ridge; IMP, inferomedianum posterius or posteriomedianum, midventral pyloric
ridge; L, lateralia; LF, lateral vertical fold of foregut wall; mg, MG, midgut; mo, mouth; OE, oesophagus;
PTS, prong-tipped spines; I–XXXIII, numbered ossicles of foregut ridges.
muscles that, aided by the action of the mandible, serves to push or suck food particles into the
foregut and then quickly to the midgut.
The design of the foregut in copepods more or less follows this model (Fig. 8.4A). One spe-
cies, Paranthessius anemoniae, has an enlarged foregut, as do most calanoids (Arnaud et al. 1978),
but in others, such as the siphonostome Lepeophtheirus salmonis, the esophagus opens directly
into the midgut (Nylund et al. 1992). As with barnacles, muscular action serves to move material
along the esophagus and into the foregut.
Foreguts of Malacostraca have been studied at least since Milne-Edwards (1834), who unfor-
tunately introduced some vertebrate terminology to describe crustacean foregut sections.
Kobusch (1998) noted that such action was not strongly challenged, so today we still have the
foregut divided into cardiac (anterior) and pyloric (posterior) regions. From there, the termi-
nology that has developed to describe the parts of the foregut can get very detailed, and there
seems to be no single, agreed-upon system (e.g., Scheloske 1976, Icely and Nott 1984, Storch
1987). In this chapter, we deal only with major features that will help us understand how the
foregut handles food material and participates in the digestive process, and in doing so, several
equivalent terms may be used.
The esophagus leads directly into the cardiac stomach or anterior part of the foregut
(e.g., Fig. 8.4C). Usually, there are valvelike structures at the esophagus-foregut junction to
keep food material from reentering the esophagus. Dilatory muscles on the esophagus cre-
ate a suction to enable passage of food material from the mouth opening into the esophagus
and then on to the foregut (Fig. 8.4F). The cardiac chamber is commonly globular in form,
often distensible, but also may be elongate, depending on the type of food material being
ingested (Kobusch 1998). The walls of the cardiac chamber often have large outpocketings,
termed lateralia, which can be armed with a variety of cuticular structures (Fig. 8.4C,E). In
some cases, the lateralia are divided into upper (superolaterale) and lower (inferolaterale) sec-
tions (Storch 1987). Ventrally, a large unpaired ridge, the inferomedianum anterius (Scheloske
1976) or anteromedianum (Storch 1987) extends from near the junction with the esophagus to
the cardiac-pyloric junction and then becomes the inferomedianum posterius in the pyloric
stomach (Fig. 8.4C). This ridge supports the primary filter through which small particles and
fluid are pressed on their way to the midgut gland or to a secondary filter (Fig. 8.4C). Larger
particles retained on the primary filter move posteriorly into the pyloric stomach and then
into the intestine. Some malacostracans, for example, amphipods, isopods, and tanaids, have a
secondary filter in front of the opening to the midgut glands. This filter is located ventrally in
the posterior stomach. Fluid and particles that pass the primary filter then are squeezed against
this filter, with the filtrate moving on to the opening of the midgut gland and the residue exit-
ing the gut through the intestine.
The maceration of food in the foregut is the result of both mechanical and chemical proc-
esses. Larger malacostracan crustaceans have enhanced the mechanical aspects of digestion by
elaborating several of the ridges and folds of the cardiac stomach with toothlike setae or calcare-
ous impregnations, referred to as ossicles (Fig. 8.4E). In decapods, 33 ossicles in seven groups
have been identified and can be used to compare foregut structures across taxa (Maynard and
Dando 1974). Some of the ossicles are large and toothed and occur in pairs. All ossicles are shed
with the old exoskeleton and have to be created anew with each molt. Felgenhauer and Abele
(1989) examined the ossicle pattern in 56 species of lower decapods (penaeoids, sergestoids,
carideans, and stenopodidians) and found various patterns of loss and fusion of ossicles more
related to higher level taxonomic position than to diet.
Function of the foregut is governed by the stomatogastric ganglion, located dorsally on the
cardiac stomach, whose motor neurons control the muscles of the foregut and the pyloric fil-
tering system. Muscles include constrictors and dilators, squeezing and pulling primarily on
the esophagus and various sections of the cardiac stomach (Fig. 8.4F). Together, these muscles
move food particles into contact with the ossicles (if present) or other structures in the foregut
involved in maceration. Some chemical digestion may also occur in the foregut due to secretions
from an anterior diverticulum (if present), or perhaps also from the midgut glands. Contraction
of the constrictor muscles serves to press the partially digested material against the one or more
filters, which may be located posteriorly in the floor of the cardiac stomach, in the pyloric stom-
ach, or both.
The final determination as to what ultimately is shunted to the caeca is made by the mesh
size of the filters in the foregut. Kunze and Anderson (1979) showed for the three species of
hermit crabs they studied that the primary filter comprised a triple sieve of increasingly finer
mesh, allowing only very small particles and liquid to pass. The mesh size varied from <1 μm
to 2 μm. Liquid and particles passing through these filters go on to the digestive gland, whereas
the coarser material left on the sieves is passed to the hindgut to become part of the fecal mate-
rial. Kunze and Anderson (1979) also noted that there was no relationship between filter size
and diet: all hermit crabs with their varied food sources, from detritus to macrophagy, had very
similar filter mesh sizes.
The stomatopod Alima laevis has one setal screen, the posterior cardiac plate, through which
fluid (mostly digestive juices from the digestive gland) and macerated particles must pass on
their way to the pyloric stomach (Kunze 1981). Only particles <0.5 μm pass through this filter
and on to the digestive gland. Wallis and MacMillan (1998) noted that the syncarid Anaspides
tasmaniae also has only a primary filter, with very rudimentary lobes where a secondary filter
might normally be. No measurements of spacing of cuticular spines making up the primary fil-
ter are given.
Storch (1987) investigated the ultrastructure of the foregut in the isopod Porcellio scaber. His
images show that the “setae” of the primary and secondary filters are probably not true setae
(see chapter 6 in this volume) but instead are essentially a cuticular “fringe” of thicker (spines)
or thinner extent (Fig. 8.5). Sometimes these cuticular elements can be subdivided and look
like plumose setae (Ullrich et al. 1991). For several species of mysids, Kobusch (1998) found
that only particles <1 μm in size could pass the secondary filter in the pyloric stomach. Ullrich
et al. (1991) observed that the primary filter in the cardiac stomach of Euphausia superba is as
fine as the secondary filter in most mysids and amphipods, with spacing between the smallest
elements being about 0.144 μm. A secondary filter in the pyloric stomach is not present.
In a study of 14 amphipod species, with diets ranging from carnivory to detritivory, Sampson
(1995) found that the spacing of the spines on the ventral cardiac ridge primary, or rough, filter
varied from 13 to 17 μ m in the carnivorous lysianassid Anonyx sarsi to 2–4 μ m in the detritus-eating
Gammarus tigrinus. Thus, there was a limitation on the size of particles that could enter the fil-
tration channels. In all cases, however, irrespective of diet and rough filter spacing, the mesh
size of the fine filter ranged from 0.05 to 0.4 μ m. The form of the fine filter also did not differ
among the species considered; it was always constructed of plumose cuticular projections borne
on dorsally projecting spines.
It seems clear that the purpose of the filtration system is to gradually reduce the food mate-
rial, no matter what its source, to a filtrate of fluid containing dissolved and almost colloidal-
sized particles that then enters the midgut caeca for the final stages of digestion and absorption.
Because crustaceans lack cilia, movement of fluid and fine particles into the midgut caeca will be
controlled by muscular action. In decapods, the tubules of the midgut gland are surrounded by
both circular and longitudinal muscles (Hopkin and Nott 1979, Leavitt and Bayer 1982). Action
of these muscles, in concert with the muscles of the foregut, move fluids, fine particles, and dead
cells into and out of the midgut tubules.
The Midgut: Digestion’s Final Stop
Some digestive breakdown (hydrolysis) of food material may occur in the foregut due to
mechanical action of teeth and ossicles, as well as some digestive enzymes or surfactants that
are added to the mix either from the digestive glands (hepatopancreas, etc.) or perhaps from
Fig. 8.5.
The foregut is responsible for predigestion of food material. The foregut muscles squeeze the liquefied
partially digested material against one or two filters. In shrimp and some other malacostracans, there is
both a primary and a secondary filter. (A and B) Primary filter of the shrimp Nematocarcinus lanceops.
(C and D) Primary filter of the shrimp Notocrangon antarcticus. Note spacing of the “setae” and setules.
(E–G) Secondary filters of the shrimp N. lanceops, N. antarcticus, and Chorismus antarcticus, respectively.
In the secondary filter, the elements are much more closely spaced, allowing only the finest particles to
pass. From Storch et al. (2001), with permission from Springer.
secretions of glands in the labrum. What remains, then, is to reduce the food material into suffi-
ciently small particles or individual molecules that can be taken up by cells of the midgut, where
the final stages of digestion occur. As one might expect, crustaceans, with their wide diversity
of sizes and very diverse lifestyles, have diverse strategies for reducing some part of the food that
F
B3
R’ B1-2 R
D
B4
R
TRANSMEMBRANE ABSORPTION
li
m mc ENZYME SECRETION
DEFECATION
TRANSMEMBRANE INTRALUMINAL
B e
R ABSORPTION DIGESTION
MIXING
LIPID EXTRUSION
STORAGE Ii INTRACELLULAR
DIGESTION
GRINDING, MUCUS COATING
AND SECRETION OF LABRAL ENZYMES
FILTRATION, PREDATION
III II I
Fig. 8.6.
The midgut is the location for final digestion and absorption of ingested food material: the midgut of a
copepod, showing subdivisions I–III, location of major cell types (B1–4, D, F, and R), and sites of enzyme
secretion and absorption of digestive products. From Brunet et al. (1994), with permission from Aberdeen
University Press.
has entered the midgut into a form that can be “digested.” This means that some proportion of
the ingested food will be absorbed by cells of the midgut, and the final breakdown products will
then be transferred to the hemolymph for transport to sites in the body where they are needed.
While the basic method of final digestion is the same in all crustaceans, the means by which this
is accomplished vary with the animal’s body size and choice of food.
Most small non-malacostracan crustaceans, for example, copepods and ostracods, have a
very simple midgut, at least in terms of macroscopic structure (Figs. 8.4A, 8.6). In these groups,
the midgut occupies most of the length of the gut tract posterior to the esophagus (e.g., Park
1966, Yoshikoshi 1975). That is, both the foregut and hindgut are reduced in length, and the
specialized digestive tissue of the midgut predominates, sometimes with an unpaired diverticu-
lum. However, the essential components of the midgut are present (Fig. 8.6): cells that secrete
digestive enzymes into the midgut lumen and cells that can absorb by pinocytosis the hydrolysis
products. The gut cellular structure and biochemistry of digestion will be treated in detail in
volume 4 of this series (Saborowski, in press).
Larger non-malacostracans and all malacostracans have a midgut in the form of a straight
tube between the foregut and hindgut from which a few or many tubules (caeca) arise at one or
both ends. Smaller malacostracans, such as amphipods, isopods, and cumaceans, have one to
four pairs of caeca. At the other extreme, most decapods have hundreds or thousands of tubules
arranged in a large structure referred to as the digestive gland or hepatopancreas. Each of these
tubules contains cells responsible for the production of digestive enzymes, which are secreted
into the lumen of the tubule, and other cells that absorb the digestive products by diffusion or
pinocytosis (Figs. 8.6, 8.7).
The very fine, mostly colloidal-size particles that pass the foregut filters of malacostracans
are moved directly into the digestive caeca. In crayfish hepatopancreatic tubules, four major
cell types have been described (Fig. 8.6; see summary in Ceccaldi 2006): E cells, located at the
apex of the digestive tubule, are responsible for production of new cells in the tubule; B cells,
lum diff
cm lm F R
To haemocoel
B
Young B-cell
Old B-cell
B-cell differentiation
Food Intracellular
ingestion digestion
Elimination
and
assimilation
diff
F-c ntia
ere
Mastication
ell tion
and primary
digestion Holocrine Pinocytosis
in stomach extrusion of nutrients Exocytosis
of enzymes
Enzymes
to stomach E-cell
mitosis
Chyme and 24 h after
DIGESTION IN LUMEN feeding
fine particules
To intestine
Contact digestion and absorption by diffusion
n
io
nt l
re cel
iat
ffe R-
Old R-cell Young R-cell

Accumulation
n
di
nt ll
io
Accumulation of lipids
re ce
Degeneration
iat
ffe M-
of minerals and glycogen

di
Mature Young Accumulation

M-cell M-cell of proteins
and glycogen
To haemocoel
Uptake of material from the haemolymph
• R-cells pinocytosis and diffusion (large arrows)
• M-cells diffusion (small arrows)
Proximal region Midregion (B-cells) Distal region
Fig. 8.7.
(A) Structure of a digestive tubule from the hepatopancreas of the shore crab Carcinus maenas; note the
arrangement of circular (cm) and longitudinal (lm) muscles, which squeeze the tubule, resulting in the
movement of digestive enzymes and unabsorbed digestive products to the posterior part of the foregut.
lum, lumen of tubule (from Hopkin and Nott 1979, with permission from Cambridge University Press).
(B) Details of the main sites of digestion in a hepatopancreatic tubule of Penaeus semisulcatus; note that
digestion begins in the lumen and then continues due to pinocytosis in B cells or by contact with R cells
(from Brunet et al. 1994, with permission from Aberdeen University Press).
or “blisterlike cells,” are responsible for production and secretion of digestive enzymes; R cells, or
resorptive cells, are responsible for uptake of digestive products; and F-cells, or fibrillar cells,
related in various ways to B-cells, are basophilic and may secrete proteases. In the lobster
Homarus americanus and other decapods, the digestive tubules possess on their outer surfaces
both longitudinal and circular muscle fibers, indicating the possibility that fluid motion into
and out of the tubule can be controlled (Hopkin and Nott 1979, Leavitt and Bayer 1982).
The Hindgut: Final Absorption and Elimination
The hindgut in crustaceans is made from ectodermally derived tissue, so it is lined with chitin,
which may vary in its permeability. In the copepod Tigriopus californicus, the hindgut epithe-
lium is highly invaginated, and the cells possess high numbers of mitochondria, suggesting that
water transport may be occurring (Sullivan and Bisalputra 1980). The gammaridean amphipod
hindgut is divided into two parts, the anterior of which is highly folded, lined with chitin about
2–5 μm in thickness with longitudinal muscles in the folds, and surrounded by intrinsic circular
muscles. The posterior part is also highly folded, and the chitin is slightly thicker; in addition
to the intrinsic circular muscles, there are as many as eight pairs of extrinsic dilator muscles
that originate on the last urosomite integument (Carlton and Schmitz 1989). This musculature
is most likely important for feces formation as well as egestion. The cells of the isopod hind-
gut directly contact those of the foregut, the midgut being relegated to digestive caeca. Isopods
appear to use the hindgut for food storage or water resorption (W ägele et al. 1981). In general,
most crustaceans use the chitinous lining, infolding, and general musculature of the hindgut to
bind fecal material and at the same time resorb some water.
CONCLUSIONS
Digestion is essentially a process of reducing food particles, regardless of size, into small bits that
can be efficiently attacked by enzymes, releasing molecules that can be absorbed by cells of the
digestive tract. Food particles, if small enough, can be swallowed whole but otherwise need to
be cut or broken into smaller fragments. In all crustaceans, the mandibles, in concert with other
mouth appendages, are the primary agent for breaking or cutting food items into smaller morsels.
Further maceration may occur in the foregut, but some chemical digestion is most likely always
involved.
In small crustaceans, there may be no or little morphological distinction between the foregut
and midgut, with digestion and absorption occurring within a large, mostly undifferentiated
chamber. Malacostracans have isolated the final digestive processes to tubular caeca that may be
variously branched, forming distinct digestive glands where enzymes are produced and diges-
tive products are absorbed. To keep larger particles from entering these caeca, one or two filters
may be present. Nevertheless, irrespective of the size and nature of the food ingested, in the end,
the component of the ingested material that will undergo final digestion and absorption needs
to be of sufficiently small size that it can be taken up by the absorptive cells using pinocytotic
processes.
The energetic strategy of digestion has been modeled by Jumars and coworkers (Penry
and Jumars 1987, Jumars 2000). They suggested that guts could be thought of as chemical reac-
tors, of which three basic types were considered: plug flow reactors, where the food moves more
or less continuously along the gut tube with little or no axial mixing; batch reactors, where a
large bolus of food is ingested, enzymes are added, and digestion is allowed to continue with
little stirring or mixing; and continuously stirred tank reactors, where food is added a bit at
a time, enzymes are added, and reaction products are either absorbed or passed out of the
reaction vessel. Jumars (2000) noted that these models are based on the understanding that,
for the most part, hydrolysis and absorption will occur in series in animal guts. Of course, the
important step is the rate of absorption since without absorption the animal receives no return
on its energetic investment of food procurement and hydrolysis.
It is interesting to think of which crustaceans fit each of these models and, if they do, what
can the model tell us about the digestive strategy the animal is likely to employ. For example,
crustacean parasites such as branchiurans, copepods, some amphipods, and isopods, are well
known to have highly distensible guts that they fill with host body fluids or tissue. Reactor
theory predicts that the rate of throughput of food should vary inversely with the rate of genera-
tion of absorbable reaction product. Since the ingested material is essentially all hydrolysable,
it makes sense to retain that material in the gut, in the form of a batch reactor, until virtually all
the food has been converted and absorbed.
An animal that ingests sediment and uses enzymes to obtain what is easily available (i.e., a
plug f low reactor) will not retain the ingested material in the gut for very long because much
of what was eaten is indigestible (sediment mineral grains, humic substances, etc.), and the
rate of return (i.e., reaction product) will drop off rapidly soon after ingestion (Dade et al.
1990). Most of the model organisms for the plug f low reactors were polychaetes; because of
the complicated structure of crustacean guts, it is unlikely that any will fit this model very
well. On the other hand, some well-known sediment ingesters, such as Corophium volutator
and thalassinid decapods, could be modeled as continuously stirred tank reactors. In this
case, material is almost continuously ingested and moved into the foregut, where enzymes
are added, and then the filtrate is passed to the digestive caeca for absorption. The remaining
unaltered food and some products of the early digestive stages continue to pass along to the
hindgut and are expelled.
FUTURE CHALLENGES
The foregut of crustaceans has been studied extensively enough that we now know how it is
constructed and, to a certain extent, how it functions. However, with the exception of cer-
tain large decapods, we know very little about the histology of the gut tract. There are some
indications that as some of the smaller animals are examined, new and intriguing cell types
are being discovered (Ceccaldi 2006). We also do not have a very satisfying theoretical basis
for understanding crustacean digestive strategies. Using the reactor theory models of Jumars
(2000) would be a start. Crustacean guts can be more complicated than most of the worm
guts used as tests of the models so far, but learning how to accommodate those complexi-
ties would be important for understanding digestion theory generally and for generating new
models that may be applicable in artificial systems such as food production or waste-water
treatment plants.
REFERENCE
Abzhanov, A., and T.C. Kaufman. 2003. Hox genes and tagmatization of the higher Crustacea
(Malacostraca). Pages 43–44 in G. Scholtz , editor. Evolutionary developmental biology of
Crustacea. Crustacean Issues, Vol. 15. Balkema, Lisse, The Netherlands.
Anderson, D.T. 1994 . Barnacles, structure, function, development, and evolution. Chapman and Hall,
New York.
Arnaud, J., M. Brunet, and J. Mazza. 1978. Studies on the midgut of Centropages typicus (Copepod,
Calanoid). I. structural and ultrastructural data. Cell and Tissue Research 187:333–353.
Barnard, J.L. 1961. Gammaridean Amphipoda from depths of 400 to 6000 meters. Galathea Report
5:23–128.
Bednarska, A., and P. Dawidowicz. 2007. Change in filter-screen morphology and depth selection:
Uncoupled responses of Daphnia to the presence of filamentous cyanobacteria. Limnology and
Oceanography 56:2358 –2363.
Boxshall, G.A. 1985 . The comparative anatomy of two copepods, a predatory calanoid and a
particle-feeding mormonilloid. Philosophical Transactions of the Royal Society of London Series B
311:303–377.
Boxshall, G.A. 2005 . Copepoda (copepods). Pages 123–138 in K. Rohde, editor. Marine parasitology.
Commonwealth Scientific and Industrial Research Organisation, Collingwood, Australia .
Briggs, R.P. 1977. Structural observations on the alimentary canal of Paranthessius anemoniae, a cope-
pod associated with the snakelocks anemone, Anemonia sulcata. Journal of Zoology, London
182:353–368.
Brunet, M., J. Arnaud, and J. Mazza. 1994 . Gut structure and digestive cellular processes in marine
Crustacea. Oceanography and Marine Biology: An Annual Review 32:335–367.
Carlton, C.E., and E. H. Schmitz . 1989. Anatomy of the extrinsic gut musculature of Gammarus minus
(Crustacea: Amphipoda). Journal of Morphology 200:87–92.
Ceccaldi, H. J. 2006. The digestive tract: Anatomy, physiology, and biochemistry. Pages 85–203 in J.
Forest and J.C. von Vaupel Klein, editors. Treatise on zoology—anatomy, taxonomy, biology.
Crustacea, Vol. 2. Brill, Leiden, The Netherlands.
Cheer, A.Y.L., and M.A.R. Koehl. 1987. Paddles and rakes: Fluid flow through bristled appendages of
small organisms. Journal of Theoretical Biology 129:17–39.
Coelho, V.R., and S.A. Rodrigues. 2001. Setal diversity, trophic modes and functional morphology of
feeding appendages of two callianassid shrimps, Callichirus major and Sergio mirim (Decapoda:
Thalassinidea: Callianassidae). Journal of Natural History 35:1447–1483.
Coleman, C.O. 1989a . Burrowing, grooming, and feeding behavior of Paraceradocus, an Antarctic amphi-
pod genus (Crustacea). Polar Biology 10:43–48.
Coleman, C.O. 1989b. On the nutrition of two Antarctic Acanthonotozomatidae (Crustacea:
Amphipoda), gut contents and functional morphology of mouthparts. Polar Biology 9:287–294.
Coleman, C.O. 1989c . Gnathiphimedia mandibularis K.H. Barnard 1930, an Antarctic amphipod
(Acanthonotozomatidae, Crustacea) feeding on Bryozoa. Antarctic Science 1:343–344.
Dade, W.B., P.A. Jumars, and D.L. Penry. 1990. Supply-side optimization: Maximizing absorptive rates.
Pages 531–556 in R.N. Hughes, editor. Behavioural mechanisms of food selection. Springer, Berlin .
Felgenhauer, B.E., and L.G. Abele. 1989. Evolution of the foregut in the lower Crustacea. Pages 205–219
in B.E. Felgenhauer, L. Watling , and A. Thistle, editors. Functional morphology of feeding and
grooming in Crustacea. Crustacean Issues, Vol. 6. Balkema, Rotterdam.
Fryer, G. 1977. Studies on the functional morphology and ecology of the atyid prawns of Dominica.
Garm, A., and J.T. Hoeg. 2000. Functional mouthpart morphology of the squat lobster Munida sarsi, with
comparison to other anomurans. Marine Biology 137:123–138.
Giesecke, R., and H. Gonzalez. 2004 . Mandible characteristics and allometric relations in copepods: A
reliable method to estimate prey size and composition from mandible occurrence in predator guts.
Revista Chilena de Historia Natural 77:607–616.
Gresty, K.A., G.A. Boxshall, and K. Nagasawa. 1993. The fine structure and function of the cephalic
appendages of the branchiurans parasite, Argulus japonicus Thiele. Philosophical Transactions of
the Royal Society of London Series B 339:119 –135.
Hansen, B., and P. Tiselius. 1992. Flow through the feeding structures of suspension feeding zooplank-
ton: A physical model approach. Journal of Plankton Research 14:821–834.
Hopkin, S.P., and J.A. Nott. 1979. Some observations on concentrically structured intracellular granules
in the hepatopancreas of the shore crab, Carcinus maenas (L.). Journal of the Marine Biological
Association of the UK 59:867–877.
Icely, J.D., and J.A. Nott. 1984 . On the morphology and fine structure of the alimentary canal of
Corophium volutator (Pallas) (Crustacea: Amphipoda). Philosophical Transactions of the Royal
Society of London Series B 306:49 –78.
Itoh, K. 1970. A consideration on feeding habits of planktonic copepods in relation to the structure of
their oral parts. Bulletin of the Planktological Society of Japan 17:1–10.
Johnston, D.J., C.G. Alexander, and D. Yellowlees. 1993. Histology, histochemistry and enzyme biochem-
istry of the digestive glands in the tropical surf barnacle Tetraclita squamosa. Journal of the Marine
Biological Association of the UK 73:1–14.
Jumars, P.A. 2000. Animal guts as ideal chemical reactors: Maximizing absorption rates. American
Naturalist 155:527–543.
Kabata, Z. 1979. Parasitic Copepoda of British fishes. Ray Society, London.
Klages, M., and J. Gutt. 1990. Observations on the feeding behavior of the Antarctic gammarid Eusirus
perdentatus Chevreux, 1912 (Crustacea: Amphipoda) in aquaria. Polar Biology 10:359 –364.
Kobusch, W. 1998. The foregut of the Mysida (Crustacea, Peracarida) and its phylogenetic relevance.
Philosophical Transactions of the Royal Society of London Series B 353:559 –581.
Koehl, M.A.R. 1993. Hairy little legs: Feeding, smelling, and swimming at low Reynolds numbers.
Contemporary Mathematics 141:33–64.
Koehl, M.A.R. 1995 . Fluid flow through hair-bearing appendages: Feeding, smelling and swimming at
low and intermediate Reynolds numbers. Pages 157–182 in C.P. Ellington and T.J. Pedley, editors.
Biological fluid dynamics. Company of Biologists, Ltd., Cambridge.
Koehl, M.A.R. 2001. Transitions in function at low Reynolds number: Hair-bearing animal appendages.
Mathematical Methods in the Applied Sciences 24:1523–1532.
Koehl, M.A.R. 2004 . Biomechanics of microscopic appendages: Functional shifts caused by changes in
speed. Journal of Biomechanics 37:789 –795.
Kunze, J.C. 1981. The functional morphology of stomatopod Crustacea. Philosophical Transactions of
the Royal Society of London Series B 292:255–328.
Kunze, J., and D.T. Anderson. 1979. Functional morphology of the mouthparts and gastric mill in the
hermit crabs Clibanarius taeniatus (Milne Edwards), Clibanarius virescens (Krauss), Paguristes squa-
mosus McCulloch and Dardanus setifer (Milne-Edwards) (Anomura: Paguridae). Australian Journal
of Marine and Freshwater Research 30:683–722.
Leavitt, D.F., and R.C. Bayer. 1982. A description of the muscle net surrounding the digestive epithelium
in the midgut gland of the lobster, Homarus americanus. Journal of Crustacean Biology 2:40–44.
Manton, S.M. 1977. The Arthropoda: Habits, functional morphology and evolution. Oxford University
Press, Oxford.
Marshall, S.M., and A.P. Orr. 1955 . The biology of a marine copepod, Calanus finmarchicus (Gunnerus).
Oliver and Boyd, Edinburgh .
Maynard, D.M., and M.R. Dando. 1974 . The structure of the stomatogastric neuromuscular system in
Callinectes sapidus, Homarus americanus and Panulirus argus (Decapoda Crustacea). Philosophical
McClatchie, S., and C.M. Boyd. 1983. Morphological study of sieve efficiencies and mandibular surfaces in
the Antarctic krill, Euphausia superba. Canadian Journal of Fisheries and Aquatic Sciences 40:955–967.
Menzies, R.J. 1957. The marine borer family Limnoridae (Crustacea, Isopoda) Part 1: Northern and
Central America: Systematics, distribution, and ecology. Bulletin of Marine Science of the Gulf and
Caribbean 7:101–200.
Miller, D.C. 1984 . Mechanical post-capture particle selection by suspension- and deposit-feeding
Corophium. Journal of Experimental Marine Biology and Ecology 82:59 –76.
Milne-Edwards, H. 1834 . Histoire naturelle des Crustacés, comprenant l’anatomie, la physiologie et la
classification de ces animaux. Tome 1: 1–468. Paris.
Moore, P.G., and P.S. Rainbow. 1989. Feeding biology of the mesopelagic gammaridean amphipod,
Parandania boecki (Stebbing, 1888) (Crustacea: Amphipoda: Stegocephalidae), from the Atlantic
Ocean. Ophelia 30:1–19.
Nickell, L.A., R.J.A. Atkinson, and E.H. Pinn. 1998. Morphology of thalassinidean (Crustacea:
Decapoda) mouthparts and pereiopods in relation to feeding, ecology, and grooming. Journal of
Nicol, E.A.T. 1932. The feeding habits of the Galatheidea. Journal of the Marine Biological Association of
the UK 18:87–105.
Nylund, A., S. Okland, and B. Bjorknes. 1992. Anatomy and ultrastructure of the alimentary canal
in Lepeophtheirus salmonis (Copepoda: Siphonostomatoida). Journal of Crustacean Biology
12:423–437.
Oliver, J.S., J.M. Oakden, and P.N. Slattery. 1982. Phoxocephalid amphipod crustaceans as predators
on larvae and juveniles in marine soft-bottom communities. Marine Ecology Progress Series
7:179 –184.
Park , T.S. 1966. The biology of a calanoid copepod, Epilabidocera amphitrites McMurrich. La Cellule
66:129 –251.
Parker, A.R. 1997. Functional morphology of the myodocopine (Ostracoda) furca and sclerotized body
plate. Journal of Crustacean Biology 17:632–653.
Penry, D.L., and P.A. Jumars. 1987. Modeling animal guts as chemical reactors. American Naturalist
129:69 –96.
Pirlot, J.M. 1933. Les amphipodes de l’expedition du Siboga. Deuxième partie. Les amphipodes gam-
marides II. Les amphipodes de la mer profonde. 1 (Lysianassidae, Stegocephalidae, Stenothoidae,
Pleustidae, Lepechinellidae). Siboga Expeditie 33c:115–167.
Porter, K.G., Y.S. Feig , and E.F. Vetter. 1983. Morphology, flow regimes, and filtering rates of Daphnia,
Ceriodaphnia, and Bosmina fed natural bacteria. Oecologia 58:156 –163.
Rainbow, P.S., and G. Walker. 1977. The functional morphology of the alimentary tract of barnacles
(Cirripedia: Thoracica). Journal of Experimental Marine Biology and Ecology 28:183–206.
Saborowski, R. (in press). Nutrition and digestion. In Natural history of the Crustacea, Vol. 4. Oxford
University Press, New York.
Sainte-Marie, B. 1984 . Morphological adaptations for carrion feeding in four species of littoral or circalit-
toral lysianassid amphipods. Canadian Journal of Zoology 62:1668 –1674.
Sampson, S.B. 1995 . The comparative functional morphology of the amphipod mandible and foregut.
PhD dissertation, University of Maine, Orono.
Sars, G.O. 1900. Cumacea. An account of the Crustacea of Norway, Vol. 3. A. Cammermayer, Christiania,
Norway.
Scheloske, H.W. 1976. Ist die Unterteilung des Magens der Malacostraca in “Cardia” und “Pyloris”
berechtigt? Ein Beitrag zur vergleichenden Anatomie der Crustacea—Malacostraca. Zeitschrift fur
Zoologische Systematik und Evolutionsforschung 14:253–280.
Schnack , S. 1982. The structure of the mouth parts of copepods in Kiel Bay. Kieler Meeresforschungen
29:89 –101.
Shillaker, R.O., and P.G. Moore. 1987. The feeding habits of the amphipods Lembos websteri Bate
and Corophium bonnelli Milne Edwards. Journal of Experimental Marine Biology and Ecology
110:93–112.
Steele, D.H., and V.J. Steele. 1993. Biting mechanism of the amphipod Anonyx (Crustacea: Amphipoda:
Lysianassoidea). Journal of Natural History 27:851–860.
Storch, V. 1987. Microscopic anatomy and ultrastructure of the stomach of Porcellio scaber (Crustacea,
Isopoda). Zoomorphology 106:301–311.
Storch, V., B.A. Bluhm, and W.E. Arntz. 2001. Microscopic anatomy and ultrastructure of the digestive
system of three Antarctic shrimps (Crustacea: Decapoda: Caridea). Polar Biology 24:604–614.
Sullivan, D.S., and T. Bisalputra. 1980. The morphology of a harpacticoid gut: A review and synthesis.
Journal of Morphology 164:89 –105.
Thiel, M., S. Sampson, and L. Watling. 1997. Extended parental care in endobenthic amphipods. Journal
of Natural History 31:713–725.
Ullrich, B., V. Storch, and H.P. Marschall. 1991. Microscopic anatomy, functional morphology, and
ultrastructure of the stomach of Euphausia superba Dana (Crustacea, Euphausiacea). Polar Biology
11:203–211.
Valdivia, N., and W. Stotz. 2006. Feeding behavior of the porcellanids crab Allopetrolisthes spinifrons,
symbiont of the sea anemone Phymactis papillosa . Journal of Crustacean Biology 26:308 –315.
Vannier, J., K. Abe, and K. Ikuta. 1998. Feeding in myodocopid ostracods: Functional morphology and
laboratory observations from videos. Marine Biology 132:391–408.
W ägele, J.W., U. Welsch, and W. Mü ller. 1981. Fine structure and function of the digestive tract of
Cyathura carinata (Krøyer) (Crustacea, Isopoda). Zoomorphology 98:69 –88.
Wallis, E.J., and D.L. MacMillan. 1998. Foregut morphology and feeding strategies in the syncarid mala-
costracan Anaspides tasmaniae: Correlating structure and function. Journal of Crustacean Biology
18:279 –289.
Warner, G.F. 1977. The biology of crabs. Van Nostrand Reinhold, New York.
Watling , L. 1972. A new species of Acetabulastoma Shornikov from Central California with a review of the
genus. Proceedings of the Biological Society of Washington 85:481–488.
Watling , L. 1988. Small-scale features of marine sediment and their importance to the study of
deposit-feeding. Marine Ecology Progress Series 47:135–144.
Watling , L. 1993. Functional morphology of the amphipod mandible. Journal of Natural History
27:837–849.
Wildish, D., and D. Kristmanson. 1997. Benthic suspension feeders and flow. Cambridge University
Press, Cambridge.
Yoshikoshi, K. 1975 . On the structure and function of the alimentary canal of Tigriopus japonicus
(Copepoda: Harpacticoida). 1. Histological structure. Bulletin of the Japanese Society of Scientific
Fisheries 41:929 –935.
Zeni, C., and A. Franchini. 1990. A preliminary histochemical study on the labral glands of Daphnia
obtusa (Crustacea, Cladocera). Acta Histochemica 88:175–181.
Zimmer-Faust, R.K. 1987. Substrate selection and use by a deposit-feeding crab. Ecology 68: 955–970.
The author has requested enhancement of the downloaded file. All in-text references underlined in blue are linked to publications
9
APPENDAGE DIVERSITY AND MODES OF LOCOMOTION:
WALKING
Jim Belanger
Crustacean limbs exhibit bewildering complexity and variety in their adaptations to spe-
cial needs. . . . Every limb can differ in structure from every other limb on the same animal,
and the whole of the often remarkable morphology is related to habits of life.
S.M. Manton, The Arthropoda: Habits, Functional Morphology, and Evolution
Abstract
Crustaceans display a dazzling array of limb morphologies. In this review, I address this diver-
sity from a functional perspective, by linking structure to behavioral demands. A general
description of crustacean limb anatomy is provided, followed by a discussion of how the physi-
cal requirements of legged locomotion may have affected this. Factors considered include the
dynamics of pedestrian locomotion, effects of animal size and speed, the differing demands of
walking on land versus underwater, and the constraints of an exoskeleton. Patterns of limb coor-
dination, along with the mechanisms producing these, are also briefly reviewed. Finally, the use
of energy-conserving mechanisms such as tendon springs is considered.
INTRODUCTION
Crustaceans are, arguably, the most morphologically diverse taxon on Earth. The insects may
have more species, but they display nowhere near the variability of crustacean body plans that
span the gamut, for example, from barnacles to copepods to lobsters. No legs, two legs, eight
legs, ten legs . . . a walking leg that can be two meters long on a Japanese spider crab or two mil-
limeters long on a commensal pea crab . . .
261
B
A
D
C
G
E
Fig. 9.1
A sampling of the diversity of crustacean walking limbs. (A) Fourth thoracopod of the isopod Phreatoicus
orarii. (B) Fifth thoracopod of the amphipod Metaingolfiella mirabilis. (C and D) First (C) and third (D)
pereopods of the shrimp Leptochela hawaiiensis. (E and F) Third (E) and fifth (F) pereopods of the shrimp
Spongiocaris semiteres. (G) Second leg of Mesocypris audax (a terrestrial ostracod). Sources: A–F redrawn
from Schram (1986); G redrawn from Chapman (1961).
Adamowicz et al. (2008) have argued that a driving force in the overall diversity of crusta-
cean morphology is, in fact, this diversity in both limb number and limb types. They showed
that both limb number and variety have increased over evolutionary time, perhaps as a result of
positive feedback: adding new limbs or new types of limbs (via tagmatization) probably allowed
for the exploitation of new niches and new habitats while simultaneously providing new raw
material for evolution and subsequent speciation. Angelini and Kaufman (2005) similarly argue
that the evolution of limb diversity is a key factor in the success of insects.
Given this “bewildering complexity,” I do not attempt to describe the morphology of walking
appendages across all crustaceans (but see Fig. 9.1 for a representative sample). Schram (1986)
has already done this in a splendid fashion, and Hessler (1982) has produced the definitive com-
parative analysis of limb anatomy across a range of eumalacostracans. I rely heavily on these
sources but also attempt to describe crustacean walking limbs from a functional perspective,
using examples as diverse as possible to show how crustaceans have answered the fundamental
question of how to walk from here to there.
GENERAL MORPHOLOGY OF WALKING APPENDAGES
It is worth beginning by recognizing that there is no compelling physical reason for legs to
be articulated appendages. The arms of an octopus and the trunk of an elephant are obvious
examples of appendages that lack both skeletal elements and joints. Closer to the matter at
hand, both onychophorans and many insect caterpillars walk on legs that are nonarticulated
Appendage Diversity and Modes of Locomotion: Walking 263
dactyl
propus
endopod
carpus
exopod
merus
podobranch ischium
epipod
basis endites
coxa
arthrobranch
precoxa
pleurobranch
body
Fig. 9.2
A “canonical” crustacean walking limb, showing the typical segments that could be present. Redrawn
from Holthuis et al. (1993).
evaginations of the body wall. These are typically operated using a combination of hydrostat-
ics for extension and muscular activation for retraction (Belanger and Trimmer 2000, Lin and
Trimmer 2010).
A canonical crustacean limb would consist of a protopod emerging from the body, to which
would be attached one or more branches (Fig. 9.2) (Schram 1986). When there are two of these
branches, they are generally termed an exopod (outer branch) and endopod (inner branch). There
may also be various segments attached to the protopod: medial endites and lateral epipodites.
In most crustacean walking legs, the exopod is absent and the endopod consists of a series of
segments.
Structurally, crustacean limbs are much like those of other arthropods (Barnes 1980). Each
segment consists of a tube with a rigid exoskeleton composed of a cuticle of chitin and usually
mineralized to some extent. The extent of mineralization can vary greatly across species and
even across different regions of the limb (Neues et al. 2007, Cribb et al. 2009). Often limbs
have pores that penetrate the exoskeleton, allowing sensory cells access to the environment.
In many cases, the exoskeletal elements are not simple tubes but have elaborated structures
for the attachment of ligaments and muscles and for articulation between segments (Fig. 9.3).
In particular, the exoskeleton may form elaborations known as condyles, which are the actual
sites of articulation. If there is a single condyle, then the segments are free to rotate in any
direction about the joint (think of a human shoulder). One of the few joints of this type in
crustacean walking limbs occurs at the coxa-basis joint of many peracarids (Hessler 1982).
Most crustacean leg joints are bicondylar, with two points of contact. This restricts the joint
to movement in a single plane (think of a human knee). Neighboring segments are usually also
attached by ligaments, but these may be absent where limbs have developed specialized sites
Fig. 9.3
The leg joints of Janiralata (isopod) to show the arrangement of skeletal elements at each of the joints in
the leg. Insets show a cross section through the joint plane containing the condyles; shaded areas depict
arthrodial membrane. Redrawn from Hessler (1982).
for autotomy (Hessler 1982). Between the segments, there is a f lexible arthrodial membrane,
and the extent of this membrane, particularly the amount of infolding, plays a significant role
in the range of motion of the joint. The range of motion of the joint is obviously constrained
by the exoskeletal elements, as well as by the properties of the tendons and muscles. It should
be noted that the range of motion of the joint minus these elements (as in a skeletal specimen
prepared by acidification) may be considerably less than that in the living animal, and the
range of motion actually used by the animal may be smaller still (Vidal-Gadea et al. 2008). A
further consideration is that in most crustaceans the most proximal three or four joints are
generally located under the body, which may further constrain their range of motion.
Crustacean walking limbs usually have what Hessler (1982) termed a limb plane: if the
limb is removed from the animal and laid on a flat surface, there is a natural orientation of the
limb that conforms to that surface. This seems to be particularly true in isopods and amphi-
pods (Hessler 1982) and is also seen in many mammalian and insect limbs. Thus, most joint
movements in these crustaceans result in extension or retraction of the leg or in rotation of
the entire limb plane. Obviously, some joints are capable of motions that rotate or twist the
limb out of the limb plane, but Hessler considered these to be for grooming movements or
for “adjustments” to the environment, rather than of fundamental importance in locomotion.
The situation is less strict in many decapods, however. In particular, as one moves proximally
along the leg, successive joints tend to have planes of motion oriented at right angles to each
other (MacMillan 1975). Thus, the propodus-dactyl, merus-carpus, and coxa-basis joints tend
to operate in the limb plane (i.e., vertically relative to the horizontal plane of the animal), but
the carpus-propodus, basis-merus, and thorax-coxa joints tend to move the limb out of the
limb plane. In many decapods the basis-ischium joint is fused, and the same is often true of
the ischium-merus joint in brachyurans. Note that as with all my other points, there are excep-
tions to these generalizations. In a spider crab, for example, the basis-merus joint rotates the
leg about its axis, while in a crayfish, the ischium-merus joint plays the same role (Vidal-Gadea
et al. 2008).
In particular, this alternating arrangement of planes of motion of the thorax-coxa and

coxa-basis joints operates as a gimbal, allowing the tip of the leg to be placed at any point within
reach of the leg—the “working space.” Interestingly, in the peracarids noted above for having
monocondylar coxa-basis joints, the thorax-coxa joint is either fused or severely restricted in its
range of motion (Hessler 1982). [As an aside, Hessler considered the driving force for this change
to be the evolution of a thoracic marsupium for brooding their young.]
In general, each joint is operated by a pair of antagonistic muscles. These generally insert
at one end on inner surfaces of the exoskeleton, often where there are specializations for
attachment, and at the other end on tendons that pass across the joint to attach to the neigh-
boring segment (if you enjoy eating crab legs, you often see the tendons extending from one
segment when two are pulled apart). There are many exceptions to the general rule of paired
antagonists, however. In most decapods, for example, the joint between the ischium and the
merus has only one muscle that flexes the joint; extension is accomplished passively. In gen-
eral, muscles that operate a joint are located in the segment proximal to the joint. This mini-
mizes energy consumption by reducing the mass that must be accelerated whenever a joint is
used (Alexander 2003). There can also be a relationship between the size of the limb segment
and the behavioral importance of a particular joint. In a comparative study of sideways- ver-
sus forward-walking decapods, Vidal-Gadea et al. (2008) found that leg segments tended to be
larger, and housed larger muscles, if they operated joints that provided power in the animal’s
preferred walking direction.
At least in the decapods, there is a remarkable conservation of both muscles and motor
neurons making up the neuromuscular anatomy of the distal segments (merus, carpus, pro-
podus, and dactyl) of the walking legs (Fig. 9.4). Typically, 7 muscles and 15 motor neurons
are involved in controlling the three distal segments of the leg (Wiens et al. 1988). The muscu-
lature for the proximal joints is considerably more complex (a point to which I return below),
and the muscles are typically located within the body rather than in the leg segments (Vidal-
Gadea 2008).
Opener inhibitor
Opener/stretcher exciter
Stretcher inhibitor
Fast extensor exciter
Slow extensor exciter
Fast reductor exciter
Slow reductor exciter
Levator motor neurons (8-19)
Promotor motor neurons (6-19)
Promotor Levator Reductor Extensor Stretcher Opener
Common inhibitor
A. Flexor
Remotor Depresor Flexor Bender Closer
Remotor motor neurons (7-13)
Depressor motor neurons (10-13)
Flexor exciters
Accessory flexor exciter

Fast bender exciter
Slow bender exciter
Fast closer exciter
Slow closer exciter
Thorax Coxa Basi-ischium Merus Carpus Propodus Dactyl
Fig. 9.4
The innervation of the walking muscles in a decapod leg. Boxes indicate muscles, solid lines indicate indi-
vidually identified neurons, broken lines indicate groups of neurons, and numbers in parentheses indicate
the range of numbers found across species.
CRUSTACEAN WALKING
Why Have Legs?
Most crustaceans can walk. For the purposes of this discussion, I am including in the definition
of walking any form of locomotion involving a limb that generates thrust by pressing against
a substratum. This would include walking, crawling, running, galloping, and so on. Obvious
exceptions to the walking crustaceans are the sessile species, such as barnacles, and pelagic ones
such as most copepods (see chapter 11 in this volume). But even most of the crustaceans that
swim as their primary mode of locomotion can generally creep about on a substratum. Indeed,
some cladocerans have been found several meters up in the canopy of tropical forest, possibly
having crawled there (Frey 1980).
If many animals can walk about on limbs that are specialized for swimming, why bother
with legs at all? Many ostracods scurry on the substratum using their antennae (Barnes
1980), and the terrestrial ostracod Mesocypris walks using its second antennae and third legs
(Chapman 1961). What kinds of specializations should we expect to see in limbs that are used
to a large extent for walking? To answer these questions, we must consider what actually
happens in pedestrian locomotion. I begin this discussion by considering terrestrial locomo-
tion, but later I extend it to underwater locomotion, where things become considerably more
complicated.
In order to direct its own movement, an organism must generate sufficient thrust in the
desired direction to overcome drag, while generating enough lift to counteract gravity
(Fig. 9.5). For an animal that uses limbs, this means that where the limb contacts the ground,
the “ground reaction force” exerted and experienced by the limb must have a vertically directed
component (Fv) that opposes gravity and a horizontally directed component (F h) that gener-
ates thrust. For an animal at rest, the force acting on any single limb is approximately F v/n,
where n equals the number of legs on the ground. The exact force experienced by each leg will
depend on the location of the center of mass of the animal and on the specific posture adopted
by the animal (see Vidal-Gadea et al. 2008). Stepping, however, involves phases when a leg is
in contact with the substratum (stance or power stroke), alternating with phases when it is not
(swing or return stroke). The duration of the stance phase plus the duration of the swing phase
gives the stride period. We can further designate the duty cycle as the proportion of the stride
period devoted to the stance phase. During each step, the forces exerted by the limb increase
as the leg touches down and begins to bear weight and decrease as the leg lifts off. The force
falls to zero during the swing phase. This means that the maximum forces exerted by legs will
be higher when the animal is walking than at rest. For an animal that is moving, the average F v
over several steps must still equal the animal’s weight. This leads immediately to the result that
as the duty cycle becomes shorter, the maximum force exerted by the limb must increase. Thus,
an organism can reduce the force required by taking steps where the leg is on the ground for a
long period of time, but this limits how quickly the animal can move.
For a walking animal, speed of movement is determined by the rate at which limbs cycle (the
stepping frequency) and the stride length (the distance covered during a single step). Thus, an
animal can increase its speed by increasing either or both of these variables. In most animals, the
duty factor decreases as the stepping frequency increases (Biewener 2003). This means that the
maximum force exerted by the limbs on the ground must also increase as the speed increases, in
order to maintain the average force greater than the weight of the animal.
Many animals increase speed by increasing stride length. In many cases, the maximum
stride length depends on the length of the legs, which is one reason to have legs with special-
izations for walking: all else being equal, a longer leg will allow a greater velocity. Cursorial
Buoyancy Lift
Thrust Drag
Acceleration
Fv reaction
Direction of
Fh
locomotion
Gravity
Fig. 9.5
The forces acting on a walking animal. Fv, vertically directed force component; F h, horizontally directed
force component.
mammals (animals adapted to run, e.g., ungulates and big cats) can extend their maximum
stride beyond the simple length of the legs by tilting their shoulders and pelvis (Alexander
2003). Crustaceans, because their walking legs are usually attached to a rigid cephalothorax,
typically do not have this option. There are exceptions, however. Some harpacticoid copepods
crawl using their thoracic limbs, and their movement is accompanied by lateral undulations of
the body (Barnes 1980). As in the case of centipedes and many lizards, these undulations may act
not only to provide thrust (from axial muscles) but also to increase the effective length of the leg
and allow for longer strides (Manton 1977, Anderson et al. 1995).
An alternative way to increase stride length is to include an aerial phase in the stride, as
in a galloping horse. The fastest known running crustaceans, ghost crabs, do exactly this.
For short distances, they can run faster than 2 m/s (Burrows and Hoyle 1973). At the high-
est speeds, they have a stepping frequency of 20 Hz. Attaining their top speed while cycling
their legs at a maximum rate of 20 Hz should require a stride length of 10 cm, but the longest
(third) legs of the largest (not the fastest) ghost crabs are only 8 cm long. In fact, the crabs leap
between steps, increasing the effective stride length by 40–60% above what could be achieved
with a maximal stretch (Burrows and Hoyle 1973). At these highest speeds, the animals actu-
ally run with a bipedal gait, using only the second and third legs on the trailing side, with the
legs of the leading side being used effectively as skids (Fig. 9.6). Interestingly, some cock-
roaches and lizards have converged on a similar strategy for high-speed running. At their top
speeds, these animals run using only their hind pair of legs, becoming a dynamically stable
biped (Full and Tu 1991).
In ghost crabs, leg length increases linearly with carapace width; therefore, the top speed of
these crabs is a function of both carapace width and leg length, but only up to a carapace width of
about 20 mm. Above this width, leg length continues to increase, but maximum speed declines.
Burrows and Hoyle (1973) attribute this decrease to the fact that mass increases exponentially,
50 mm
R3 R3
L3
L3
Fig. 9.6
Rapid running in the ghost crab Ocypode ceratophthalma . The figure shows an image of a crab running
from left to right. The tips of the dactyls of right leg 3 (R3) and left leg 3 (L3) were dipped in paint to leave
tracks on a sheet of paper under the crab. L3 (trailing) leaves clearly defined spots (circled), while R3 (lead-
ing) leaves a smear of paint, indicating that the trailing leg touches down and pushes off a single spot, while
the leading leg skids along the substratum. Redrawn from Burrows and Hoyle (1973).
rather than linearly, with carapace width, and this increase in mass reduces maximum attain-
able speeds. This is actually an interesting point that may generalize to other organisms—
where is the optimum trade-off between the positive effects on increasing speed of increasing
size and the negative ones of increasing mass? There is an interesting literature on the effects of
size on animal velocity (Alexander 2003, Biewener 2003), focusing largely on mammals, where
there are approximately six orders of magnitude in the mass difference between a pygmy shrew
and an African elephant. If we consider the difference in mass between the spider and pea
crabs of my opening paragraph, there is also a range of about six orders of magnitude. But there
is a larger difference in the relative limb lengths—the elephant limb is about 150 times longer
than the pygmy shrew leg, while the spider crab leg is 1,000 times longer than the pea crab leg.
Any limb can be subject to two kinds of stresses: compressive stresses that act along the axis,
threatening to crush the limb, and bending stresses perpendicular to the long axis, threatening
to buckle or break the limb. The physically longer legs of the spider crabs are likely to experi-
ence much larger bending stresses, due to the longer moment arms when they act as levers to
move the animal.
Gaits
In effect, the ghost crabs change their gait in order to increase speed. We can define a gait as
a particular combination of leg movements, such as walking or running (Alexander 2003).
Transitions between gaits are abrupt—walking does not smoothly change to running. In many
cases, gaits are described using kinematic variables (e.g., duty cycles, order of foot placement),
but this makes it difficult to compare gaits among organisms that have different numbers of legs.
Alternatively, gaits can be described by their dynamics (Biewener 2003). For example, in a stiff-
legged walk, there is a regular exchange between the potential and kinetic energy of the organ-
ism’s center of mass, in the same manner as in a pendulum (Alexander 2003). Kinetic energy is
converted to potential energy as the body rises over the stiff leg during the first half of the step,
and then the exchange reverses as the body falls during the second half of the step. The process
is then repeated. Note that this process can only occur at slow speeds because the acceleration of
the center of mass by gravity sets a limit on how quickly the exchange can occur. In contrast, dur-
ing running the kinetic and potential energy oscillate together as the body bounces on springy
legs. This is energetically less efficient but permits higher speeds. Using this definition, ghost
crabs walk at slow speeds, change to a trot as they speed up, and then run at their top speeds
(Blickhan et al. 1993). It is unclear whether other crustaceans show similar gait changes. Hermit
crabs (Herreid and Full 1986) and sea roaches (Alexander 1971) are thought to use just one gait
at all speeds, although this conclusion is based on limb kinematics alone. Quadrupeds change
from a trot to a gallop both to save energy and to reduce the peak forces experienced by tendons
(Cavagna et al. 1977). In the ghost crab, the exoskeletal strain actually increases fivefold when
the animals switch from a trot to a run (Blickhan et al. 1993). This places a clear constraint on the
construction of the walking legs because they must be able to bear this strain without buckling.
Direct comparison of the maximum forces experienced by the limb and the force required to
cause the limb to buckle reveals a safety factor of about 2.7, which is comparable to that seen in
the limbs of running mammals (Blickhan et al. 1993).
Walking Underwater
Walking is fundamentally different for an organism underwater than for one on land. Fluid
forces such as lift and drag become much more important in the aquatic environment, and they
may be as great or greater than gravitational forces, which are often the only significant ones for
terrestrial pedestrians. Martinez (1996, 2001) has outlined the relevant issues very nicely; here I
summarize those points that appear to have affected crustacean limb morphology.
One major issue facing aquatic pedestrians is drag. While drag is generally ignored for ani-
mals walking in air (however, for an example of how it may affect small organisms, see Full and
Koehl 1993), it is a major force underwater. Drag acts to resist the animal’s locomotion, and so
on energetic grounds one would expect adaptations designed to reduce drag. Related to drag
is the acceleration reaction. This force acts along the axis of flow relative to the animal. It is, in
essence, the force required to accelerate the mass of the organism plus a mass of water that acts
as though it were dragged along with the organism (Denny 1988). Importantly, the acceleration
reaction is proportional to the volume of the organism, unlike lift and drag, which are propor-
tional to the area of the organism facing the flow. This makes the acceleration reaction more
important for large animals than for small ones. Note also that we may consider both drag and
the acceleration reaction for individual limbs as well as for the entire organism. This is because
walking involves regular acceleration and deceleration of limbs as the animal takes each step.
Minimizing both of these forces is probably the reason that decapods tend to be elongated in
the direction in which they walk and to have limbs that are streamlined in the same direction
(Vidal-Gadea et al. 2008). And minimizing acceleration reaction is probably the driving force
behind most crustaceans having very thin walking limbs.
Buoyancy and lift are also important considerations for aquatic walking. Buoyancy reduces
the animal’s effective weight and so makes energy-conserving mechanisms such as those dis-
cussed above difficult. Lift may act in the same manner but adds the potential for the organ-
ism to be swept off the substratum. To the extent that the organism may have to actively grip
the substratum to prevent being swept away, lift can actually prevent walking.
Spider and king crabs appear to have converged on the same set of solutions to these hydro-
dynamic problems. A small body minimizes the effects of lift. And in spider crabs, the fact that
the caudal legs are shorter than the rostral ones means they make less contribution to the overall
drag on the animal (Vidal-Gadea 2008).
Interlimb Coordination
The fact that animals can produce recognizable gaits (e.g., Fig. 9.7) implies the existence of cen-
tral mechanisms for producing coordinated motor output. In fact, decapod crustaceans in par-
ticular have been a popular model for studying these mechanisms for decades (for an excellent
Water Land
Lead 1 Lead 1
Lead 2 Lead 2
Lead 3 Lead 3
Lead 4 Lead 4
Trail 1 Trail 1
Trail 2 Trail 2
Trail 3 Trail 3
Trail 4 Trail 4
–75 –50 –25 0 25 50 75 100 125 150 175 200 225 250 –75 –50 –25 0 25 50 75 100 125 150 175 200 225 250
Percent Time Percent Time
Fig. 9.7
Average footfall patterns for fiddler crabs walking underwater and on land. The bars indicate the time a
leg is in swing, normalized to the duration of the step cycle for leading leg 1. Thus, underwater the dura-
tion of swing is approximately 60% of the step cycle. On land, this decreases to approximately 40%. Since
the crabs walk sideways, legs are marked as leading or trailing and are numbered from front to back. The
chelae are not used in walking and so are not included. The leading thin lines by the bars show the standard
deviation of the onset of swing, and the trailing thin lines show the standard deviation of swing duration.
The figure is based on 32 steps from six animals. Note the “alternating tetrapod” gait, in which one group
of four legs (e.g., leading legs 1 and 3, trailing legs 2 and 4) swing together, while the other four (leading legs
2 and 4, trailing legs 1 and 3) are in stance. Redrawn from Schreiner (2004).
review, see Clarac 2002). While a thorough review of this literature is outside the scope of the
present work, a brief synopsis of this work seems appropriate. In the most general sense, inter-
limb coordination is thought to be the interaction between a centrally produced motor program
and the sensory feedback that arises as the animal moves through its environment. The degree
to which this interaction is biased toward central mechanisms or sensory feedback depends
on both the organism and the behavioral task (Dickinson et al. 2000). Traditionally, mecha-
nisms of interlimb coordination have been studied using intact animals walking on treadmills
(e.g., Cruse and Mü ller 1986) or using in vitro thorax preparations (e.g., Sillar and Skorupski
1986). In the first approach, animals are fixed above a treadmill, which may be motor driven to
control speed, or driven by the animal’s own movement. This allows the collection of data on
the kinematics of limb movements, forces produced by the legs, and, with the implantation of
electromyographic electrodes, data on muscle activation patterns. In these experiments, indi-
vidual limbs are often amputated, or sensory structures ablated, to discern the effects on the
motor pattern. These experiments allowed the inference of a number of “rules” governing inter-
limb coordination (Cruse 1990). For example, during the return stroke of a particular leg, neigh-
boring legs are inhibited from initiating swing. The start of a power stroke by one leg excites the
start of the return stroke in neighboring legs, and coupling between ipsilateral limbs appears to
be stronger than between contralateral limbs (Cruse 1990). However, these experiments do not
provide descriptions of the actual neural circuitry involved. Such data require preparations in
which it is possible to record intracellularly from the central nervous system. These have allowed
descriptions of the neural substrates underlying some of the coordination rules, but we are far
from a complete understanding of this circuitry (for an excellent entry to this literature, see
Cattaert and Le Ray 2001). In particular, we know almost nothing about the presumed “central
pattern generator,” the neural circuit producing the basic motor output that is then sculpted by
these coordination rules (Clarac 2002). This is in stark contrast to the best understood central
pattern generator, the crustacean stomatogastric ganglion (Harris-Warrick et al. 1992).
Skeletal Constraints
A glance at an Olympic sprinter and long-distance runner will show how easy it is for verte-
brates to have very different muscle masses on essentially the same skeleton. The situation is
more complicated for arthropods. Their hard, inf lexible shells mean that the amount of muscle
mass an animal can have is constrained by the size of its skeleton. This has consequences—the
amount of force that a muscle can produce is proportional to its cross-sectional area (Hoyle
1983). To fit a more powerful muscle into a smaller space, many crustaceans organize their
limb muscles in a pinnate fashion, attaching them to a long apodeme (the crustacean equiva-
lent of a tendon). But there are trade-offs here, too: pinnate muscles cannot move a joint as far
as long muscles can, nor can they move it as quickly, since the speed with which a muscle can
contract is controlled by both the myosin isoform and the number of sarcomeres along the
length of the muscle. The more sarcomeres there are in series, the more quickly the muscle
can contract. This is simply a consequence of the fact that a sarcomere is the fundamental
contractile unit of the muscle—if each sarcomere can shorten by 10%, then a muscle with only
one sarcomere can shorten by 10% per unit time, while a muscle with two sarcomeres in series
can shorten by 20%, and so on (Huxley and Niedergerke 1954, Thuma et al. 2007). This may
be part of the reason why spider and king crabs, with their heavily calcified shells, have such
long limbs. The longer lever arms mean that small joint angle changes can still produce large
movements at the ends of the long segments.
“Feet”
An interesting lack of specialization in crustaceans is the absence of a morphological “foot” in

most species. Most insects have a tarsus, which, even if it does not possess specialized attach-
ment structures (claws, adhesive pads), still offers a distributed, compliant surface for the leg
to contact the substratum. This offers an opportunity for energy storage via elastic structures
in the foot or between the foot and the remainder of the limb. The feet of many vertebrates
also allow the center of pressure to move along the foot as the animal steps, saving energy by
making it easier to keep the force vector aligned with the animal’s center of mass (Alexander
2003). These effects can be very important. A bio-inspired robot based on cockroach anatomy
and physiology was originally constructed with legs ending in hard points (much like a brachy-
uran dactyl). It failed to produce realistic locomotion until the tips of the legs were fitted with
compliant endings. Despite the lack of a morphological foot, some brachyurans appear to have
a functional one because many species walk using the propodus-dactyl joint as a strut, at least
when walking slowly or underwater (Schreiner 2004).
The right kind of “feet” may also simplify the control mechanisms required for locomotion.
Spagna et al. (2007) showed that the spines present on the legs and feet of many insects and
spiders provide distributed mechanical feedback that allows the animals to move across chal-
lenging terrain (such as foliage or wire mesh)—the possibility of multiple contact points on each
foot makes the exact foot placement less important. They emphasized this point by challenging
ghost crabs, which have smooth dactyls with no spines at all, to traverse the same kind of ter-
rain, and the crabs failed miserably. When the authors added artificial spines to the crabs’ legs,
the crabs’ performance improved. While most decapods have relatively spine-free limbs, some
(e.g., the king crab and some grapsid crabs) have rather spiny legs and so may be using a similar
strategy as insects and spiders.
The exact morphology of the dactyl may be important for other reasons. Hampton and
Griffiths (2007) compared the abilities of two crabs (Carcinus maenas and Plagusia chabrus)
to cling to rocky shores under wave-swept conditions. They found that Carcinus was much
more likely to be swept off of a rock surface by current, largely because of its shorter and
lighter limbs. But a second factor was the short, more powerful dactyls of Plagusia , which
seemed better adapted to grabbing irregularities in the rocks. The idea that relatively longer
dactyls should be associated with animals that rely on speed for avoiding predators is attrac-
tive and is borne out for some species. For instance, the relative dactyl length is about 10% of
the length of the leg for a grapsid crab (Plagusia), and about 15% for a spider crab, consistent
with the dactyls being important for clinging to the substratum. Considering crabs apparently
more adapted for running, the dactyls of ghost crabs are approximately 25% of the length of
the entire limb, while those of Carcinus maenas are approximately 20%. However, in fiddler
crabs, which are clearly adapted for rapid running, the dactyl length is only 10–15% of the leg.
Similarly, the dactyl is about 15% of leg length in another terrestrial crab, the Christmas Island
red crab (Gecarcoidea natalis).
Energy-Conserving Specializations
Springs can play an important role in energy recovery during locomotion, particularly in larger
mammals and birds (Biewener 2003). They seem to be less important, however, in smaller ani-
mals (Alexander 2003). This may be because the mechanical properties of collagen—the pre-
dominant spring material in most vertebrates—do not operate well at smaller masses. Insects,
however, make abundant use of springs composed of resilin. These are found associated with
many insect wings, where they store energy as the wings decelerate during flapping, and in fleas,
where they are used to slowly accumulate energy that is then rapidly released during a jump.
Resilin is found at the merus-ischium joint in decapod crustaceans (Andersen and Weis-Fogh
1964). This joint has only a flexor muscle, and a resilin spring may act as the functional antago-
nist. Burrows (2009) has shown this precise arrangement in the maxillipeds of crabs and cray-
fish—rhythmic beating movements of the maxilliped are accomplished by a single abductor
muscle and elastic recoil against a resilin spring. Given the diversity of such springs in insects,
and their proven existence in crustaceans, they are likely to be widespread, if only we will look
for them.
An alternate method of elastic energy storage may be to use the muscles themselves. Without
activation of the muscle, the merus-carpus joint in Carcinus maenas has a passive tension suf-
ficient to support the weight of the animal in water, and this has been proposed as an energy-
efficient mechanism for the maintenance of posture (Yox et al. 1982). The tension is thought
to result from the passive properties of either the muscles and/or the connective tissue sheath
which surrounds them. It is not known, however, whether this passive tension can act as an
energy-conserving spring during locomotion.
CONCLUSION
If we really want to understand the functional morphology of crustacean limbs, we need kin-
ematic and dynamic data on locomotion in species other than decapods. I am unaware of such
work in any other crustaceans. The careful work of, in particular, Manton (1977) and Hessler
(1982) on the motions of limbs in nondecapod crustaceans has given us an excellent start, but
these authors relied on purely behavioral observation and so could not elaborate on move-
ments that were too fast, too small, or too obscured to see with the naked eye. Modern video
and force-plate techniques solve all these problems with ease, and the vast array of species
waiting to be examined offer an excellent trove to mine for student projects. The resulting
comparative data should shed light on questions raised above in both functional morphology
and evolution.
A second issue of particular interest is the presence of comparatively very long legs in both
spider crabs and some anomurans. Convergence like this suggests a common solution to a com-
mon problem, and experiments such as those proposed in the previous paragraph will help. But
there are other possibilities. Many crustaceans track chemosensory signals using sensor arrays
located on their feet, and a broader sensor array could allow better tracking (Weissburg and
Duesnbery 2002).
And perhaps the most interesting comparative question, at least to someone who is funda-
mentally a neurobiologist, is this: The conservation of both motor neurons and muscles in the
distal segments of decapod legs is so strong as to be almost stunning. How far across the crusta-
cean phylogeny can we see this conservation? Is it due to a functional constraint, a developmen-
tal one, or something else?
Crustaceans have proven to be organisms providing a rich store of insights, and just plain
cool things, to offer. In an era where there seems to be a rush to concentrate on a small number
of “model” systems, we would do well to remember just how much comparative studies have
taught us.
ACKNOWLEDGMENTS
The work reported here was supported by grants from the National Science Foundation. I thank
Jennifer Schreiner, Andrés Vidal-Gadea, Richard Dewell, and Marc Rinehart for enlightening
discussions on many of these topics. I particularly thank Ívan Hinojosa for his superb help with
the illustrations.
REFERENCES
Adamowicz , S.J., A. Purvis, and M.A. Wills. 2008. Increasing morphological complexity in multiple
parallel lineages of the Crustacea. Proceedings of the National Academy of Sciences of the United
States of America 105:4786 –4791.
Alexander, C.G. 1971. Locomotion in the isopod crustacean, Ligia oceanica (Linn.) Comparative
Biochemistry and Physiology A 42:1039 –1047.
Alexander, R.M. 2003. Principles of animal locomotion. Princeton, Princeton, NJ.
Anderson, B.D., J.W. Schultz , and B.C. Jayne. 1995 . Axial kinematics and muscle activity during terres-
trial locomotion of the centipede Scolopendra heros. Journal of Experimental Biology 198:1185–1195.
Andersen S.O., and T. Weis-Fogh. 1964 . Resilin. A rubberlike protein in arthropod cuticle. Advances in
Insect Physiology 2:1–65.
Angelini, D.R., and T.C. Kaufman. 2005 . Insect appendages and comparative ontogenetics.
Barnes, R.D. 1980. Invertebrate Zoology, 4th ed. Saunders College, Philadelphia .
Belanger J.H., and B.A. Trimmer. 2000. Combined kinematic and electromyographic analyses of proleg
function during crawling in Manduca sexta. Journal of Comparative Physiology A 186:1031–1039.
Biewener, A.A. 2003. Animal locomotion. Oxford University Press, Oxford.
Blickhan R., R.J. Full, and L. Ting. 1993. Exoskeletal strain: Evidence for a trot-gallop transition in rapidly
running ghost crabs. Journal of Experimental Biology 179:301–321.
Burrows, M. 2009. A single muscle moves a crustacean limb joint rhythmically by acting against a spring
containing resilin. BMC Biology 7:27–44.
Burrows, M., and G. Hoyle. 1973. The mechanism of rapid running in the ghost crab Ocypode ceratoph-
thalma. Journal of Experimental Biology 58:327–349.
Cattaert, D., and D. Le Ray . 2001. Adaptive motor control in crayfish. Progress in Neurobiology
63:199 –240.
Cavagna, G.A., N.C. Heglund, and C.R. Taylor. 1977. Mechanical work in terrestrial locomotion:
Two basic mechanisms for minimizing energy expenditure. American Journal of Physiology
233:R243–R261.
Chapman, A. 1961. The terrestrial ostracod of New Zealand, Mesocypris audax sp. nov. Crustaceana
2:255–261.
Clarac , F. 2002. Neurobiology of crustacean walking: From past to future. Pages 119–137 in K. Wiese, edi-
tor. Crustacean experimental systems in neurobiology. Springer, Berlin.
Cribb, B.W., A. Rathmell, R. Charters, R. Rasch, H. Huang , and L.R. Tibbetts. 2009. Structure, composi-
tion and properties of naturally occurring non-calcified crustacean cuticle. Arthropod Structure
Cruse, H. 1990. What mechanisms coordinate leg movement in walking arthropods? Trends in
Neuroscience 13:15–21.
Cruse, H., and U. Mü ller. 1986. Two coupling mechanisms which determine the coordination of ipsilat-
eral legs in the walking crayfish. Journal of Experimental Biology 121:349 –369.
Denny, M.W. 1988. Biology and the mechanics of the wave-swept environment. Princeton University
Press, Princeton, NJ.
Dickinson, M.H., C.T. Farley, R.J. Full, M.A.R. Koehl, R. Kram, and S. Lehman. 2000. How animals
move: An integrative view. Science 288:100 –106.
Frey, D. 1980. The non-swimming chydorid Cladocera of wet forests, with descriptions of a new genus and
two new species. Internationale Revue der gesamten Hydrobiologie und Hydrographie 65:613–641.
Full, R.J., and M.A.R. Koehl. 1993. Drag and lift on running insects. Journal of Experimental Biology
176:89 –101
Full, R.J., and M.S. Tu. 1991. Mechanics of a rapid running insect: Two-, four- and six-legged locomotion.
Hampton, S.L., and C.L. Griffiths. 2007. Why Carcinus maenas cannot get a grip on South Africa’s
wave-exposed coastline. African Journal of Marine Science 29:123–126.
Harris-Warrick R.M., E. Marder, A.I. Selverston, and M. Moulin. 1992. Dynamic biological networks:
The stomatogastric nervous system. MIT Press, Cambridge, MA.
Herreid C.F., and R.J. Full. 1986. Locomotion of hermit crabs (Coenobita compressus) on beach and tread-
mill. Journal of Experimental Biology 120:283–296.
Hessler, R.R. 1982. The structural morphology of walking mechanisms in eumalacostracan crustaceans.
Philosophical Transactions of the Royal Society, Series B 296:245–298.
Holthuis, L.B., C.H.J.M. Fransen, and C. van Achterberg. 1993. The recent genera of the caridean and
stenopodidean shrimps (Crustacea: Decapoda): With an appendix on the order Amphionidacea.
Backhuys, Leiden .
Hoyle, G. 1983. Muscles and their neural control. John Wiley and Sons, New York.
Huxley, A.F., and R. Niedergerke. 1954 . Structural changes in muscle during contraction. Nature
173:971–973.
Lin, H.-T., and B.A. Trimmer. 2010. The substrate as a skeleton: Ground reaction forces from a
soft-bodied legged animal. Journal of Experimental Biology 213:1133–1142.
MacMillan, D.L. 1975 . A physiological analysis of walking in the American lobster, Homarus americanus.
Philosophical Transactions of the Royal Society London, Series B 270:1–59.
Manton, S.M. 1977. The Arthropoda: Habits, functional morphology, and evolution. Clarendon Press,
Oxford.
Martinez , M.M. 1996. Issues for aquatic pedestrian locomotion. American Zoologist 36:619 –627.
Martinez , M.M. 2001. Running in the surf: Hydrodynamics of the shore crab Grapsus tenuicrustatus.
Neues, F., A. Ziegler, and M. Epple. 2007. The composition of the mineralized cuticle in marine and ter-
restrial isopods: A comparative study. CrystEngComm 9:1245–1251.
Schreiner, J. 2004 . Motor control adaptations of amphibious and terrestrial crabs to locomotion on land
and under water. MS thesis, Louisiana State University, Baton Rouge.
Sillar, K.T., and P. Skorupski. 1986. Central input to primary afferent neurons in crayfish, Pacifastacus len-
iusculus, is correlated with rhythmic motor output of thoracic ganglia. Journal of Neurophysiology
55:678–688.
Spagna, J.C., D.I. Goldman, P.-C. Lin, D.E. Koditschek , and R.J. Full. 2007. Distributed mechanical
feedback in arthropods and robots simplifies control of rapid running on challenging terrain.
Bioinspiration and Biomimetics 2:9 –18.
Thuma, J.B., P.I. Harness, T.J. Koehnle, L.G. Morris, and S.L Hooper. 2007. Muscle anatomy is a primary
determinant of muscle relaxation dynamics in the lobster (Panulirus interruptus) stomatogastric
system. Journal of Comparative Physiology A 193:1101–1113.
Vidal-Gadea, A.G. 2008. Neuroethology of forward walking in the spider crab Libinia emarginata . PhD
dissertation, Louisiana State University, Baton Rouge.
Vidal-Gadea, A.G., M.D. Rinehart, and J.H. Belanger. 2008. Skeletal adaptations for forwards and
sideways walking in three species of decapod crustaceans. Arthropod Structure and Development
37:95–108.
Weissburg , M.J., and D.B. Dusenbery 2002. Behavioral observations and computer simulations of blue
crab movement to a chemical source in a controlled turbulent flow. Journal of Experimental Biology
205:3387–3398.
Wiens, T.J., L. Maier, and W. Rathmayer. 1988. The distribution of the common inhibitory neuron in
brachyuran limb musculature. II. Target fibers. Journal of Comparative Physiology A 163:651–664.
Yox , D.P., R.A. DiCaprio, and C.R. Fourtner. 1982. Resting tension and posture in arthropods. Journal of
10
MORPHOLOGICAL ADAPTATIONS FOR DIGGING
AND BURROWING
Zen Faulkes
Abstract
Many crustaceans are highly adapted for digging (submerging into sand or mud) or burrowing
(excavating a structure in sand or mud). The physics of sand and mud pose different problems
for crustaceans that move in them. For example, sand has to be liquefied to dig through it, but
mud has to be cracked. Some of the mechanisms that crustaceans use for digging include shovels,
fans, wedges, and pile drivers. Burrowing often requires some part of the body to act as a basket
to hold sand while it is moved, and occasionally crustaceans generate secretions to stabilize the
resulting chamber. The modular crustacean body plan has resulted in many different appendages
being modified for digging and burrowing, from antennae to uropods and all limbs in between.
Appendages in digging species are often flattened or lined with long setae compared to the homo-
logous appendages in nondigging species. Species that spend long periods submerged in a substra-
tum often show additional adaptations relating to respiration and feeding. Oxygen levels in sand
and mud are low, requiring modifications for ventilation of the gills and respiration. Similarly,
sand- or mud-dwelling crustaceans are often filter feeders or sediment feeders, and setae on or
around the mouthparts often play a critical role in trapping or filtering particles during feeding.
The rigid exoskeleton of crustaceans stands in sharp contrast to other common digging species
that have portions of the body that are soft and flexible, such as molluscs and worms. Research
on digging and burrowing is fragmentary and progressing slowly in part because of the complex
physics of granular materials and elastic materials and also because there are no transparent sand
or mud analogues that allow for direct observations of behavior.
INTRODUCTION
Were it not for dirt, the expressions “as common as sand” or “as cheap as mud” might be clichés.
Sand and mud are found throughout terrestrial and aquatic habitats and often cover immense
276
Morphological Adaptations for Digging and Burrowing 277
areas (Dorgan et al. 2007, Welland 2009). These materials become habitat and home for many
crustaceans, although the research on the interactions between sand and animals living in it
could be politely described as fragmentary. The word burrowing provides an example of how
little is agreed upon. Burrowing can refer either to the excavation of a semipermanent structure,
namely, a burrow (Mukai and Koike 1984, Stamhuis et al. 1996), or to locomotion through a sub-
stratum (Trueman 1970, Savazzi 1986, Dorgan et al. 2006). I advocate using burrowing to refer
only to the construction of a burrow (Bellwood 2002, Faulkes 2006a). Locomotion through a
substratum has usually been called burying (Pinn and Ansell 1993, Bellwood 2002) or digging
(Faulkes and Paul 1997a). I prefer the latter term, if for no other reason than that it sounds less
funereal.
Before exploring adaptations of crustaceans to digging and burrowing, I briefly review the
physics of sand and mud, which creates the constraints for both behaviors. This review focuses
on decapods, not because they are inherently more interesting but because they are the best-
studied taxa.
WHAT IS KNOWN?
Physics of Sand and Mud
Sand and mud are the major substrata in aquatic habitats. Crustaceans inhabit both, although
taxa tend to specialize in one or the other, because the key physical properties of sand and mud
are rather different (Dorgan et al. 2006, Jumars et al. 2006).
Sand is a granular material. The physics of dry granular materials are extremely complex and
the subject of ongoing research (Jaeger et al. 1996a, 1996b). The physics of wet sand, also known
as slurries (Jaeger et al. 1996a), is even less investigated. One of the major properties of granular
materials is that they can sometimes behave as a solid, and they can sometimes behave as a liquid,
albeit an unusual non-Newtonian fluid. Sand can be made to flow by high-frequency agitation.
This allows an animal to penetrate sand, as the liquefaction relieves the weight of overlying sedi-
ment and reduces friction between sand grains (Dorgan et al. 2006). The liquefaction of sand is
sometimes called thixotropy (Chapman 1949, Cubit 1969, Faulkes 2006a), although the term is
arguably better reserved for gels and highly viscous liquids (Barnes 1997). The solidification of
sand, preventing flow, is dilatancy (Jaeger et al. 1996a). To burrow or dig, animals must make
sand transition from a solidlike to a liquidlike state and cause it to flow. To do this, animals must
break stress chains that form between individual particles in resting sand (Jaeger et al. 1996a,
Dorgan et al. 2006). Particles in a stress chain are difficult to move compared to particles that
are not (Dorgan et al. 2006). Stress chains are not uniform at the small scale, and chains may
extend for hundreds of particle lengths. Because most crustaceans are large compared to grain
size, however, the heterogeneous distribution of stress chains will rarely come into play, although
the stress chains will affect the minimum amounts of agitation needed to cause the sand to begin
to flow in a liquidlike way.
Sand can still be penetrated without liquefaction, however. The amount of force needed to
do so varies with the angle of pressure, dropping dramatically when the angle of pressure applied
to the sand falls below 30° (Brown and Trueman 1991). Thus, many crustaceans dig into sand at
shallow angles. Few crustaceans dig into sand that is merely damp rather than wet (but see the
discussion of Tylos, below; Brown and Odendaal 1994).
The size of sand grains could influence the ability of animals to dig. For example, sand par-
ticles about 180 μm in diameter are the easiest to move by flowing water (presumably including
animal-generated currents) (Sanders 1958). Particles smaller than 180 μm, en masse in a substra-
tum, are less likely to be picked up by a current than are larger particles in a substratum, because
substrata made of uniformly small particles are hydrodynamically smooth surfaces. Particles
larger than 180 μm, if picked up by a current, will settle more quickly than smaller ones because
of their greater mass (Sanders 1958). Such physical factors help explain sediment distributions
and could influence the sediment choices of digging species (Sanders 1958, Pinn and Ansell
1993). However, most research on the physics of granular materials focuses on grains larger than
1 mm (Dorgan et al. 2006).
Mud is better described by linear elastic fracture models (Johnson et al. 2002, Jumars et al.
2006) than by granular material physics. Mud has tensile strength, so physics related to fractures
(Mach et al. 2007) are critical when considering mud. For example, two key physical factors
that can help determine if an existing crack will elongate are Young’s modulus (stress-to-strain
ratio) and critical stress intensity fracture (Jumars et al. 2006). Animals that move through
mud commonly create and lengthen cracks, thus fracturing the mud (Dorgan et al. 2006, Che
and Dorgan 2010). To date, studies of the movement of animals in mud have been largely on
soft-bodied organisms (Dorgan et al. 2005, 2007, 2008, Che and Dorgan 2010).
Although many types of sediment are quite uniform in composition, many are complex mix-
tures of different-size particles. The proportion of large particles, such as gravel, can affect bur-
row stability (Palomar et al. 2005), suggesting that burrowing is most likely to be successful in
mud, while digging is the major viable behavior for sands.
Function of Digging and Burrowing
Two hypotheses for the function of digging and burrowing revolve around concealment. First,
digging crustaceans benefit from being concealed from predators. This is often suggested
(Bowers 1964, Coleman 1989) but less often supported by experiment (but see Barshaw and
Able 1990). The burrows of Nephrops norvegicus were hypothesized to be refuges through a proc-
ess of elimination; for example, they are not used for sex or trapping food (Rice and Chapman
1971). Second, ambush predators might similarly benefit by concealing themselves from prey
(McGaw 2005). Ahyong (1997) hypothesized that the long ischium of lysiosquilloid stomato-
pods increased the reach of their raptorial appendages, implying that this allowed these stomat-
opods a greater striking distance while remaining within the confines of the burrow. However,
this hypothesis remains to be tested.
A third hypothesis suggests that individuals save energy by staying immobile for prolonged
times after digging into the substratum (McGaw 2004, 2005). When buried, crabs in the genus
Cancer slow their ventilation rate, and C. productus increases the amount of time it spends with
its heartbeat stopped (McGaw 2004).
Mechanisms
Digging
Crustaceans use several broad mechanisms for digging into sand (Fig. 10.1), including wedges
(Faulkes 2006a), shovels (Faulkes 2006b), fans (Faulkes 2006b), and pile drivers (Bellwood
2002, McGaw 2005). A species may use just one of these mechanisms or several in combina-
tion. These are meant as heuristic, not absolute, categories. For instance, the “shovel” and “fan”
categories no doubt have similarities. In many cases, it is not clear from a description of digging
which term better describes the action of the body part.
Wedges use mechanical leverage to force bulk sand apart. The action of a wedge does not
encourage sand to transition to a liquidlike state, although some small avalanches may occur as
sand is moved. Wedge digging is similar to shoveling (described below) in that both mechanisms
Ocypode
Arenaeus
Lysiosquilla Emerita Ovalipes
Calappa
Lepidopa
Ogyris
Callianassa Callinectes
B C.i C.ii
C.iii C.iv
D.i fr D.ii D.iii D.iv
p4
if
s if
cts th
rp
le
a1 rp
a2
Fig. 10.1.
Digging behavior. (A) Positions of digging and burrowing species in the beach ecosystem, with approx-
imate postures (from Pearse et al. 1942, with permission from the Ecological Society of America). (B)
Brachyuran crabs digging in sand (photo by Martin Thiel). (C) Video frames of Ibacus peronii digging
(see Faulkes 2006a): i, initial probing of substratum with pereopods; ii, body repositioning caused by
abdominal extension; iii, repositioning of legs to brace body movements; iv, animal almost entirely sub-
merged in sand. (D) Nebalia bipes digging. i, ii, movement of appendages (first and second antennae, pleo-
pods, abdominal shaft) indicated by arrows; iii, iv, animal proceeding into the sediment, with rostral plate
diverting mud flow (white arrows). Abbreviations: a1, first antenna; a2, second antenna; cts, cephalotho-
racic shield; fr, furcal rami; le, lateral eye; lf, left lateral pleural fold; p4, fourth pleomere; rp, rostral plate;
s, substratum; th, foliaceous thoracopods (from Vannier et al. (1997), with permission from John Wiley
and Sons).
involve translocation of sand particles, which might be termed excavation (Dorgan et al. 2006).
Crustaceans using only this method of digging tend to be slow. Shrimps and prawns tend to dig
into the sand head first: the narrow cephalothorax acts as a thin wedge (Dall 1958, Egusa and
Yamamoto 1961, Fuss 1964, Pinn and Ansell 1993) driven into sand by pleopod fanning. The
wedge mechanism alone is used by several taxa, including slipper lobsters in the genus Ibacus,
which use the abdomen as a wedge (Jones 1988, Faulkes 2006a; Fig. 10.1C); box crabs in the
genus Calappa, which use the thorax (Bellwood 2002); and amphipods and isopods, which use
the anterior dorsal exoskeleton (i.e., head) as a wedge that is driven by appendages (e.g., gnatho-
pods and pereopods; Watkin 1939, Griffith and Telford 1985, Brown and Trueman 1996, Dorgan
et al. 2006; Fig. 10.1D).
Shovels use thin edges to penetrate sand with low resistance and then use broad edges
to solidify and excavate sand. Crustaceans using shovellike mechanisms to dig may be the
most likely to show morphological specialization, because they largely rely on pereopod seg-
ments that are broad in one direction and narrow in another. Examples of shovels include the
pereopods of hippoid sand crabs (Faulkes and Paul 1997a, 1998) and raninid crabs (Faulkes
2006b).
Virtually any appendage, large or small, has the potential to liquefy sand if it moves fast
enough. Such high-frequency movements might be considered fans, although Jumars et al. (2006)
referred to such quick back-and-forth action as “eraser rubbing.” The leptostracan Nebalia bipes
digs “face first” into mud using rapid fanning movements of its two pairs of antennae (Vannier
et al. 1997). Dendrobranchiate and caridean shrimps use their pleopods as fans when they dig,
thereby scouring the sand bottom, liquefying the sand and suspending some of it in the water
column, which then falls back down on the body (Dall 1958, Fuss 1964, Pinn and Ansell 1993). In
albuneid and blepharipodid sand crabs, the abdomen fans the sand by tail-flipping (Faulkes and
Paul 1997b). Similarly, the small uropods of hippid sand crabs make large, fast excursions that
liquefy the sand during digging (Faulkes and Paul 1997b, Trueman 1970). Fans will generally
have higher frequencies than shovels. For example, the abdomen of albuneid and blepharipodid
sand crabs cycles at a frequency about one and a half times higher than that of pereopods, and
the uropods of mole crabs cycle at about twice the frequency of the pereopods (Faulkes and Paul
1997b).
Some crabs, including Cancer productus (McGaw 2005) and the genus Ovalipes (Bellwood
2002), dig by “body slamming,” which is analogous to a pile driver in its use of fast, forceful
downward movements. This is somewhat surprising, giving that pressing on sand creates and
strengthens force arches, making grains harder to dislodge (Jumars et al. 2006). While the bio-
mechanics of body slamming await a complete description, it seems likely that the crab’s force-
ful movements generate enough water flow to liquefy the top layer of sand and force it outward,
away from the center of the thorax, rather than putting stress on the sand particles directly. The
particles suspended in water would then settle back on the carapace, concealing it.
Burrowing
The main mechanism needed to create a burrow might be a “basket” that can pick up and move
sediment. Many appendages can serve this role, including the chelae alone (Savazzi 1985), the
first two pairs of pereopods (Coelho et al. 2000a), or the gnathopods (Atkinson et al. 1982).
Although the digging mechanisms listed above are also ways that a crustacean might begin
a burrow, making the final structure semipermanent requires something to prevent the bur-
row from collapsing (i.e., to keep the sand or mud in a solidlike state). This can be done simply
by compacting sand or mud, thereby creating dilatancy (Fig. 10.2), or by using another mate-
rial, such as a sticky secretion. Corophium species use small strands of “amphipod silk,” which
Barnard et al. (1988) described as originating from the dactyls. Similarly, some stomatopods are
A B.i
7 4
B.ii 7 B.iii
B3
B2
4
B1
B
1 7
Anterior
10 mm
Fig. 10.2.
Burrowing behavior. (A) Ocypode quadrata excavating a burrow, holding sand in its chelae (from Savazzi
1985, with permission from John Wiley and Sons). (B) Tylos granulatus excavating a burrow. i, entry into
the sand (see long arrow above head): single arrows show movement of pereopods, and the double-headed
arrow shows up-and-down movement of head into the sand; ii, movement of sand: the burrow is exca-
vated by pereopods 1–3, while the head consolidates the burrow walls with up-and-down movements (see
double-headed arrow); iii, dorsal view before body is rotated in burrow: pereopods 4–6 push backward,
and sand is ejected by pereopod 7. Abbreviations: 1–7, pereopods; B1–B3, boluses of sand (from Brown and
Trueman 1996, courtesy of Brill).
thought to solidify their burrows with secretions “presumably from the mouth area” (Dingle
and Caldwell 1978). Thalassinid shrimp are variable in this regard: some use mucus to line their
burrows (Mukai and Koike 1984) secreted by “rosette glands” in the appendages (Dworschak
1998), whereas others do not appear to secrete mucus (Torres et al. 1977).
Morphological Specializations for Digging and Burrowing
Body Shape
There is no simple correlation between body shape and digging (Bellwood 2002). Some
sand-dwelling amphipods are laterally compressed, which suggests that this compression left
amphipods poorly suited to terrestrial locomotion (Bowers 1964). Other amphipods living in
sand tend to be wider than those not living in sand (Bousfield 1970). Jumars et al. (2006), sug-
gesting that some digging amphipods had shapes that “obviously” use discoid cracks. Scyllarids
are dorsoventrally compressed (Faulkes 2006a). Albuneid sand crabs tend toward a somewhat
square carapace when viewed dorsally (Boyko 2002), whereas Emerita are ovoid and have a
slightly elongated carapace (McLay and Osborne 1985). Cumaceans have an enlarged carapace,
which is correlated with digging (Watling 1981).
Suggested relationships between body shape and burrowing are better described as intuitive
suggestions rather than rigorous analyses. Savazzi (1986) suggested that burrowers tended to
have elongated bodies, as small cross sections would make it possible to build narrow burrows,
which are both less likely to collapse and less likely to be invaded by predators. A reduced, lightly
A 5 mm B C
Pull of
scour
Sediment
Sand
Cross orientation
pressure
Perimeter smoothing
Frictional asymmetry
Fig. 10.3.
Cuticular terraces. (A) Emerita analoga, with anterior at top (from Seilacher 1973, with permission from
Oxford University Press). Terrace ridges are aligned at right angles to the direction of movement (cross
orientation), and ridge edges are shallow along the leading edge of movement (frictional asymmetry).
Ridges are less common and less pronounced where the carapace is widest (perimeter smoothing), result-
ing in a more even distribution of friction over the body’s surface. (B) Scanning electron micrograph of
cuticular terraces on front region of Emerita analoga carapace (from Schmalfuss 1978, with permission
from Springer Science + Business Media). (C) Mechanism of action of cuticular terraces (redrawn from
Schmalfuss 1978).
calcified carapace and exoskeleton in stomatopods (Glaessner 1957, Ahyong 1997) and thalassi-
nid shrimps (Glaessner 1957) may be an adaptation to burrowing: greater body flexibility would
allow animals to move around within the burrow rather than needing to leave it. Presumably,
using the burrow for protection would be more energetically efficient than growing a heavy
exoskeleton.
Cuticular Terraces
Cuticular terraces are directed rough surfaces that provide little resistance to materials moving
along their surface in one direction but great resistance to materials moving in the opposite
direction (Fig. 10.3). Terraces on digging and burrowing crustaceans provide friction against
the nonpreferred direction of movement (Seilacher 1973, Schmalfuss 1978, Vannier et al. 1997).
In most digging crustaceans, the friction from terraces probably prevents backward slippage
during digging (Seilacher 1973, Schmalfuss 1978) and assists individuals from being dislodged
by wave action (Schmalfuss 1978). The degree of friction, however, depends more on the grain
size of the sediment than the shape of the terrace (Savazzi and Huazhang 1994). In small crusta-
ceans, such as the leptostracan Nebalia bipes, the small size of terraces suggests they may not be
effective in creating direction friction and may have other sensory or hydrodynamic functions
(Vannier et al. 1997). Burrowing crustaceans also benefit from the additional friction of terraces
by pressing their legs against the burrow’s side when disturbed; thus, terraces reduce the chance
of the animal being removed from the burrow by predators (Savazzi 1985).
Pereopods
Perhaps the most readily recognizable adaptations for digging are modifications to the main
walking legs, that is, pereopods 2–5 (Fig. 10.4). The most common specialization is to have
A B C
Cx B-I M Cx Cx
C B-I M
M B-I
C C
P P P
D
D
D
Fig. 10.4.
Second pereopods of walking and digging species. (A) Munida quadrispina , which has a typical decapod
walking leg. (B) Blepharipoda occidentalis, showing the shovel-shaped dactyl typical of digging species.
(C) Emerita analoga, showing the f lattened dactyls and thickened limb segments. Abbreviations: Cx,
coxa; B-I, basi-ischium; M, merus; C, carpus; P, propodus; D, dactyl.
flattened dactyls, which can be seen in hippoid sand crabs (Faulkes and Paul 1997a, 1998, Boyko
2002) and many brachyuran crabs (Bellwood 2002, McGaw 2005, Faulkes 2006b). Indeed, in
some species, such as Orithyidae, burrowing behavior has been inferred from the presence of
flattened dactyls alone (Bellwood 2002). This may not be wise, as flattened dactyls can also
be used for swimming (Hartnoll 1971, Faulkes and Paul 1997b). Some digging amphipods are
described as having no dactyls on the pereopods (Bousfield 1970).
The individual segments of the pereopods are often robust and are shorter and wider than
the homologous segments in walking species (Bousfield 1970, Griffith and Telford 1985). Emerita
species were described as having “reduced” limbs (McLay and Osborne 1985), but it is important
to note that its leg segments, while short, are very thick (Fig. 10.4). This is not surprising, given
the extreme loads that a digging crustacean encounters: large volumes of muscle are needed to
power the limbs. Given this, the endophragmal skeleton should also be modified, because it pro-
vides attachment points for muscles moving the two most proximal limb segments (Antonsen
and Paul 2000). The morphologies of endophragmal skeletons are rarely described, probably
because such descriptions would require time-consuming dissections that would destroy speci-
mens, a particular problem for rare species. Schram (1986) provided one of the few attempts to
document variation of endophragmal skeletons; unfortunately, examples of hippoid sand crabs
presented therein were misidentified (Boyko 2002).
In burrowing species, pereopod adaptations are often subtle at best. That there are so few sug-
gested modifications to the limbs of burrowing species indicates the flexibility and generality of
the basic pereopod structure. Hessler (1982) noted that the limbs of burrowing species may have
the distal segments bent so as to enhance resistance of the tip to the surrounding medium.
Abdomen
In dendrobranchiate (Dall 1958, Egusa and Yamamoto 1961, Fuss 1964) and caridean shrimp
(Pearse et al. 1942, Pinn and Ansell 1993), the abdomen is large and laterally compressed. Pearse
et al. (1942) considered Ogyrides alphaerostris a “peculiar” digger in part because of its large
abdomen. The pleopods almost always play an important role in digging in these species, but no
author has remarked on any particular specialization associated with this. Haustoriid amphi-
pods move sand using their pleopods (Dennell 1933), which Bousfield (1970) describes as “pow-
erfully modified,” although how they are modified is not specified.
Scyllarid lobsters (Faulkes 2006a) also have large abdomens, but these are dorsoventrally
compressed. Unlike shrimp, the pleopods play no role in digging in scyllarids; instead, the abdo-
men acts as a wedge, and digging sequences are occasionally terminated with a short series of
tail-flips.
Anomuran and brachyuran digging species have small abdomens, although abdominal
reduction is typical of most species in these taxa, not just the diggers. The abdomens can play
an important role in digging, however. Blepharipodid and albuneid sand crabs perform vigor-
ous tail-flipping during digging (Faulkes and Paul 1997b). Similarly, Ranina ranina rhythmically
move the abdomen during digging, even though the abdomen is relatively inflexible (Faulkes
2006b).
Hippid mole crabs beat their uropods during digging, but the rest of the abdomen remains
still (Trueman 1970, Faulkes and Paul 1997b). The tail fan has undergone huge skeletal, muscu-
lar, and neural modifications (Paul 1981a, 1991, Paul et al. 1985, Paul and Wilson 1994), including
enlargement of the telson to house muscles powering the uropods.
Pleopods of burrowing species, notably thalassinid shrimps, are frequently enlarged because
of their roles in excavating and maintaining the burrow by fanning away sand particles and in
oxygenating the burrow by fanning water through it and ventilating it with new water (Torres
et al. 1977). In others, the pleopods become one of the main appendages used in excavating sand
from burrows.
Ventilatory Apparatus
Crustaceans are aerobic organisms, but oxygen concentration in sediments falls sharply over
just a few millimeters from the interface with open water (Jorgensen and Revsbech 1985),
including tubes within the sediment (Meyers et al. 1988). Thus, the need to have oxygenated
water flowing over the gills can significantly constrain digging or burrowing behavior.
In nondigging decapods, water is typically drawn up between the walking legs or through
openings dorsal to the basis of the claws and then flows forward into the branchial chambers and
out through the buccal area. Many digging decapods reverse this pattern; that is, water flows in
an anterior to posterior direction. Several genera of shrimp (Dall 1958, Egusa and Yamamoto
1961) and brachyuran crabs (Pearse et al. 1942, Caine 1974, McLay and Osborne 1985) draw water
in around the side and back margins of the carapace and pump it out at the anterior end. In
Ovalipes guadalpensis, the morphological features enabling this reversed current include dense
setae on the maxillipeds, second antennae, and bases of pereopods, which filter the water twice
to prevent entry of sand; elongation of the distal portion of the merus of the third maxillipeds and
the endopodite of the first maxillipeds; fusion of the second and third segments of the second
antenna; and relatively small openings for water flow to the gill chamber (Milne-Edwards open-
ings, dorsal to the basis of the chelipeds), which can be closed (Caine 1974; see also Davidson
and Taylor 1995 for another Ovalipes species).
To create spaces where water can flow to the gills, some shrimp use the antennal scales and
antennules (Egusa and Yamamoto 1961), which often have dense interlocking setae to keep sand
out (Dall 1958). Some anomuran and brachyuran crabs create such spaces by placing the claws in
front of the mouth (Pearse et al. 1942, Bellwood 2002). Some brachyuran crabs (Bellwood 2002)
and Emerita species (Pearse et al. 1942) form a breathing tube using antennae, with interlocking
setae though which the water flows while the crab is buried. That many crustaceans dig into sand
backward (Faulkes and Paul 1997a, Faulkes 2006a, 2006b) may be advantageous to maintaining
such gaps around their mouthparts for water flow, rather than backward motion providing a
mechanical advantage.
Burrowing species face similar problems with low-oxygen conditions. One adaptation for
this is to increase the respiratory surface area available. In thalassinid shrimp, gill surface area
correlates with burrowing strategy and amount of hypoxia (Astall et al. 1997a). Further, because
the burrow itself forms a pathway for water flow, ventilating the burrow with water with higher
oxygen content from above the sand becomes a viable solution. The pleopods of stomatopods
(Dingle and Caldwell 1978) and thalassinid shrimp (Torres et al. 1977, Felder 1979, Astall et al.
1997b, Stamhuis and Videler 1998) are often used to keep water flowing through their burrows.
Some burrows, such as those of the alpheid Alpheus macellarius (Palomar et al. 2005) and the
thalassinid Corallianassa longiventris (Dworschak et al. 2006), are often closed at one or both
ends, so their burrows are not ventilatory pathways.
Setae
Setae are commonly found on appendages of many digging and burrowing species (Fig. 10.5).
Classifying setae and their functions is complex (see chapter 6 in this volume): they have many
morphologies and functions, including a variety of sensory functions (Bock and Paul 2009,
Stamhuis et al. 1998). The size of setae compared to sand and mud particles may make setae
ideally suited to act as screens, sieves, and filters, blocking sand while allowing water to pass
through. As noted above, setae can be key to filtering sand, which is necessary to maintain water
flow for ventilation and gas exchange (Caine 1974).
A Oral
Esophagus
Mandibles 4. Ingestion
Accumulated Maxilla 1
Maxilla 2 3. Combing setae → transport
small particles
Maxilliped 1
2. Selective retention
Maxilliped 2
Maxilliped 3
Suspension
1. Stirring → floatation
Sediment
State Process
Aboral
B C D
1 mm 10 mm
Fig. 10.5.
Setae. (A) Use of setose mouthparts during sediment feeding of Callianassa subterranea (from Stamhuis
et al. 1998, with kind permission from Springer Science + Business Media). (B) Setose antennae of Emerita
analoga extended for feeding (see Efford 1966). (C) Profile of Chiridotea coeca, showing numerous setae
lining the limbs (from Griffith and Telford 1985, reprinted with permission from the Marine Biological
Laboratory, Woods Hole, MA). (D) Setose second pereopods of Blepharipoda occidentalis (from Boyko
2002, courtesy of the American Museum of Natural History).
Setae are often the key morphological features for feeding in sediment-living crustaceans,
which usually have two broad strategies for getting food: deposit feeding (Stamhuis et al. 1998)
and filter feeding (Pearse et al. 1942, Efford 1966, Dworschak 1987; but see Matthews 1955 for
an example of an active scavenger). Setae are important for both strategies because they can
be used both for capturing particles of many sizes (e.g., by forming a basketlike structure) and
filtering out large particles (e.g., by acting as a sieve; Nickell et al. 1998, Coelho et al. 2000b).
Both strategies can be found distributed across many thalassinid shrimp species, which tend to
specialize in one or the other (Torres et al. 1977, Dworschak 1987, Nickell et al. 1998, Stamhuis
et al. 1998, Coelho et al. 2000b, Coelho and de Almeida Rodrigues 2001), although some spe-
cies do both. Similarly, the amphipod Corophium volutator feeds both on deposited sediment
particles and on particles obtained from the overlying water (Nielsen and Kofoed 1982, Møller
and Riisgå rd 2006, Riisgå rd and Schotge 2007) and uses setae to scrape food off individual
sand grains when deposit feeding (Nielsen and Kofoed 1982).
Setae may be used to increase surface area needed for locomotion (Griffith and Telford 1985,
Boyko 2002). Breaking stress chains or force arches between sand grains is facilitated by protu-
berances of similar size as the sand grains (Jumars et al. 2006). If setae function to break stress
chains in this way, there may be a relationship between the size of setae and sand grains on dig-
ging appendages. In the isopod Chiridotea coeca, the extensive setae lining the pereopods were
hypothesized to prevent sand from falling between the legs and under the body, which would
impede pereopod movement during digging (Griffith and Telford 1985). This hypothesis was
supported by showing that the distance between setae remained roughly constant as animals
grew, as expected for a mechanism to keep sand out.
Eyes
Crustaceans’ stalked eyes seem preadapted for digging and burrowing lifestyles. The eyes can
remain just above the sand surface, acting like a periscope when the rest of the body is sub-
merged (Glantz and Barnes 2002). Nevertheless, many crustaceans living in sand beaches
have small eyes (MacGinitie 1934, Pearse et al. 1942), the reduction of which seems more pro-
nounced in more specialized diggers. In the albuneid sand crabs, the ocular peduncles are flat-
tened and sometimes have no visible pigments (Boyko 2002). Modification to the eyes takes an
extreme form in the albuneid genus Zygopa, in which the peduncles are fused (Boyko 2002). In
contrast, the peduncles of the albuneid genus Stemonopa are lengthy, causing Boyko (2002) to
wonder “how the animal is able to move through the sediment without causing damage to the
peduncles.”
Color
Because the function of digging appears to revolve around concealment, it is perhaps not sur-
prising that many digging crustaceans have uniform coloration that would reduce conspicu-
ousness (Pearse et al. 1942, McLay and Osborne 1985, Seilacher 2007). Many digging animals
are white, tan, or cream, perhaps with flecks of other colors (Pearse et al. 1942). Some species
match the color of the sands they dig into. Several species of Hippa generally match the gen-
eral color of the beach they inhabit, presumably for camouflage purposes: white coral beaches
are inhabited by ivory-white individuals, while black volcanic beaches are populated by black
individuals (Wenner 1972, Bauchau and Passelecq-Gér ì n 1987). When placed in a new substra-
tum, individuals can change carapace color over successive molts (Wenner 1972, Bauchau and
Passelecq-Gér ì n 1987). In contrast, Lepidopa benedicti collected on a single uniformly colored
beach can vary from dark gray to white (Nasir and Faulkes 2011). Their ability to change color
by molting is untested.
Species with No Obvious Specializations
Some crustaceans have no obvious morphological specializations for digging or burrowing.

Examples of generalized digging species include many penaeid (Dall 1958, Egusa and Yamamoto
1961, Fuss 1964) and caridean (Pearse et al. 1942, Pinn and Ansell 1993) shrimps and brachyuran
crabs (Bellwood 2002; e.g., Fig. 10.1B). There are probably many species that are not recognized
as diggers because of lack of specializations.
Similarly, and more emphatically, many crustacean species that build burrows have no par-
ticular morphological specializations for the task. Behavior, rather than morphology, allows
these species to build burrows. For example, a major review of functional morphology of sto-
matopods lists nothing in regard to burrowing or burrows (Kunze 1981). Other examples include
alpheid snapping shrimps (Karplus 1987), astacidean crayfish and lobsters (Rice and Chapman
1971, Grow and Merchant 1980, Correia and Ferreira 1995), brachyuran crabs (Rice and Chapman
1971, Savazzi 1985), and amphipods (Brown and Trueman 1996). Most burrowing species with no
obvious morphological specializations create their burrows using their maxillipeds (e.g., amphi-
pods: Bowers 1964, Nelson 1980, Atkinson et al. 1982, Coleman 1989), pereopods (e.g., brachy-
urans: Dembowski 1926, Barrass 1963, Schmalfuss 1978, Savazzi 1985; astacideans: Rice and
Chapman 1971; amphipods: Bowers 1964, Brown and Trueman 1996; alpheid shrimp: Karplus
1987, Palomar et al. 2005; hermit crabs: Rebach 1974), or some combination of the two. Sand is
scooped up by these appendages, removed, and deposited some distance away on the sediment
surface until a burrow is formed. In many cases, the pleopods are fanned to move sand parti-
cles for short distances and clear out tunnels made during burrowing (Rice and Chapman 1971,
Dingle and Caldwell 1978).
Case Studies
Digger
Mole crabs in the genus Emerita are found in sand beaches worldwide. When all size classes are
considered, including very small juveniles, they can occur in densities of thousands per square
meter of beach (Efford 1965, Perry 1980, Veloso and Cardoso 1999). Emerita analoga is described
here, but the behavior should be almost the same for all species in the genus, which are quite dif-
ficult to distinguish from each other anatomically.
Emerita analoga swim backward by uropod beating (Paul 1971a, 1981b), a fast, directional
form of locomotion that the crabs use to remain in the swash zone where they reside (Contreras
et al. 1999, Veloso and Cardoso 1999, Dugan et al. 2000, Jaramillo et al. 2000, Forward et al.
2005). The uropods are highly modified from the decapod tail-fan ground plan (Paul 1971b,
1981a, 1991). Although they are small, the uropods make larger excursions than any other
appendage during digging (Faulkes and Paul 1997b) and, by bilaterally synchronized beat-
ing, allow an individual to swim down to the surface of the sand. When an individual touches
sand, the uropods continue beating in bilateral synchrony at frequencies of around 3–8 Hz,
liquefying the sand (Faulkes and Paul 1997a). Contact with the sand, no doubt detected by
numerous innervated setae (Bock and Paul 2009), triggers rhythmic activity of the second,
third, and fourth pairs of pereopods, which are robust and have f lattened dactyls (the first
pereopods are used primarily as rudders during swimming and little for digging; the fifth
are very small and not used in locomotion, as is typical of anomurans). The fourth pair of
pereopods is initially closely linked to the uropods, moving in bilateral synchrony at about
the same frequency as the uropods. The frequencies of the uropods and fourth pereopods are
about double those of the second and third pairs of pereopods, which move in bilateral alter-
nation (Faulkes and Paul 1997a, 1997b), making for a very complex interplay of coordinated
movement. The second and third pairs of pereopods act as shovels: the legs are extended
away from the body and scoop sand forward relative to the crab and then are brought back
toward the body in a low-drag, feathered position. As an individual descends into sand, the
frequency of the movements of the uropods and fourth pereopods slows down and begins to
match that of the second and third pereopods, and the fourth pereopods tend to stop moving
in bilateral synchrony (Faulkes and Paul 1997b).
Once submerged, the cuticular terraces along the carapace (Seilacher 1973, Schmalfuss 1978)
keep individuals secured in the turbulent, high-energy environment of the swash zone. Emerita
analoga normally digs into the sand so it is oriented toward the ocean. When waves recede, an
animal will extend its long, plumose antennae from behind the third maxillipeds, which it uses
for filter feeding (MacGinitie 1938, Efford 1966).
Burrowers
Aquatic Burrower
Thalassinid shrimps are among the best-known and most abundant burrowing crustaceans.
The following description is largely based on Coelho et al. (2000a). Upogebia omissa gath-
ers sediment using the dactyls of the first and second pereopods, which is held in a “basket”
of setae, with setae on the first pereopods forming the sides and setae of the second pere-
opods forming the bottom. The gathered sediment is moved out of the burrow opening and
deposited. The shrimp will leave the burrow only in the very early stages of burrowing until
a chamber is formed, 3–4 cm below the surface, at which point the animal can reverse direc-
tion within the burrow by bending its abdomen over the cephalothorax and no longer needs
to leave the burrow. In other species, the ability of the setae on the first and second pereopods
to form a basket can also be important in feeding (Dworschak 1987). Long-term burrow sta-
bility is achieved by a variety of mechanisms, including pleopod beating (Astall et al. 1997b,
Stamhuis and Videler 1998), which removes particles that could block passages, and mucus
secretions (Dworschak 1998).
Semiterrestrial Burrower
Tylos granulatus is an example of a semiterrestrial burrower (Fig. 10.2B). This description of
burrowing is based on Brown and Trueman (1996). Individuals start burrowing in an irregu-
larity of the surface or where sand has been disturbed, where the animal can bend its head
down into the sand. The head presses into the sand and moves up and down, compacting
sand into burrow walls, which can take up to 3 s, after which the animal begins to burrow
downward. Initially, pereopods 1–3 move the substratum at 2–4 Hz, often extending laterally
past the tergal folds of the pereon to excavate sand. The head and pereopods 4–7 support the
body, and the maxillipeds are not used. It takes approximately 12 s for the body to pass into
the sand. Sand is passed backward in the midline from the anterior limbs and, with the sand
excavated by pereopods 2 and 3, forms a compact ball that is pushed back by the posterior
pereopods. When sand begins to move backward, all pereopods begin digging, which can
continue for several minutes. During digging, sand accumulates in small heaps at the sur-
face, but some sand stays in the burrow, partially blocking the animal. As a bolus of sand is
pushed back by the seventh pereopods, the body is forced into the sand by the thrust of pere-
opods 4–7. Pereopods 1–3 continue excavating sand, which may contribute to the downward
thrust. An animal will often rotate somewhat within the burrow as it progresses, stepwise,
into the sand.
COMPARISON WITH OTHER TAXA
The dominant taxa on sandy beaches besides crustaceans are molluscs and polychaetes
(McLachlan 1983); we know less about the use of sandy and muddy environments in subtidal
regions. Unfortunately, the literature on digging in these other taxa is as fragmentary as it is for
crustaceans.
Unlike hard-bodied crustaceans, molluscan and polychaete diggers have at least some part
of the body that is flexible: shelled molluscs dig using their foot, and squid, octopuses, and
polychaete worms are entirely soft. Octopuses simply use their arms as shovels (von Boletzky
1996), but in most other cases, the soft body regions allow for peristaltic muscle contractions,
which is advantageous to creating and propagating cracks in mud (Dorgan et al. 2006). The
basic digging mechanism for worms and molluscs is similar (Trueman 1966), consisting of
establishing an anchor, extending a protrusion into the sand, establishing a new anchor, and
then contracting longitudinal muscles to pull the body down into sand (Jumars et al. 2006).
A major difference between crustaceans and some other taxa is that other taxa have a
mechanism available to them for digging that crustaceans apparently do not: pumps. Pumps
literally inject water into sand. This separates many of the grain particles from each other and
allows the particles to move as a fluid (Dorgan et al. 2006). The potential difference between
fluidization and fanning is that it is possible that fluidizing could be accomplished by pump-
ing water without high-frequency appendage movements. For example, some molluscs that
inject water into sand are squid, cuttlefish, and bivalves (Mather 1986, Trueman et al. 1966, von
Boletzky 1996).
Bivalve molluscs are perhaps one of the best-investigated sand diggers outside crustaceans
(Ansell and Trueman 1967, Savazzi 1989, Winter and Hosoi 2011), particularly the genus Donax,
which are rapid diggers (reviewed in Ansell 1983). Surprisingly, the fine structure of the shell
surface is similar to that of digging and burrowing crustaceans in containing terraces that pro-
vide unidirectional friction (Seilacher 1973, Savazzi 1989). The wedge-shaped shell plays a major
role in allowing these clams to dig into sand (Trueman et al. 1966) and, secondarily, in Donax,
allows individuals to be carried along the beach by wave action (Ellers 1995).
FUTURE DIRECTIONS
It is no accident that “clear as mud” is always meant ironically. This highlights a depressingly
simple, but major, obstacle to studying digging and burrowing: we can’t see what’s going on.
Sand or mud blocks the view, so observing digging behavior has been a consistent challenge
(Dorgan et al. 2007). X-rays can provide information on sediment disturbance (Howard 1968,
Gingras et al. 2008) but little information on detailed behavior. Several transparent alter-
natives to sand and mud have been proposed. Cryolite, proposed as a material for studying
sand-dwelling organisms (Josephson and Flessa 1972), is toxic (Hunter 1982). Methylcellulose
(Hunter 1982) and gelatin (Dorgan et al. 2005) have served as analogues for very fine mud.
Alternatively, for relatively large crustaceans, electromyograms of muscle activity have revealed
elements of behavior that are not readily visible (Faulkes and Paul 1997a, 1997b, Faulkes 2006b).
Many interesting questions in digging revolve around the movements of many joints at once,
however, which requires making several electromyograms simultaneously, which is a techni-
cally challenging task for an animal moving through a substratum.
Given that there is active research on the physics of granular materials, it would seem that
there is great potential for biologists and physicists to collaborate in developing more quantitative
approaches to investigate digging. For example, it may be possible to generate models describ-
ing the forces that organisms need to make sand flow, which is critical for most animals to be
able to dig.
That said, more basic natural history and ecology of digging species are also needed. Sandy
habitats have often been considered uninteresting ecological “deserts” (McLachlan 1983), and
organisms living in them have not received as much attention as they might. Vast stretches
of ocean floor are covered in mud, often rich with nutrients. Many crustaceans have become
adept at exploiting this habitat and thus become important agents of global elemental cycles
(e.g., carbon).
REFERENCES
Ahyong , S.T. 1997. Phylogenetic analysis of the Stomatopoda (Malacostraca). Journal of Crustacean
Biology 17:695–715.
Ansell, A.D. 1983. The biology of the genus Donax . Pages 607–635 in A. McLachlan and T. Erasmus, edi-
tors. Sandy beaches as ecosystems. Dr. W. Junk , The Hague.
Ansell, A.D., and E.R. Trueman. 1967. Burrowing in Mercenaria mercenaria (L.) (Bivalvia, Veneridae).
Antonsen, B.L., and D.H. Paul. 2000. The leg depressor and levator muscles in the squat lobster Munida
quadrispina (Galatheidae) and the crayfish Procambarus clarkii (Astacidae) have multiple heads
with potentially different functions. Brain, Behavior and Evolution 56:63–85.
Astall, C.A., S.J. Anderson, A.C. Taylor, and R.J.A. Atkinson. 1997a . Comparative studies of the branchial
morphology, gill area and gill ultrastructure of some thalassinidean mud-shrimps (Crustacea:
Decapoda: Thalassinidea). Journal of Zoology 241:665–688.
Astall, C.M., A.C. Taylor, and R.J.A. Atkinson. 1997b. Behavioural and physiological implications of a
burrow-dwelling lifestyle for two species of upogebiid mud-shrimp (Crustacea: Thalassinidea).
Estuarine, Coastal and Shelf Science 44:155–168.
Atkinson, R.J.A., P.G. Moore, and P.J. Morgan. 1982. The burrows and burrowing behaviour of Maera
loveni (Crustacea: Amphipoda). Journal of Zoology 198:399 –416.
Barnard, J.L., J.D. Thomas, and K.B. Sandved. 1988. Behavior of gammaridean Amphipoda: Corophium,
Grandidierella, Podocerus, and Gibberosus (American Megaluropus) in Florida. Crustaceana
Barnes, H.A. 1997. Thixotropy—a review. Journal of Non-Newtonian Fluid Mechanics 70:1–33.
Barrass, R. 1963. The burrows of Ocypode ceratophthalmus (Pallas) (Crustacea, Ocypodidae) on a tidal
wave beach at Inhaca Island, Moçambique. Journal of Animal Ecology 32:73–85.
Barshaw, D.E., and K.W. Able. 1990. Deep burial as a refuge for lady crabs Ovalipes ocellatus: Comparisons
with blue crabs Callinectes sapidus. Marine Ecology Progress Series 66:75–79.
Bauchau, A.G., and E. Passelecq-Gér ì n. 1987. Morphological color changes in anomuran decapods of the
genus Hippa. Indo-Malayan Zoology 4:135–144.
Bellwood, O. 2002. The occurrence, mechanics and significance of burying behaviour in crabs
(Crustacea: Brachyura). Journal of Natural History 36:1223–1238.
Bock , N.L., and D.H. Paul. 2009. Habitat-related divergence among tailfan sensory systems in reptantian
decapod crustaceans. Brain, Behavior and Evolution 73:188 –205.
Bousfield, E.L. 1970. Adaptive radiation in sand-burrowing amphipod crustaceans. Chesapeake Science
11:143–154.
Bowers, D.E. 1964 . Natural history of two beach hoppers of the genus Orchestoidea (Crustacea:
Amphipoda) with reference to their complemental distribution. Ecology 45:678 –696.
Boyko, C.B. 2002. A worldwide revision of the recent and fossil sand crabs of the Albuneidae Stimpson
and Blepharipodidae, new family (Crustacea, Decapoda, Anomura, Hippoidea). Bulletin of the
American Museum of Natural History 272:1–396.
Brown, A.C., and F.J. Odendaal. 1994 . The biology of oniscid Isopoda of the genus Tylos. Advances in
Brown, A.C., and E.R. Trueman. 1991. Burrowing of sandy-beach molluscs in relation to penetrability of
the substratum. Journal of Molluscan Studies 57:134–136.
Brown, A.C., and E.R. Trueman. 1996. Burrowing behaviour and cost in the sandy-beach oniscid isopod
Tylos granulatus Krauss, 1843. Crustaceana 69:425–437.
Caine, E.A. 1974 . Feeding of Ovalipes guadulpensis (Saussure) (Decapoda: Brachyura: Portunidae), and
morphological adaptations to a burrowing existence. Biological Bulletin 147:550–559.
Chapman, G. 1949. The thixotropy and dilatancy of a marine soil. Journal of the Marine Biological
Che, J., and K.M. Dorgan. 2010. Mechanics and kinematics of backward burrowing by the polychaete
Cirriformia moorei. Journal of Experimental Biology 213:4272–4277.
Coelho, V.R., R.A. Cooper, and S. de A. Rodrigues. 2000a . Burrow morphology and behavior of the mud
shrimp Upogebia omissa (Decapoda: Thalassinidea: Upogebiidae). Marine Ecology Progress Series
200:229 –240.
Coelho, V.R., and S.A. Rodrigues. 2001. Trophic behaviour and functional morphology of the feeding
appendages of the laomediid shrimp Axianassa australis (Crustacea: Decapoda: Thalassinidea).
Journal of the Marine Biological Association of the UK 81:441–454.
Coelho, V.R., A.B. Williams, and S.A. Rodrigues. 2000b. Trophic strategies and functional morphol-
ogy of feeding appendages, with emphasis on setae, of Upogebia omissa and Pomatogebia operculata
(Decapoda: Thalassinidea: Upogebiidae). Zoological Journal of the Linnean Society 130:567–602.
Coleman, C.O. 1989. Burrowing, grooming, and feeding behaviour of Paraceradocus, an antarctic amphi-
Contreras, H., O. Defeo, and E. Jaramillo. 1999. Life history of Emerita analoga (Stimpson) (Anomura,
Hippidae) in a sandy beach of south central Chile. Estuarine, Coastal and Shelf Science 48:101–112.
Correia, L., and O. Ferreira. 1995 . Burrowing behavior of the introduced red swamp crayfish Procambarus
clarkii (Decapoda: Cambaridae) in Portugal. Journal of Crustacean Biology 15:248 –257.
Cubit, J. 1969. Behavior and physical factors causing migration and aggregation of the sand crab Emerita
analoga (Stimpson). Ecology 50:118 –123.
Dall, W. 1958. Observations on the biology of the greentail prawn, Metapenaeus mastersii (Haswell)
(Crustacea Decapoda: Penaeidae). Marine and Freshwater Research 9:111–134.
Davidson, G.W., and H.H. Taylor. 1995 . Ventilatory and vascular routes in a sand-burying swimming
crab, Ovalipes catharus (White, 1843) (Brachyura: Portunidae). Journal of Crustacean Biology
15:605–624.
Dembowski, J.B. 1926. Notes on the behavior of the fiddler crab. Biological Bulletin 50:179 –201.
Dennell, R. 1933. The habits and feeding mechanism of the amphipod Haustorius arenarius Slabber.
Journal of the Linnean Society of London, Zoology 38:363–388.
Dingle, H., and R.L. Caldwell. 1978. Ecology and morphology of feeding and agonistic behavior in mud-
flat stomatopods (Squillidae). Biological Bulletin 155:134–149.
Dorgan, K.M., S.R. Arwade, and P.A. Jumars. 2007. Burrowing in marine muds by crack propagation:
Kinematics and forces. Journal of Experimental Biology 210:4198 –4212.
Dorgan, K.M., S.R. Arwade, and P.A. Jumars. 2008. Worms as wedges: Effects of sediment mechanics on
burrowing behavior. Journal of Marine Research 66:219 –254.
Dorgan, K.M., P.A. Jumars, B.D. Johnson, and B.P. Boudreau. 2006. Macrofaunal burrowing: The
medium is the message. Oceanography and Marine Biology: An Annual Review 44:85–121.
Dorgan, K.M., P.A. Jumars, B. Johnson, B.P. Boudreau, and E. Landis. 2005 . Burrowing mechanics:
Burrow extension by crack propagation. Nature 433:475–475.
Dugan, J.E., D.M. Hubbard, and M. Lastra. 2000. Burrowing abilities and swash behavior of three crabs,
Emerita analoga Stimpson, Blepharipoda occidentalis Randall, and Lepidopa californica Efford
(Anomura, Hippoidea), of exposed sandy beaches. Journal of Experimental Marine Biology and
Ecology 255:229 –245.
Dworschak , P.C. 1987. Feeding behaviour of Upogebia pusilla and Callianassa tyrrhena (Crustacea,
Decapoda, Thalassinidea). Investigación Pesquera 51:421–429.
Dworschak , P.C. 1998. The role of tegumental glands in burrow construction by two Mediterranean cal-
lianassid shrimp. Marine Biodiversity 28:143–149.
Dworschak , P.C., H. Koller, and D. Abed-Navandi . 2006. Burrow structure, burrowing and feed-
ing behaviour of Corallianassa longiventris and Pestarella tyrrhena (Crustacea, Thalassinidea,
Callianassidae). Marine Biology 148:1369 –1382.
Efford, I.E. 1965 . Aggregation in the sand crab, Emerita analoga (Stimpson). Journal of Animal Ecology
34:63–75.
Efford, I.E. 1966. Feeding in the sand crab, Emerita analoga (Stimpson) (Decapoda, Anomura).
Egusa, S., and T. Yamamoto. 1961. Studies on the respiration of the “Kuruma” prawn Penaeus japonicus
Bate.—I. Burrowing behavior, with special reference to its relation to environmental oxygen con-
centration. Bulletin of the Japanese Society of Scientific Fisheries 27:22–26.
Ellers, O. 1995 . Form and motion of Donax variabilis in flow. Biological Bulletin 189:138 –147.
Faulkes, Z. 2006a . Digging mechanisms and substrate preferences of shovel nosed lobsters, Ibacus peronii
(Decapoda: Scyllaridae). Journal of Crustacean Biology 26:69 –72.
Faulkes, Z. 2006b. The locomotor toolbox of the spanner crab, Ranina ranina (Brachyura, Raninidae).
Faulkes, Z., and D.H. Paul. 1997a . Digging in sand crabs (Decapoda, Anomura, Hippoidea): Interleg
coordination. Journal of Experimental Biology 200:793–805.
Faulkes, Z., and D.H. Paul. 1997b. Coordination between the legs and tail during digging and swimming
in sand crabs. Journal of Comparative Physiology A 180:161–169.
Faulkes, Z., and D.H. Paul. 1998. Digging in sand crabs: Coordination of joints in individual legs. Journal
of Experimental Biology 201:2139 –2149.
Felder, D.L. 1979. Respiratory adaptations of the estuarine mud shrimp, Callianassa jamaicense (Schmitt,
1935) (Crustacea, Decapoda, Thalassinidea). Biological Bulletin 157:125–137.
Forward, R.B., Jr., H. Diaz , and J.H. Cohen. 2005 . The tidal rhythm in activity of the mole crab Emerita
talpoida. Journal of the Marine Biological Association of the UK 85:895–901.
Fuss, C.M., Jr. 1964 . Observations on burrowing behavior of the pink shrimp, Penaeus duorarum
Burkenroad. Bulletin of Marine Science, Gulf and Caribbean 14:62–73.
Gingras, M.K., S.G. Pemberton, S. Dashtgard, and L. Dafoe. 2008. How fast do marine invertebrates bur-
row? Palaeogeography, Palaeoclimatology, Palaeoecology 270:280–286.
Glaessner, M.F. 1957. Evolutionary trends in Crustacea (Malacostraca). Evolution 11:178 –184.
Glantz , R.M., and W.J.P. Barnes. 2002. Visual systems: Neural mechanisms and visual behaviour. Pages
203–226 in K. Wiese, editor. Crustacean experimental systems in neurobiology. Springer, Berlin.
Griffith, H., and M. Telford. 1985 . Morphological adaptations to burrowing in Chiridotea coeca
(Crustacea, Isopoda). Biological Bulletin 168:296 –311.
Grow, L., and H. Merchant. 1980. The burrow habitat of the crayfish, Cambarus diogenes diogenes
(Girard). American Midland Naturalist 103:231–237.
Hartnoll, R.G. 1971. The occurrence, methods and significance of swimming in the Brachyura. Animal
Behaviour 19:34–50.
Hessler, R.R. 1982. The structural morphology of walking mechanisms in eumalacostracan crustaceans.
Howard, J.D. 1968. X-ray radiography for examination of burrowing in sediments by marine invertebrate
organisms. Sedimentology 11:249 –258.
Hunter, R.D. 1982. Methylcellulose—an alternative medium for the study of burrowing aquatic inverte-
brates. Marine Behaviour and Physiology 8:199 –203.
Jaeger, H.M., S.R. Nagel, and R.P. Behringer. 1996a . Granular solids, liquids, and gases. Reviews of
Modern Physics 68:1259.
Jaeger, H.M., S.R. Nagel, and R.P. Behringer. 1996b. The physics of granular materials. Physics Today
49:32–39.
Jaramillo, E., J.E. Dugan, and H. Contreras. 2000. Abundance, tidal movement, population structure
and burrowing rate of Emerita analoga (Anomura, Hippidae) at a dissipative and a reflective sandy
beach in south central Chile. Marine Ecology 21:113–127.
Johnson, B.D., B.P. Boudreau, B.S. Gardiner, and R. Maass. 2002. Mechanical response of sediments to
bubble growth. Marine Geology 187:347–363.
Jones, C.M. 1988. The biology and behaviour of bay lobsters, Thenus spp. (Decapoda: Scyllaridae),
in northern Queensland, Australia. PhD dissertation, Department of Zoology, University of
Queensland, Brisbane, Australia .
Jorgensen, B.B., and N.P. Revsbech. 1985 . Diffusive boundary layers and the oxygen uptake of sediments
and detritus. Limnology and Oceanography 30:111–122.
Josephson, R.K., and K.W. Flessa. 1972. Cryolite: A medium for the study of burrowing aquatic organ-
isms. Limnology and Oceanography 17:134–135.
Jumars, P.A., K.M. Dorgan, L.M. Mayer, B.P. Boudreau, and B.D. Johnson. 2006. Physical constraints on
infaunal lifestyles: May the persistent and strong forces be with you. Pages 442–457 in W. Miller III,
editor. Trace fossils: Concepts, problems, prospects. Elsevier, Amsterdam .
Karplus, I. 1987. The association between gobiid fishes and burrowing alpheid shrimps. Oceanography
and Marine Biology: An Annual Review 25:507–562.
Kunze, J.C. 1981. The functional morphology of stomatopod crustacea. Philosophical Transactions of the
Royal Society of London Series B 292:255–328.
MacGinitie, G.E. 1934 . The natural history of Callianassa californiensis Dana. American Midland
Naturalist 15:166 –177.
MacGinitie, G.E. 1938. Movements and mating habits of the sand crab, Emerita analoga. American
Midland Naturalist 19:471–479.
Mach, K.J., D.V. Nelson, and M.W. Denny. 2007. Techniques for predicting the lifetimes of wave-swept
macroalgae: A primer on fracture mechanics and crack growth. Journal of Experimental Biology
210:2213–2230.
Mather, J.A. 1986. Sand digging in Sepia officinalis: Assessment of a cephalopod mollusc’s fixed behavior
pattern. Journal of Comparative Psychology 100:315–320.
Matthews, D.C. 1955 . Feeding habits of the sand crab Hippa pacifica (Dana). Pacific Science 9:382–386.
McGaw, I.J. 2004 . Ventilatory and cardiovascular modulation associated with burying behaviour in two
sympatric crab species, Cancer magister and Cancer productus. Journal of Experimental Marine
Biology and Ecology 303:47–63.
McGaw, I.J. 2005 . Burying behaviour of two sympatric crab species: Cancer magister and Cancer produc-
tus. Scientia Marina 69:375–381.
McLachlan, A. 1983. Sandy beach ecology—a review. Pages 321–380 in A. McLachlan and T. Erasmus,
editors. Sandy beaches as ecosystems. Dr. W. Junk , The Hague.
McLay, C.L., and T.A. Osborne. 1985 . Burrowing behaviour of the paddle crab Ovalipes catharus
(White, 1843) (Brachyura: Portunidae). New Zealand Journal of Marine and Freshwater Research
19:125–130.
Meyers, M.B., E.N. Powell, and H. Fossing. 1988. Movement of oxybiotic and thiobiotic meiofauna in
response to changes in pore-water oxygen and sulfide gradients around macro-infaunal tubes.
Møller, L.F., and H.U. Riisgå rd. 2006. Filter feeding in the burrowing amphipod Corophium volutator.
Marine Ecology Progress Series 322:213–224.
Mukai, H., and I. Koike. 1984 . Behavior and respiration of the burrowing shrimps Upogebia major (de
Haan) and Callianassa japonica (de Haan). Journal of Crustacean Biology 4:191–200.
Nasir, U., and Faulkes, Z. 2011. Color polymorphism of sand crabs, Lepidopa benedicti (Decapoda,
Albuneidae). Journal of Crustacean Biology 32:240–245.
Nelson, W.G. 1980. Amphipods. Little-known crustaceans. Sea Frontier 26:138 –144.
Nickell, L.A., R.J.A. Atkinson, and E.H. Pinn. 1998. Morphology of thalassinidean (Crustacea:
Decapoda) mouthparts and pereiopods in relation to feeding, ecology and grooming. Journal of
Nielsen, M.V., and L.H. Kofoed. 1982. Selective feeding and epipsammic browsing by the deposit-feeding
amphipod Corophium. Marine Ecology Progress Series 10:81–88.
Palomar, N.E., M.A. Juinio-Meñez , and I. Karplus. 2005 . Behavior of the burrowing shrimp Alpheus
macellarius in varying gravel substrate conditions. Journal of Ethology 23:173–180.
Paul, D.H. 1971a . Swimming behavior of the sand crab, Emerita analoga (Crustacea, Anomura) I. Analysis
of the uropod stroke. Zeitschrift f ü r vergleichende Physiologie 75:233–258.
Paul, D.H. 1971b. Swimming behavior of the sand crab, Emerita analoga (Crustacea, Anomura) II.
Morphology and physiology of the uropod neuromuscular system. Zeitschrift f ü r vergleichende
Physiologie 75:259 –285.
Paul, D.H. 1981a . Homologies between neuromuscular systems serving different functions in two deca-
pods of different families. Journal of Experimental Biology 94:169 –187.
Paul, D.H. 1981b. Homologies between body movements and muscular contractions in the locomotion of
two decapods of different families. Journal of Experimental Biology 94:159 –168.
Paul, D.H. 1991. Pedigrees of neurobehavioral circuits: Tracing the evolution of novel behaviors by
comparing motor patterns, muscles, and neurons in members of related taxa. Brain, Behavior and
Evolution 38:226 –239.
Paul, D.H., A.M. Then, and D.S. Magnuson. 1985 . Evolution of the telson neuromusculature in decapod
Crustacea. Biological Bulletin 168:106 –124.
Paul, D.H., and L.J. Wilson. 1994 . Replacement of an inherited stretch receptor by a newly evolved stretch
receptor in hippid sand crabs. Journal of Comparative Neurology 350:150 –160.
Pearse, A.S., H.J. Humm, and G.W. Wharton. 1942. Ecology of sand beaches at Beaufort, N.C. Ecological
Monographs 12:135–190.
Perry, D.M. 1980. Factors influencing aggregation patterns in the sand crab Emerita analoga (Crustacea:
Hippidae). Oecologia 45:379 –384.
Pinn, E.H., and A.D. Ansell. 1993. The effect of particle size on the burying ability of the brown shrimp
Crangon crangon. Journal of the Marine Biological Association of the UK 73:365–377.
Rebach, S. 1974 . Burying behavior in relation to substrate and temperature in the hermit crab, Pagurus
longicarpus. Ecology 55:195–198.
Rice, A.L., and C.J. Chapman. 1971. Observations on the burrows and burrowing behaviour of two
mud-dwelling decapod crustaceans, Nephrops norvegicus and Goneplax rhomboides. Marine Biology
10:330–342.
Riisgå rd, H.U., and P. Schotge. 2007. Surface deposit feeding versus filter feeding in the amphipod
Corophium volutator. Marine Biology Research 3:421–427.
Sanders, H.L. 1958. Benthic studies in Buzzards Bay. I. Animal-sediment relationships. Limnology and
Oceanography 3:245–258.
Savazzi, E. 1985 . Functional morphology of the cuticular terraces in burrowing terrestrial brachyuran
decapods. Lethaia 18:147–154.
Savazzi, E. 1986. Burrowing sculptures and life habits in Paleozoic Lingulacean brachiopods.
Paleobiology 12:46 –63.
Savazzi, E. 1989. Burrowing mechanisms and sculptures in recent gastropods. Lethaia 22:31–48.
Savazzi, E., and P. Huazhang. 1994 . Experiments on the frictional properties of terrace sculptures.
Lethaia 27:325–336.
Schmalfuss, H. 1978. Structure, patterns, and function of cuticular terraces in recent and fossil arthro-
pods. Zoomorphology 90:19 –40.
Seilacher, A. 1973. Fabricational noise in adaptive morphology. Systematic Zoology 22:451–465.
Seilacher, A. 2007. Trace fossil analysis. Springer, Berlin.
Stamhuis, E.J., B. Dauwe, and J.J. Videler. 1998. How to bite the dust: Morphology, motion pattern and
function of the feeding appendages of the deposit-feeding thalassinid shrimp Callianassa subterra-
nea. Marine Biology 132:43–58.
Stamhuis, E.J., T. Reede-Dekker, Y. van Etten, J.J. de Wiljes, and J.J. Videler. 1996. Behaviour and time
allocation of the burrowing shrimp Callianassa subterranea (Decapoda, Thalassinidea). Journal of
Stamhuis, E.J., and J.J. Videler. 1998. Burrow ventilation in the tube-dwelling shrimp Callianassa subter-
ranea (Decapoda: Thalassinidea). I. Morphology and motion of the pleopods, uropods and telson.
Torres, J.J., D.L. Gluck , and J.J. Childress. 1977. Activity and physiological significance of the pleopods in
the respiration of Callianassa californiensis (Dana) (Crustacea: Thalassinidea). Biological Bulletin
152:134–146.
Trueman, E.R. 1966. The mechanism of burrowing in the polychaete worm, Arenicola marina (L.).
Biological Bulletin 131:369 –377.
Trueman, E.R. 1970. The mechanism of burrowing of the mole crab, Emerita. Journal of Experimental
Biology 53:701–710.
Trueman, E.R., A.R. Brand, and P. Davis. 1966. The dynamics of burrowing of some common littoral
bivalves. Journal of Experimental Biology 44:469 –492.
Vannier, J., P. Boissy, and P.R. Racheboeuf. 1997. Locomotion in Nebalia bipes: A possible model for
Palaeozoic phyllocarid crustaceans. Lethaia 30:89 –104.
Veloso, V.G., and R.S. Cardoso. 1999. Population biology of the mole crab Emerita brasiliensis (Decapoda:
Hippidae) at Fora Beach, Brazil. Journal of Crustacean Biology 19:147–153.
von Boletzky, S. 1996. Cephalopods burying in soft substrata: Agents of bioturbation? Marine Ecology
17:77–86.
Watkin, E.E. 1939. The swimming and burrowing habits of some species of the amphipod genus
Bathyporeia. Journal of the Marine Biological Association of the UK 23:457–465.
Watling , L. 1981. An alternative phylogeny of peracarid crustaceans. Journal of Crustacean Biology
1:201–210.
Welland, M. 2009. Sand: The never-ending story. University of California Press, Berkeley.
Wenner, A.M. 1972. Incremental color change in an anomuran decapod Hippa pacifica Dana. Pacific
Science 26:346 –353.
Winter, A.G., and Hosoi, A.E. 2011 . Identification and evaluation of the Atlantic razor clam (Ensis
directus) for biologically inspired subsea burrowing systems. Integrative and Comparative Biology
51:151–157.
11
APPENDAGE DIVERSITY AND MODES OF LOCOMOTION:
SWIMMING AT INTERMEDIATE REYNOLDS NUMBERS
Jeannette Yen
Abstract
This contribution provides an overview of morphological adaptations found in copepods and
other small crustaceans that swim in the water column. At their size (predominantly <1 to 10
mm), the viscosity of water greatly influences crustacean morphology and behavior. An exami-
nation of the functional morphology of locomotory appendages of aquatic microcrustaceans
reveals adaptations to achieve efficient performance while swimming at the interface between
laminar and turbulent regimes. These multifunctional appendages not only are used for loco-
motion at different gaits with species specific trajectories but also are useful in sensing and in
food and mate acquisition. The biologically generated flows caused by the motion of locomo-
tory appendages of copepods also have different uses: the anterior flow field serves as a feeding
and sensory current, while the posterior wake provides thrust. Information about size, speed,
location, and identity can be discerned by studying the dynamics of these fluid deformations.
These mechanistic analyses have benefited from techniques in small-scale flow visualization,
from high-speed and high-magnification imaging, and, most importantly, from a deeper appre-
ciation of the unique aspects of the behavior of copepods (rapid responses, high acceleration)
and the conditions that evoke those behaviors. This chapter discusses behavioral constraints
(and benefits) imposed by life in a viscous medium. Morphological adaptations in small plank-
tonic crustaceans are compared.
INTRODUCTION
Many small crustaceans (e.g., copepods, krill, hyperiid amphipods, decapod larvae) are part of
the plankton. Most of the plankton are small, <1 cm in length, starting from eggs of 0.25 mm.
The word plankton is derived from the Greek word πλαγκτος (planktos), meaning passive
296
Appendage Diversity and Modes of Locomotion 297
Fig. 11.1.
Appendage diversity. (A) Photographs of several key groups found in the plankton to illustrate the range in
sizes (left to right, starting from top center): the krill Euphausia mucronata, the mysid Stylocheiron affine,
a porcellanid crab zoea larva, the copepod Calanus chilensis, and the zoea larva of the sand crab Lepidopa
chilensis. (B) Images from (A) shown to scale. The copepod is the smallest species (far left), followed by
the porcellanid zoea, the sand crab zoea, and the mysid, with the krill being the largest in this group (far
right).
drifters, unable to resist the ebb and flow of the seas. At the scale of kilometers, plankton do
drift with the flow. Yet planktonic crustaceans perform long-distance diurnal migrations over
thousands of body lengths, indicating that they are quite capable of actively swimming with
an efficient propulsive mechanism. A glimpse at the appendages of dominant members of the
plankton (Fig. 11.1) shows an array of many more locomotory limbs than two legs, all of which
serve a useful function or, more likely, many functions. So, why have such complex append-
ages? Over evolutionary time, each appendage has adapted morphologically to fulfill specific
functions that enhance survival and reproduction. Such functions include the ability of these
appendages to move rapidly, essential in behaviors such as gathering dispersed food particles
and avoiding predators. Their locomotory appendages enable these plankters to propel them-
selves in response to the flow of the seas or to environmental gradients of light, temperature,
nutrients, or other chemical constituents. For species that stay in the plankton for their entire
life, locomotion can be essential for finding mates; the discovery and recognition of mates are
often accompanied by tactics that enhance encounter rates such as vertical migrations and
aggregations.
Much of the interest in aquatic propulsion and the locomotory movements of swimming is
motivated by a need to understand the structure of the propulsive wakes that serve as commu-
nication channels. Biologists are studying flows generated by swimming organisms in order to
characterize their distinct wake signatures (Yen and Strickler 1996, Yen 2000, Denhardt et al.
2001, Pohlmann et al. 2001). High-speed, high-resolution video, Schlieren flow visualization
techniques, holography, and state-of-the-art particle image velocimetry techniques have been
developed and successfully applied to study planktonic flow fields (Malkiel et al. 2003, Yen et al.
2003, Catton et al. 2007, 2011 Jiang and Kiørboe 2011). Large-volume observations of isolated
individuals or groups provide three-dimensional trajectories to assess speed and acceleration
exhibited by freely swimming plankton (Bundy et al. 1993, Yen et al. 1998, Schmitt and Seuront
2001). These recent studies have shown that planktonic organisms can generate complex vorti-
cal wakes while achieving stunningly high (considering their size) bursts of propulsive speed
and acceleration rates (Lenz et al. 2004, Kiørboe et al. 2009). Many challenges stem from the
anatomical complexity of such organisms, the existence of multiple appendages moving with
complex kinematics, and the strongly coupled fluid-structure interaction that ensues when a
body with moving appendages advances through a fluid by the thrust force it generates by its
own swimming motion. This chapter describes the diversity of appendages, the complexity
of coordinated movements of these appendages, and the resultant fluid deformations in both
laminar and quasi-turbulent wakes. Here, I present an analysis of locomotion by plankton, with
a detailed focus on copepods where new techniques have led to significant discoveries. This
contribution examines movement and feeding at intermediate Reynolds numbers (Re) to assess
the advantages of living at the interface between laminar and turbulent regimes.
PHYSICAL CONSTRAINTS AT THE INTERFACE BET WEEN LAMINAR AND

TURBULENT REGIMES
The study of aquatic microcrustacean locomotion through water requires an analysis of both
sides of the interaction: the biology of the organism and the properties of their surrounding
environment, the water. With knowledge of the f luid physics that govern the interactions
of moving limbs and water, a deeper understanding of their functional morphology can be
attained. The two key forces are viscosity and inertia, and the ratio of inertial forces to vis-
cous forces can be calculated as its Reynolds number, Re = UL/n, where U is the speed of the
object moving through the water, L is its length, and n is viscosity of the f luid. This index can
be used to evaluate the relative importance of viscosity and inertia to an organism moving
through the f luid.
By definition, microcrustaceans are small, and L is often in millimeters. The dominant mem-
bers of the plankton, such as copepods and krill, range in size from 1 to 60 mm in length as adults,
moving on average one body length per second (bl/s). If all length-time parameters are entered
in terms of millimeters and seconds, with U = 1–60 mm/s for organisms that are 1–60 mm in
length L moving in water with viscosity of 1 mm 2/s, the range of Re is 1–3,600. Therefore, plank-
ton organisms occupy a special niche, characterized by an environment transitioning from a
laminar to a turbulent field. Here, slight variations in size, speed, and viscosity can shift the
balance between viscous and inertial forces. At this size, viscosity (the resistance to motion) is a
primary force with which small aquatic creatures contend and presents a strong constraint that
influences the morphology and behavior.
What are the physical constraints on movement by small aquatic crustaceans in water? One
parameter to consider is the boundary layer (BL). The BL is a zone of little or no water move-
ment that will be of varying thickness depending on certain conditions. This sticky BL forms
where the flow decreases with proximity to the solid boundary. The thickness δ of the BL at a
distance x downstream can be calculated as δ/x = 5 Re x–0.5 (Vogel 1994).
For plankton, viscosity is large compared to their speed and size, and at such low Re, the BL
is thick and can restrict movement. To reduce the thickness of the BL for an organism of fixed
small size, the organism could accelerate to higher speeds to escape from viscosity (van Duren
and Videler 2003). To move forward, thrust, generated by the moving legs, must be greater than
the drag of the limbs. One solution is to produce an asymmetry in the magnitude of drag, where
high drag during the power stroke propels the organism forward. Feathering the limb mini-
mizes the drag force in the recovery stroke that carries the limb back in the direction of flow.
Internally, the presence of thinner promotor and larger or multiple remotor musculature for the
cephalic appendages (Boxshall 1982) supports the noted asymmetry needed in the speed of the
power versus recovery strokes utilized at low Re values. This asymmetry in appendage kinemat-
ics of reciprocating appendages results in a positive translation. Artemia nauplii, for example,
have little asymmetry in appendage movement and show inefficient body translation.
In addition to dynamic variations in drag on the limbs through the propulsive cycle, viscos-
ity influences the function of the mouthparts. Multifunctionality can be achieved by organisms
living at the interface between laminar and turbulent regimes by modifying two parameters
(Cheer and Koehl 1987). At low speed and close spacing of setae along the limb, the mouthpart
has a thick BL and acts like a paddle to maneuver food into its capture area. At higher speeds,
with wider spacing of setae, or when closing in toward a surface, the mouthpart acts like a sieve,
capturing particles larger in size than the mesh spacing, allowing smaller particles and water to
escape (Frost 1972, Koehl 2001). Hence, specific adaptations to life in transition and the low-Re
constraints of reversible flow and thick BL can be identified: (1) asymmetry in limb oscillations,
(2) variation in setule spacing, and (3) variation in limb speed. These examples illustrate that,
by understanding the fluid physics, an account can be made for some of the unique behavior and
morphological adaptations documented for plankton.
COPEPOD APPENDAGE DIVERSIT Y
Copepods rely on an intricate set of locomotory appendages that serve many functions, such as
generating a feeding current, setting up a sensory field, and advancing the organism by different
gaits (sinking, hovering, cruising, hopping, escaping). Because of the multiple functions of the
limbs, it is important to discuss how appendages are used for locomotion, as well as their use in
feeding and sensing. Here I describe how each appendage of the tiny crustacean is used to enable
them to execute a diverse set of behaviors and how these behaviors have led to their success in
the aquatic environment.
Cephalic Appendages
Diversity is seen in the morphology of the articulated body parts of the copepod that contribute
to its mobility (Fig. 11.2; Mauchline 1998). There are two distinct sections of the body: the cepha-
lothorax, which has six pairs of cephalic appendages and five pairs of thoracic appendages, and
A
antennule
rostrum
Metasome Cephalosome
antenna
mandible
maxillule
maxilla
Prosome
maxilliped
leg 1
1 leg 2
2 leg 3
leg 4
3 leg 5
4
5
genital somite
Urosome
anal somite
furca or caudal ramus
en
ex
maxillule
mandible
antenna
swimming leg
antennule maxilliped
maxilla
en
ex
Fig. 11.2.
Locomotory appendages of the aquatic microcrustacean copepod. (A) Body form and appendage connec-
tions. (B) Drawings of six cephalic appendages and one representative drawing of the five thoracic pairs
of legs show the setae that adorn the segmented limbs. Abbreviations: en, endopodites; ex, exopodites.
Adapted from Mauchline (1998), with permission from Elsevier Books.
the urosome, which is a single flexible tail. The cephalic appendages include, from anterior to
posterior, antenna 1 (antennule), antenna 2 (antenna), mandible, maxilla 1 (maxillule), maxilla 2
(maxilla), and maxillipeds. The thoracic appendages include four pairs of biramous or branched
swimming legs that are joined by an intercoxal sclerite. The fifth legs are sexually dimorphic.
These 11 pairs of appendages take on three basic forms: a long unjointed antennule, a jointed
brushlike appendage, and a jointed paddlelike appendage. The two basic forms can be found
in the cephalic appendages, while only the fifth leg of the adult male copepod departs from the
dominant paddlelike form of the rest of the thoracic appendages. The narrower tail or urosome
is separated from the prosome by a major articulation. All of these appendages, with the excep-
tion of the fifth legs, are used in locomotory activity (Huys and Boxshall 1991, Mauchline 1998,
Bradford-Grieve 2002).
As summarized in Bradford-Grieve (2002), each appendage has joints and musculature,
adorned with setae, and these limbs can be used for multiple functions: sensing, propelling,
and feeding. Starting from the head, the antennule is richly adorned with sensory hairs. The
paired antennules (or first antenna) are the longest of the cephalic appendages, making it use-
ful as an oar (Borazjani et al. 2010), as well as a bilateral sexually dimorphic sensory apparatus,
comparing signals arriving at the copepod’s left versus right (Ohtsuka and Huys 2001, Fields
and Weissburg 2005). The length permits extension of these sensors out beyond the BL and
f low field of the copepod, so inner sensors perceive signals within its f low field and distal
sensors perceive signals outside its f low (Lenz and Yen 1993). Because of viscous forces, f low
created by the centrally located cephalic appendages is attenuated strongly. The distal setal
mechanoreceptors are exposed to f low undisturbed by the self-generated f low, thus improv-
ing the signal-to-noise ratio, enabling the perception of signals approaching from beyond the
f low field. These include those of attacking predators or approaching vortices of turbulent
f lows. Within the f low field, the faster water speeds around the proximal chemoreceptive sen-
sors of the antennules thin the BL, enhancing chemical detection of food or mate scents (Yen
et al. 1998).
Multifunctionality is noted for these organisms, where sensory appendages become rap-
torial and locomotory appendages are used as sensors. Male copepod antennules often are
geniculated, enabling them to use this extended limb to reach and grasp their female mate
prior to placement of the spermatophore. The marine coastal copepod Temora not only uses its
antennules to sense its environment but also bends the appendages to direct particles toward
its other appendages that guide the food to the mouth (personal observations). Furthermore,
sensors adorn the mouthparts, indicating their function as part of the sensor array. The dual
functionality of the antennules, serving both as a sensory organ and as a propulsive organ, also
relies on utilizing viscous forces. The high drag of the long antennules propels the copepod
forward when the antennules bend. When antennules flex and achieve higher Re, the sensors
that line the antennules shed the old BL and sample a new parcel of water. Thus, the antennules
can function as a chemical sensor, a fluid mechanical sensor, a food acquisition appendage, a
mate acquisition appendage, and a generator of propulsive force.
For foraging, the copepod utilizes six pairs of cephalic limbs that rhythmically reciprocate to
entrain water. Evidence of redirected flow (Koehl and Strickler 1981) and reoriented swimming
(as in Yen 1988) indicates that limbs within each pair can move independently to divert flow or
turn the body. Once particles of nutritional value are entrained into the area enclosed by the
cephalic appendages, the fluid dynamics change. Strickler (1984) documented the coordinated
reciprocation of head appendages (Fig. 11.3A) and the movements that copepods use to capture
food particles at low Re. An efficient mechanism is to move those reciprocating limbs (Fig. 11.2)
in what Strickler (1984) calls “chopsticks feeding” (see Fig. 11.3B). Here, rather than paddling
back and forth, the pairs of feeding appendages open, expand, surround, and retract to bring
the water containing a food particle close to the mouth. A nice squeeze against the body pushes
the water through the feathery mouthparts, directing the food particle into its mouth, two man-
dibles lined with silica teeth. When the limbs are pressed against the mouthparts, the maxillae
become leaky, sieving the particles from the water, enabling ingestion. High-speed cinematog-
raphy allows us to see that at times the mouthparts, lined with thin setae, act like a paddle and
at other times act like a rake.
Carnivorous copepods use maxillipeds that are more robust and have fewer setae (Fig. 11.3C).
For these raptorial copepods, the maxillipeds are deployed at high Re. Drag is reduced both by
A C
18 Hz
MXP B A B
MAX1 B A B
MP B A B
A2EX B A B
A2EN B A B
0.3 mm
0 10.2 15.1 24.3 34.7 43.7 56.2 66.4 71.3
msec
Fig. 11.3.
Cephalic appendages and kinematics of the aquatic microcrustacean copepod. (A) While feeding,
Eucalanus pileatus deploys two “fling-and-clap” pairs on the second antennae, maxillipeds (MXP) and
endopodites (A2EN), and first maxillae (MAX1) and exopodites (A2EX), reciprocating at regular inter-
vals, with flow direction governed by the mandibular palp (MP). Thick lines depict the movement of the
appendage, starting at A and ending at B. The first pair starts at 24.3 ms, followed by the second pair start-
ing at 34.7 ms. One cycle of the entire motion pattern takes 56.2 ms for a beat frequency of about 18 Hz. The
error of ±1.5 ms for all the timing measurements indicates the high precision of coordinated movement
used to create a flow field of constant structure (adapted from Strickler 1984, with permission from the
American Association for the Advancement of Science). (B) Diagram illustrates “chopsticks” feeding by
a copepod at low Re, showing four steps in the sequence, starting from right to left. The two dark bars are
the starting positions of one pair of mouthparts, with the mouth of the copepod to the left. The entrained
particle comes in from the right. Step 1: the pair of appendages opens and moves the particle in from the
right. Step 2: the proximal sections of the appendages open to move particle closer to mouth. Step 3: the
distal ends close to trap the particle. Step 4: the proximal sections squeeze the particle into the mouth on
left (adapted from Strickler 1984, with permission). (C) Trophic differences are noted in the morphology
of the mouthparts of a herbivorous (top) versus a carnivorous (bottom) copepod (adapted from Ohtsuka
et al. 1997, with permission from the Journal of Crustacean Biology).
feathering the limb to reduce surface area and by shedding the BL with very fast extensions of the
maxillipeds. These limb movements of carnivorous copepods, performed at high Re values of
20–5000 (Kiørboe et al. 2009), enable the capture of mobile prey without pushing the prey away
with the viscous BL. Food is guided to the mouth, where strongly reinforced mandibles crush
prey, such as siliceous diatoms, between short, robust, silica-capped mandibular gnathobases
of herbivores, whereas live prey are opened with long sharp teeth (Michels and Schnack-Schiel
2005) on the ventral surfaces of the mandibles of raptorial carnivorous species. One group, the
heterorhabids, have a tubular lumen in the ventralmost tooth of the mandible, through which
anesthetic is injected into the prey (Nishida and Ohtsuka 1996).
Thoracic Appendages
Thoracic body segments are fused to the cephalic body segments in the copepod to form an
ellipsoid prosome, separated from the urosome by a defined articulation. On each thoracic
A Coxa Praecoxa B Th rem 6

Intercoxa
Th prm 3 Th rem 5
Basis sclerite Th rem 4
Th prm 2
Th rem 3
Th prm 1
Th rem 2
Th rem1
0.5 mm
C D
0.16 35
0.14 P4 30
Acceleration (mm s-2)

P3 Acartia C V, VI F
Leg Surface Area (mm2)
0.12 P2
P1 25
Temora C VI M
0.10
20 Temora C IV, V, VI F
Temora early copepodite
0.08
15 Temora C IV M Temora C V M
0.06
10
0.04
Temora longicornis
0.02 5
Acartia tonsa
0
Acartia Female Temora Female Temora Male 0.2 0.4 0.6 0.8 1.0 1.2
Species Body Length (mm)
Fig. 11.4.
Thoracic appendages of an aquatic copepod. (A) Camera lucida tracing of the pereopod or swimming leg
of a calanoid copepod shows the presence of feathered and stout setae that line the segmented articulated
swimming leg appendage (redrawn from Huys and Boxshall 1991). (B) Cross section through the second
pedigerous somite of the thorax (Th) reveals the thicker remoter (rem1–6) and thinner promoter (prm1–3)
musculatures that move the swimming legs of the copepod (adapted from Boxshall 1982, with permission
from the Royal Society of London). (C) Leg surface area of adult males and females of the coastal copepod
Temora longicornis compared to Acartia tonsa. For A. tonsa, the largest swimming legs are the last two (pere-
opods P3, P4), while for T. longicornis, the middle two (P1, P2) are the largest (from Liu 1996, used with per-
mission). (D) Acceleration achieved in escapes from a predator mimic (mean ± SE) for adult female Acartia
tonsa and copepodite stages (C IV–VI) of Temora longicornis male (M) and female (F) (from Liu 1996, used
with permission).
segment is a pair of swimming legs (Fig. 11.4A), where thicker remoter muscles (compared
to thinner promoter muscles) provide thrust in the power stroke (Fig. 11.4B; Boxshall 1982).
Fig. 11.4, C and D, shows the morphology and function of thoracic appendages of two cala-
noid copepods: Temora longicornis and Acartia tonsa. Of the four effective swimming legs for
Temora longicornis, the third pair of pereopods or pereopod 3 swimming leg is the longest,
while pereopod 2 has the greatest surface area (Fig. 11.4C). In Acartia tonsa, the pereopods are
10–27% smaller for their body length than the ratio of pereopod length to body length found for
T. longicornis (Liu 1996). These differences affect how far the copepod travels and how quickly
the swimming legs accelerate to transport the copepod (Fig. 11.4D). With the advent of high-
speed filming, we are able to resolve the streak of a copepod escape into specific limb move-
ments deployed in a metachronal rhythm (Wilson 2001, van Duren and Videler 2003). Using
high-speed videography to document escape maneuvers from simulated predators, Liu (1996)
found that because A. tonsa accelerated its smaller pereopods at a higher rate, it traveled much
faster than similar-sized T. longicornis. In fact, while three developmental stages of the copepod
T. longicornis could accelerate to 20 m/s2 (about twice the acceleration due to gravity), the adult
600
Male T. longicornis
500 Fish attack on male
400
mm s–1
300
200
100
600
female T. longicornis
500 Fish attack on female
400
mm s–1
300
200
100
0.05 0.10 0.15 0.20 0.25 0.30

Time (sec)
Fig. 11.5.
Analyses of the high-speed movement patterns of a calanoid copepod in response to fish attacks. Multiple
hops performed by Temora longicornis when escaping from juvenile Menidia menidia enable the copepod
to escape predation (top panel illustrates copepod escape response to fish attack; Wilson 2001). Speed pro-
files for a fish attack on male (top graph) T. longicornis and female (bottom graph) T. longicornis illustrate
how the female can escape farther by performing a series of multiple hops.
stage of A. tonsa could accelerate at even higher rates (Fig. 11.4D). An examination of body
shape showed that A. tonsa is more streamlined, with a ratio of body length to body width of
2.70, compared to 2.35 for adult T. longicornis. At Re > 200, this is important because drag and
required propulsive force are reduced. Longer and wider legs of larger copepods give them the
ability to move farther in one stroke, while smaller copepods perform multiple strokes to travel
similar distances. Species with comparatively short pereopods appear to accelerate fast, and
their intermittent movements result in the commonly seen hopping pattern, while species with
longer pereopods may be more persistent swimmers that continuously move in a smooth cruis-
ing pattern. Multiple thrusts of the swimming legs enable the copepods to escape from fish
at accelerations more than three times gravitational acceleration (Liu 1996). For large cope-
pods, such as Calanus, this single movement can transport them far enough to evade capture
(56–103 mm; Wilson 2001). Temora, on the other hand, can sustain more than 10 strokes per
hop, traveling a distance of 33–54 mm, which is not significantly different from that achieved
by a Calanus single stroke. This enables escape speeds up to 600 bl/s (540 mm/s), sufficient for
the 0.9 mm female T. longicornis to evade capture by a juvenile fish predator (Fig. 11.5; Wilson
2001). For smaller copepods, multiple thrusts of the pereopods maintain the high escape speed
to get the needed translation distance (Acartia uses four to five hops to travel up to 15 mm;
Table 11.1. Four activity models exhibited in the swimming behavior of adult
Centropages typicus.
Activity Description Occurrence

Slow Directly related to the creation of feeding currents; con- Frequent
swimming sists of the rhythmic motion of cephalic appendages (sec-
ond antennae, first maxillae and maxillipeds)
Breaks Organism at rest, without moving the appendages Frequent
Fast swim- Rhythmic swimming thrusts with the thoracic legs, Rare
ming and sometimes with flipping antennae and a thrust of beat-
escape ing of the abdomen
reactions
Grooming Cleaning of the antennulae by brushing them through Occasional
part of the cephalic appendages (mouthparts); maxillae
and second antennae brushed by maxillipeds
From Alcaraz et al. (2007), with permission from Elsevier Ltd.
Wilson 2001). After the antennules participate in the initiation of the movement, they remain
closely folded against the streamlined body to reduce drag. At high Re, the copepods can now
use some inertia to coast when its stroke cycles are complete.
Speeds of 1 m/s for copepods <1 mm are achieved in milliseconds. Such high speeds and
jetlike wakes for plankton movement patterns were once thought inconceivable because of the
physical parameters that dominate small aquatic organisms. This leap places the escaping cope-
pod into another Re realm, where inertial forces come into play, thinning the BL and allowing
the copepod to shed the sticky water—momentarily coasting. The puzzle of the torpedo-shaped
body is solved: during these high-speed escapes, the streamlined body form is essential to the
copepod by reducing pressure drag, enabling such accelerative nonlinear impulsive events.
COPEPOD LOCOMOTORY PAT TERNS
To discuss the functional morphology of the cephalic and thoracic appendages, I present how
they are used in three-dimensional maneuvers to explore the three-dimensional space of the
open ocean and how they propel the copepod using two distinct gaits: cruising and escap-
ing. By analysis of the dynamics of limb morphology and movements when performing these
three-dimensional maneuvers, we begin to understand the fluid dynamics of the wake and their
role in transporting the organism through the water.
Like many small organisms that swim in the sea, copepods must mate, find food, and
evade capture by fish. Analyses of ethograms (Alcaraz et al. 2007) show that copepods spend
time on many additional activities, such as grooming, sinking, or fast and slow swimming
(Table 11.1). With so many moving parts, we expect to find that copepods can maneuver
effectively through their three-dimensional f luid environment and exhibit a diversity of
three-dimensional trajectories. Notable distinctions in the behavioral repertoire of copep-
ods involve variations in speed, turning frequency, or turning angle. Some of these responses
have been identified as specific survival tactics, such as foraging in a patch by increased turn-
ing (Williamson 1981, Tiselius 1992, Bundy et al. 1993), increased swarming in areas with
A Standard D
eviation of
B
Velocit y / Mean of
Velocity
500 tf
400
300
Z (mm)
200
Z-Component 3 3 100
2 0
ent
2 –100 t0
pon
1 100
80 80
om
0 1 60 60
X ( 40 20 40 min)
X-C
3 mm 20
2 ) –20 0
6 m in 5
Y-Component 0 –40 4.1
1 0 oved
Y (M
C D
200 0
150 50 t0
tf
100
Z (mm)
Z (mm)
100
50
t0 150
0
–50 200 tf
–100 –250
40 50
30 20 40 80
20 0 30 70
X ( 10 –40 –20 in) X ( 20 60 in)
mm 0 –80–60 m in 30 m
mm
) 10 50 m in 12 m
) 40
–10 –120–100 ed 1.29 0 30 0.562
ov oved
Y (M Y (M
Fig. 11.6.
Distinct trajectories of different copepod species performing different behaviors. (A) Species-specific
differences in swimming trajectories of two copepods: Temora longicornis (solid symbols) and Acartia
hudsonica (open symbols). Temora swims smoothly, at a steady velocity, while Acartia swims erratically,
hopping up and sinking down, resulting in a high coefficients of variation in their swimming speeds. (B–D)
Representative simulated sampling ambits for each copepod species: Clausocalanus furcatus showing fast
swimming along nonoverlapping paths (B), Paracalanus aculeatus performing slow swimming (C), and
Oithona plumifera while sinking (D). The inset illustrates the sampling method employed by each species.
The start (t 0) and end (t f ) points of each ambit are shown; the amount of time represented by each track
and the distance traveled are shown on the right Z-component axes. The intermediate steps indicated by
the asterisks represent the copepod’s location after every 100 time steps, which here is equivalent to 50 s.
Adapted from Wiggert et al. (2005), with permission from Oxford University Press.
amino acids (Poulet and Ouellet 1982), mate tracking by chemical and f luid mechanical cues
(Doall et al. 1998, Weissburg et al. 1998, Yen et al. 1998), escapes from fish (Holzman and
Wainwright 2009), fish mimics (Bollens and Frost 1989, Fields and Yen 1997a), and small-
scale turbulence (Hwang et al. 1994) or quiet swimming in response to the presence of
predators (Folt and Goldman 1981). These patterns led to the hypothesis that copepods can
be biosensors, where their behavior informs us of the distribution of small-scale biological-
chemical-physical features in the ocean.
Not only can behavior reveal environmental structure, but also species identity often can be
recognized from the path structure and rhythm. Many copepodologists would agree that they
can recognize Acartia because of its peculiar hop-and-sink vertically dominated movement pat-
terns, while Aetideus advances along in a horizontal plane, in contrast to Temora, which cruises
continuously in three dimensions. Mauchline (1998) illustrates common patterns, noting dis-
tinctions in their trajectories. Kinematic analyses have shown that the male moves much faster
during mate tracking than during normal swimming (Doall et al. 1998). The rhythmic hopping
of Acartia is distinguished from the smooth swimming of Temora by the high coefficient of vari-
ation in their locomotory behavior (Fig. 11.6A). Differences in propulsive patterns can be attrib-
uted to the longer thin pereopods of Acartia that are moved at higher accelerations than the
thoracic appendages of Temora (Liu 1996).
Distinct trajectories also enable copepods to explore their three-dimensional space, or

ambit, by minimizing the overlap of paths. These patterns appear to be most strongly influenced
by feeding behavior (Wiggert et al. 2005). Fig. 11.6B–D shows three typical trajectories exhib-
ited by different copepod species: fast swimming along nonoverlapping paths that increases
encounter rates with prey, slow swimming where additional advection facilitates exchange of
water carrying food particles, and sinking to save energy and minimize movement that can
create disturbances. Noise reduction during quiet sinking permits greater sensitivity to prey
signals, with the added advantage of generating fewer signals that would alert predators. Other
groups of copepods have limbs and lifestyles that reflect their habitat: harpacticoids have short
antennules and crawl through interstitial spaces of sand; parasitic copepods have clawlike tho-
racic appendages and attachment pads and do not propel themselves since they are hitching a
ride on a host; tiny pelagic cyclopoids barely sink and use their limbs to slip stealthily to another
parcel of water (Jiang and Paffenhöfer 2008).
KINEMATICS AND GAITS
Because of their small size, copepods typically operate in a low-Re environment. With the buoy-
ancy imparted by swimming through the dense medium of water, copepods can exhibit a number
of movement patterns. Depending on the orientation of limbs, the location of the center of mass,
and the negative buoyancy due to the weight of the chitinous exoskeleton and internal network of
muscles and organs, a copepod can hover or sink slowly. Viscous forces are beneficial for maintain-
ing position in the water column by reducing the sinking speed. Tethered by body weight in the
viscous medium (like a fly in a pot of honey), the hovering copepod can advect surrounding fluid
containing food particles and scents past its sensors and toward its mouth, funneling information
from a large volume entrained in the flow field. The laminarity of the low-Re flow in the feed-
ing current smoothes out the random spatial distribution of flow and mass in the surrounding
isotropic turbulence as found at the scale of copepods. Since streamlines connect to specific loca-
tions in three-dimensional space, the copepod creates a familiar local environment where particles
coming into the flow field originate from known locations outside the flow field (Yen and Strickler
1996). Thus, viscosity provides a means to organize the copepod’s fluid environment.
Copepods move during the deployment of their appendages. To accomplish this, some
appendages are feathery, flaring out during the power stroke to increase drag and collapsing
or bending during the recovery stroke. When the fan collapses during the recovery, drag is
reduced, thus setting up the asymmetry in limb kinematics. At low Re, this asymmetry allows
the water to be pushed back and the copepod to move forward. Each set of limbs moves accord-
ing to a rhythm to efficiently transport water or translate the copepod relative to its surround-
ings (Strickler 1984). Using only cephalic appendages, water is advected past its body parts and
expelled into a thin laminar wake. As a result, the copepod barely disturbs the flow. Stealth
may be achieved during cruising because the metachronal deployment of multiple appendages
smoothes out the flow versus an intermittent wake as might be created by a single appendage or
by synchrony in multioared movement. Behind the copepod, little momentum is transferred to
the water, allowing stealth. Leaving a thin laminar streamlike wake has another function: sig-
naling molecules, such as pheromones, can persist without immediate dispersion and be useful
to attract and guide male copepods to their pheromone-exuding female mates (Yen et al. 2004).
This swimming behavior, leading to the translation of the copepod in a smooth and continuous
movement, has been called cruising.
But even more thrilling is the ability to escape, accelerating more than three times gravi-
tational acceleration! With high-resolution imaging, the complex coordination of the many
limbs that is necessary for the copepod to achieve forward-directed movement is appreciated
1 2 3 4
A B
(a)
(b)
X-position of appendage tip (mm)

C P5 P4 P3 P2 P1 0 1
corr'n
150° 0
Pereopod Angle
150°
90° 90°
30°
30°
Force (μN)
400 RS
0.05
Time (s)
200 return-stroke transient
0 RS
Appendage
90° A1 90°
Angle
A2
Maxilliped
60° Thorax
30°
Urosome 60° RS
30° 0.10
0°
0 5 10 15 20 25 30 35
Time (ms)
Fig. 11.7.
Copepod appendage coordination and orientation. (A) Orthogonal views (a, plan view; b, side view) of a
tethered copepod exhibiting the escape response to a simulated predator (picojet). Each pair represents
successive positions (1–4) of copepod appendages during the escape response. Prior to escape, the plan
view (1a) of the copepod has a T-shape, with the side view showing the initial downward position of the
urosome (1b). When an escape is initiated, the antennules are folded down against the body (2a) at the
same time that the urosome is flexed behind the prosome (2a) and flipped anteriorly (2b). To increase the
surface area of the legs and urosome during the power stroke, the setae on the endopodites fan out while
rowing ventrally, and the setae on the exopodal rami fan out while flapping and extending laterally away
from body (3a). These expanded legs clap against the urosome (4b, shows both legs and urosome pointing
posteriorly), where the motion can produce a vortex jet. Here, at the end of the power stroke (4a, 4b), all the
legs as well as the urosome are trimmed with setae collapsing against each other. During multiple thrusts,
the antennules remain flexed against the body (4a, 4b), streamlining its shape to optimize speed and eva-
siveness (4a). (B) Traces of tip position of swimming legs: spatiotemporal analyses of the kinematics of leg
movement by an escaping female Temora longicornis show a precise rhythm of the sequential strokes of each
swimming leg. Symbols for pereopods: P5, solid triangles; P4, open diamonds; P3, solid squares; P2, open
inverted triangles; P1, solid circles. RS indicates the return stroke (adapted from van Duren and Videler
2003; with permission from the Journal of Experimental Biology). (C) Spatiotemporal analyses of the kin-
ematics and force production during a copepod escape show that maximum propulsive force is achieved
when the pereopods are nearly perpendicular to the direction of motion during the power stroke, when
the setulated leg segments are flared (left inset) to increase drag; drag is reduced during recovery stroke
by collapse of setal fan (right inset). Bottom plot indicates angular positions of other appendages and the
thoracic segments. Symbols for pereopods: P5, open triangles; P4, solid triangles; P3, open diamonds; P2,
open squares; P1, open circles. During the return stroke, pereopods return synchronously (solid circles)
(from Lenz et al. 2004, with permission from Elsevier).
(Fig. 11.7A). Timing is everything. A simple hop may rely solely on the flexion of the antennules,
but to execute a high-speed escape, all appendages are used. To leave the viscous realm, the
escape behavior is initiated by two opposing limb movements: a forward-directed retraction
of the urosome occurs at the same time as the downward flexion of the antennules. If only the
urosome retracted, the copepod would move backward, a consequence of initiating movements
at low Re. The multiple thoracic appendages used in the escape (the thoracic pereopods), the
fanning of their setal hairs, the size and number of muscles, the presence of resilin in the thoracic
leg joints—all point to the power derived from the legs. The legs and tail are essential for the
escape response (Gill and Crisp 1985). Together, the pair of antennules plus the multiple pairs of
legs and the strong urosome provide the force behind the escape. Furthermore, the discovery of
myelination of copepod axons (Davis et al. 1999) accentuates the speediness of this behavior and
the force achieved with acceleration. These appendages all must move in a precisely coordinated
manner where the downward-directed power stroke of the urosome to return to its initiating
position occurs simultaneously with the downward power stroke of the legs, bringing the uro-
some and legs against each other simultaneously.
To accelerate into a higher-Re regime, the copepod has many pairs of thoracic appendages
or swimming legs. Deployed metachronally (Fig. 11.7B), the most posterior pair of legs initiate
the fluid entrainment, and the sequential wave of stroking legs in the anterior direction further
accelerates the copepod relative to the fluid, advancing the copepod smoothly. A synchronous
deployment of all the legs could lead to a jerky discontinuous translation, resulting in a more
conspicuous (and dangerous) locomotory pattern. Like the cephalic appendages, these swim-
ming legs fan out during the power stroke and collapse together in the recovery stroke to reduce
drag, thus maximizing the thrust achieved. One stroke cycle produces a hop; many stroke cycles
result in a long-distance escape maneuver.
To evaluate the cost of propulsion, models must utilize nonsteady velocity with quantified
accelerative sequences. Models of Morris et al. (1985, 1990) examine the effects of leg length,
width, and rotation angle from analysis of thoracic swimming legs (pereopods) with the simpli-
fication to omit consideration of the antennules, second antennae, abdominal and furcal oscilla-
tions, or combinations of these. Morris et al. (1985) documented that each swimming leg moves
2.4 times faster during the power stroke than during the recovery stroke, based on mean angular
velocity. Based on these kinematics, Morris et al. (1985) modeled the sequence of force produc-
tion to show the temporal variation in force intensity, with peaks for each leg stroke. As assumed
in Morris’s model, the exopod and endopod are fully separated and extended, and setae rotate
away from the limbs during the power stroke, exposing maximal surface area. During recovery,
the exopod pulls in toward the endopod and setae, which are inserted posteriorly, rotate pas-
sively backward, and close to the limbs to reduce the frontal area. By bending posteriorly at
several joints, the legs fold closer to the ventral surface.
Measurements by Lenz et al. (2004) show that the frontal area during the power stroke is
twice that during the recovery stroke, maximizing and minimizing the leg surface area dur-
ing power and recovery strokes, respectively. Lenz et al. (2004) coupled the visual observations
with direct measurements of force by tethering the copepods to a force transducer. They found
that one of the larger calanoid copepods, Calanus finmarchicus, produced forces of 500–600 μ N
and energy outputs estimated at 8 × 107 J during the pereopod power stroke sequence. “Per gram
of muscle, this is one of the higher rates of energy output yet reported in cold-blooded animals”
(Lenz et al. 2004, 134). Mapping the force dynamics over the angle of the leg (Fig. 11.7C) shows
that the peak in force production occurs when the limb is perpendicular or just posterior of 90°
to the body, leading to the conclusion of Lenz et al. (2004) that copepods rely on drag-based
paddling for their escape. A capture lunge by a carnivorous copepod also requires a forceful leap
using the same pereopod motion as during escapes to counter the fast extension of the robust,
sparsely setulated maxilliped. The antennules and the urosome bend, preparing the copepod for
a rapid leap that is provided by the simultaneous power stroke of the swimming legs collapsing
against the power stroke of the urosome, culminating in the ejection of a jet of fluid. Fine-scale
adaptations show that, while all copepods close their rami and flex their legs posteriorly, the
carnivorous copepod can feather its oarlike rami to form a median keel that the particle feeding
copepods cannot do (Boxshall 1985). Perhaps this keel helps with the accuracy of the aim of the
capture lunge.
A B → 1 cm s–1
0.5 1.4
1.2
1.0
0.8
0.6
0.4
y (cm)
0.2
0 0.0
cm s–1
–0.5
0 0.5 1
x (cm)
→ 1 cm s–1
0.5 1.4
1.2
1.0
0.8
0.6
0.4
z (cm)
0.2
0 0.0
cm s–1
–0.5
0 0.5 1
x (cm)
C D
plain mouse trap trap with paddling plate
paddler paddler/jetter
Fig. 11.8.
Anterior and posterior flow fields created by the locomotory appendages of the aquatic microcrusta-
cean copepod. (A) Particle pathlines, obtained using particle image velocimetry, show left/right sym-
metry (top) and dorsal/ventral asymmetry (bottom) in the anterior flow field created by the cephalic
appendages of a freely swimming Euchaeta antarctica (from Catton et al. 2007, with permission from the
Journal of Experimental Biology). Flow pathlines show a small diversion toward the reciprocating cephalic
appendages, yet the flow field remains smooth and laminar after passing by the thorax of the copepod.
(B) Orthogonal vector fields (top panel, plan view; bottom panel, side view) showing high-velocity zones
near cephalic appendages of freely swimming Euchaeta antarctica, with lateral symmetry (top panel) and
a maximum velocity (longest vectors = 1.4 cm/s) achieved ventrally (bottom panel). (C) Schlieren images
visualize the posterior flow fields or wakes left by copepods moving at different speeds. When swimming
slowly, a smooth, laminar, trail-like wake (top) is left at Re = 10. A large copepod impulsively accelerates,
leaving toroidal horseshoe vortices (bottom), coasting at Re = 300. Scale bar, 4 mm. (D) Enhanced speed
of an escaping copepod relying on jet propulsion was tested by using a modified mousetrap apparatus. A
mousetrap with a single “paddling” plate on the spring mechanism (top right) collapsing against two side
plates moved faster by jetting (bottom right), with a second bottom plate in place, than by paddling (bot-
tom left), without the second bottom plate (additional light gray plate added to equalize mass). The pad-
dling plate of the mouse trap model represents the paddling legs; the second (bottom) plate represents the
urosome, and the two side plates represent the flared exo- and endopods of the paddling pereopods. The
entire trap was suspended off a guideline in a highly viscous medium (corn syrup) so as to closely approxi-
mate the dynamics of the real copepod moving in water (from Liu 1996, used with permission).
Wakes
When considering the morphology of a copepod, we generally examine the exoskeletal form.
While the chitinous exoskeleton is important in identifying species or as an assessment of visual
signal size, the flow field created as these appendages move through water defines the unit cope-
pod + flow field, which is sensed by its mechanoreceptive neighbors. This flow field can magnify
the presence of the copepod up to 10 times its purely exoskeletal form if the edges of the flow are
defined by the threshold strain rate that evokes perception by other mechanoreceptive plank-
ters (Catton et al. 2007). The hydrodynamic disturbance generated by a copepod comprises two
sectors: an anterior flow field and the posterior wake (Fig. 11.8).
Anterior Flow Field
The anterior flow field (Fig. 11.8A,B) accomplishes several functions. For herbivores, the
high-velocity current advects a large funnellike volume that entrains odor signals, as well as prey
that have limited mobility and limited sensitivity. These herbivorous copepods maximize the
volume scanned by generating a strong, symmetrically strained flow field (Pleuromamma, Fields
and Yen 1993). Phycospheres, which are odor fields exuded by phytoplankton cells, and phe-
romonal signals excreted by reproductively receptive adult copepods are stretched in the lami-
nar streamlines, reaching the sensors prior to encounter with the prey (particle) or mate, giving
advanced warning of their approach (Moore et al. 1999). To maximize the volume scanned, a
copepod can hover, tethered by the balance of forces created by the reciprocation of three sets
of cephalic appendages that are opposed by the weight of the chitinous protein-rich body mass
(Strickler 1982).
For carnivores, the flow field is a bit more complex. These copepods capture lively rheo-
tactic prey. A different construction of the flow field allows a choreographed interplay of the
predator, the prey, and the velocity gradients of the biologically generated flow. Predator flow
is broad, with lower velocities, so strain rates are weaker, just enough to evoke a short hop but
not a full escape (Fields and Yen 1997b). Copepod prey that are entrained are reoriented by the
bottom-heavy mass distribution and the alignment of the elliptical body parallel to the stream-
lines. The double vorticity field concentrates the prey centrally, gathering them closer to the
centrally located mouth (Fields and Yen 1997b). When a mobile prey enters the flow field, the
strain rate triggers a jump response of the prey. As a consequence of the reorientation of the
copepod body in the flow, the copepod prey jumps, so its wake is directed toward the sensory
setae of the antennules. As soon as the prey wake is close enough to cross the threshold signal
strength indicating that prey of the preferred size is within reach by being in the capture volume
(Doall et al. 2002), the capture response by the predator is evoked (Fields and Yen 2002). Such
focused jetlike hydrodynamic features in the wake cast off by the escaping prey bend the linear
array of mechanoreceptive setae to inform the equally mechanosensitive predatory copepod
of the distance, size, speed, and location of the prey. The prey, trapped in the cage of serrated
setules of the paired maxillipeds, is subdued by first removing locomotory appendages: pere-
opods and antennules (Yen 1985). Then the predatory copepod maneuvers the now limbless
copepod prey such that the ellipsoid prey morsel is positioned with the small end toward the
mouth, where sharp silica-capped teeth sink into the chitinous carapace to access the lipid- and
protein-rich internal contents. Empty exoskeletons may be left for scavengers. Hence, the ante-
rior flow field can function both as a feeding current and a sensory field, achieved through the
coordinated movements of precisely oriented appendages at controlled speeds.
To summarize, the anterior flow field has two dominant forms: high-intensity flow in a fun-
nel versus broader channel. For herbivores, high-intensity flow maximizes the volume scanned
to collect food particles, utilizing smoothly oscillating, finely setulated fanlike head append-
ages. Carnivores generate a double-sheared field with robust, sparsely setulated head append-
ages, where the vorticity field serves to aggregate prey and evoke escapes when within capture
range. For mate-seeking copepods, such as males of Euchaeta, we expect flow fields more like
an herbivore as its purpose is to collect water-borne chemical pheromones, not food. Hovering
copepods entrain a funnel-shaped flow, while freely swimming copepods interact with broader
channel flow (Yen and Strickler 1996).
Posterior Flow Field
Lenz et al. (2004) did not find evidence for jet propulsion in their tethered copepods. Yet jets
and toroids (Yen and Strickler 1996) have been imaged using Schlieren optics (Fig. 11.8C). When
the urosome and legs meet, a toroidal jet is produced in the wake. Multiple distinct toroids are
produced during the oscillations of the urosome that occur simultaneously with the power
stroke of the legs. To determine if the orifice forming the nozzle of the jet is produced by the
urosome on the top of the orifice and legs on the bottom flanked by a viscous fluid, Liu (1996)
made a dynamically scaled model: a Victrola mousetrap with a top plate representing the uro-
some collapsing against the bottom plate representing the legs, equipped with and without side
plates (Fig. 11.8D). The mousetrap with the side plates moved faster and farther than the one
without. Computational fluid dynamic models also show the formation of coherent vertical
structures. A jetlike pressure field is generated by computational fluid dynamic models that use
the prescribed kinematics (Gilmanov and Sotiropoulos 2005). In their model, the flexion of the
antennules creates a counterclockwise startup eddy that pushes the clockwise rotating body
eddy away. This forward-directed and thus drag-producing clockwise eddy is formed from the
previous recovery stroke. The interaction of these eddies, enhanced by the tail and leg move-
ments, starts the generation of a pocket of downstream-directed thrust jet. Simulations suggest
that the bursts of thrust produced during the power stroke of an escaping copepod propel the
animal forward, possibly allowing it to coast during the drag-inducing recovery stroke because
of the inertial forces of the now accelerating body. The production of nonlaminar fluid dynamic
features confirms the move into an inertial realm. Jets also have been documented to evoke
escapes as well as captures (Fields and Yen 2002), indicating that a jet is a signal that is detectable
by a copepod and that copepods have evolved to react appropriately to this kind of signal. Jiang
and Kiørboe (2011) showed how the vortex shed by the self-propelled body can interact with the
vortex generated in the wake, canceling each other, thus minimizing the strength of the fluid
signal and possibly serving as a tactic for hydrodynamic camouflage.
In conclusion, the 11 sets of paired appendages attached to an articulated body give copep-
ods a diverse repertoire of possible locomotory tactics. Their size and speed of movement allow
them to use viscous forces to paddle and organize their local fluid environment or leave coherent
wakes. Shifting the balance to a regime where more inertia can be gained, the copepod can rake
out nutritious food particles or jet quickly away from an attacking predator. Many copepod spe-
cies show different patterns of movement. Some patterns are common for copepods and could
be considered different gaits, as follows. When no appendages are moving, the negatively buoy-
ant copepod in its three-dimensional fluid environment sinks. Barely disturbing the surround-
ing flow, this is a good tactic for hiding from movement-dependent perceivers. When only the
head appendages oscillate and reciprocate, the copepod can hover in place, moving water past
its body, or the copepod can cruise smoothly with forward translation of the body. When all tho-
racic appendages, urosome, and antennules are flexed, the copepod is able to accelerate rapidly
when escaping , often entering an intermediate to high-Re regime (Re = 10–1000). With so many
branched appendages with different angles of movement, a copepod has the ability to modify
the shape of the flow field to its advantage: hide, hover and collect water and particles, cruise
to explore another patch, or escape to leave quickly. All point to a well-evolved life of plankton
adapted to the three-dimensional fluid environment.
DO OTHER MEMBERS OF THE PLANKTON EXHIBIT THESE DUALITIES?
As emphasized in the first section, copepods live at the interface between two regimes: lami-
nar and turbulent domains. They balance two forces: viscosity and inertia. They drift in the
ocean at the large scale but maneuver agilely at the small scale. Copepods move slowly, cleanly
swimming through the viscous medium, leaving a thin wake, barely discernable by mech-
anoreceptors of other animals. With little momentum, chemical cues exuded by the moving
copepod stick around, dispersed by the slow rate of molecular diffusion. In this low-Re regime,
the coherent chemical trail has become an indispensable signal, a distinct chemical wake that
males are able to follow (Yen et al. 1998). Copepods also move quickly and impulsively, thin-
ning the boundary layer surrounding their body and appendages. Without the hindrance of
the viscous boundary layer, predators can use their capture appendages to grab their prey
without pushing them away, prey can escape quickly without entraining their captors, and
dispersive wakes are left that contain little directional information allowing them to “disap-
pear” into the surrounding f low.
Do other plankters also exhibit these dualities, alternately using the two forces of viscosity
and inertia to make the transition between the fluid domains characterized by laminar versus
turbulent properties to accomplish their survival tactics? And if so, do they also exhibit similar
morphological adaptations and behavioral repertoires to take advantage of living at intermedi-
ate Re? In this final section, comparisons are made between the holoplanktonic krill that spend
their entire life in the open ocean and the meroplanktonic stages of benthic organisms that
begin life as freely dispersing larvae (Table 11.2).
To assess this, the “simply” calculated Re will be used. But is it really so simple? If L is the
length of the surface moving against the flow, do we use body length, body width, leg length,
or expanded width of leg while in the power stroke? If U is the speed of movement through
the fluid, do we use swimming speed, flow speed of the wake, or speed of the moving tip of
the locomotory appendage? Since viscosity varies as a function of temperature, do Antarctic
pelagic crustaceans, which live at viscosities twice that of tropical species, have different
appendage morphology?
For example, the Antarctic krill Euphausia superba can have Re = 3600 for a body length of
60 mm and speed of 1 bl/s or 60 mm/s, but Re = 1200 if we use the body width of 20 mm as the
length scale. And for a krill limb, Relimb is 315, calculated as follows. Arc distance = R × [2π ×
(C/360°)], where C is the central angle of the arc in degrees, and R is the radius of the arc. If the
stroke angle is 60° and the length of the krill leg is 5 mm, the arc distance is 5 mm. Since the limb
oscillates at 5 Hz, the speed of the leg = 25 mm/s. If the width of the expanded leg is twice the
body width (about one-third its length), or 12.6 mm, and that is used as the length scale, then
Relimb for the krill leg is 315.
If flow is laminar when Re < 2300, transient when 2300 < Re < 4000, and turbulent when 4000
< Re, then the krill operates at transitional Re. Asymmetry is used for the paddling legs, flaring
during the power stroke and collapsing during the recovery stroke. Using a drag-based model,
the metachronal rhythm of the pleopod paddling was calculated to be the best for achieving
the highest swim speed (Alben et al. 2010). This is important for krill that travel 10 km/day or
200,000 bl/day. However, when we examine the flow field of the wake of E. superba, it is not
laminar. Do krill also exhibit suitable behaviors to balance viscous and inertial forces?
Table 11.2. Reynolds number regimes occupied by aquatic arthropods of increasing

size.
Animal Size Speed Re Reference

Euterpina acutifrons 0.1 mm 0.98 mm/s 0.1 Titelman and
nauplii Kiørboe 2003
Heterosaccus 0.2–0.3 3–4 mm/s 0.6–1.2 Walker 2004
lunatus nauplii mm
Bosmina longirostris 0.3 mm 1.5 mm/s 0.5 Zaret and Kerfoot
1980
Heterosaccus 0.3 mm 10 mm/s 3 Walker 2004
lunatus cyprids
Semibalanus 0.3 mm 4.3 mm/s 4–13 Singarajah 1969
balanoides nauplii
Temora longicornis 0.3 mm 0.57 mm/s 0.18 Titelman and
nauplii Kiørboe 2003
Artemia salina 0.4–4 mm 1.8–9.9 mm/s 0.7–40 Williams 1994
larvae
Semibalanus 1 mm 50 mm/s 50 Yule 1982, Crisp
balanoides cyprids 1955
Triops cancriformis 1.2 mm 3.5 mm/s 4 Fryer 1988
larvae
Centroptilum 2–6 mm 1–7 mm/s 2–22 Sensenig et al.
triangulifer mayfly (flow speed 2009
nymph through gills)
Antarctomysis sp., 5–10 mm 20–40 mm/s 100–400 Schabes and
Neomysis rayii, Hamner 1992
Acanthomysis
sculpta mysids
Brachyuran crab 7–27 mm 2–4 mm/s 10–100 Sulkin 1984,
larvae Forward et al. 1996
Cancer magister 10 mm 85–448 mm/s 850–4500 Fernandez et al.
Dana megalopae 1994
Speleonectes lucay- 15 mm 6.7 mm/s 100 Kohlhage and
ensis remipede Yager 1994
Enallagma 19 mm 150 mm/s 3000 Brackenbury 2002
cyathigerum dam-
selfly larva
Euphausia pacifica 20 mm 30 mm/s 500 De Robertis et al.
2003
Idotea resecata 35 mm 120 mm/s 4200 Alexander 1988
isopod
Sergestes similis 43.5 mm 74 mm/s 3200 (though Cowles 1994
penaeid shrimp would be
smaller for
juveniles)
Euphausia superba 60 mm 300 mm/s ≤1,0000 Kils 1981
The data in Table 11.2 show that many aquatic arthropods live at this transitional fluid
regime, where many of these organisms rely on viscous as well as inertial forces to propel
themselves. Variations in appendage morphology and kinematics through ontogeny can be
compared to variations observed for different sizes. Asymmetry in locomotory movement and
the surface area of appendages used during reciprocating propulsive strokes should be apparent
for small, slower-moving arthropods, while streamlining of the body will be noted for larger,
faster-moving plankton. How do these other planktonic organisms adapt to this special niche?
Are their appendages and behaviors specially shaped to enable them to maneuver in this tran-
sitional realm? To address these questions, research is needed not only on the morphology of
the appendages but also on the dynamics of their propulsive wakes, locomotory appendage
kinematics, and behavioral reactions to fluid flow. Now, with the improvements in visualizing
flow and capturing high-speed movements, along with secrets revealed for evoking specific
behaviors in response to certain cues, fascinating studies of animal-fluid interactions of so many
aquatic crustaceans are possible to test these intriguing hypotheses.
REFERENCES
Alben, S., K. Spears, S. Garth, D. Murphy, and J. Yen. 2010. Coordination of multiple appendages in
drag-based swimming. Journal of the Royal Society Interface 7:1545–1557.
Alcaraz , M., E. Saiz , and A. Calbet. 2007. Centropages behavior: Swimming and vertical migration.
Progress in Oceanography 72:121–136.
Alexander, D.E. 1988. Kinematics of swimming in two species of Idotea (Isopoda: Valvifera). Journal of
Bollens , S.M., and B.W. Frost. 1989. Zooplanktivorous fish and variable diet vertical migration in the
marine planktonic copepod Calanus pacificus . Limnology and Oceanography 34:1072 –1083.
Borazjani, I., F. Sotiropoulos, and E. Malkiel. 2010. On the role of copepod antennae in the production of
hydrodynamic force during hopping. Journal of Experimental Biology 213:3019 –3035.
Boxshall, G.A. 1982. On the anatomy of the misophrioid copepods, with special reference to
Benthomisophria palliate Sars. Philosophical Transactions of the Royal Society of London
297:125–181.
Boxshall, G.A. 1985 . The comparative anatomy of two copepods, a predatory calanoid and a
particle-feeding mormonilloid. Philosophical Transactions of the Royal Society of London
311:303–377.
Brackenbury, J. 2002. Kinematics and hydrodynamics of an invertebrate undulatory swimmer: The
damsel-fly larva. Journal of Experimental Biology 205:627–639.
Bradford-Grieve, J.M. 2002. Colonization of the pelagic realm by calanoid copepods. Hydrobiologia
485:223–244.
Bundy, M.H., T.F. Gross, D.J. Coughlin, and J.R. Strickler. 1993. Quantifying copepod searching effi-
ciency using swimming pattern and perceptive ability. Bulletin of Marine Science 53:15–28.
Catton, K.B., D.R. Webster, J. Brown, and J. Yen. 2007. Quantitative analysis of tethered and
free-swimming copepodid flow fields. Journal of Experimental Biology 210:299 –310.
Catton, K.B., D.R. Webster, S. Kawaguchi and J. Yen. 2011. The hydrodynamic disturbances of two
species of krill: implications for aggregation structure. J. Exp. Biology 214: 1845–1856.
Cheer, A.Y.L., and M.A.R. Koehl. 1987. Paddles and rakes: Fluid flow through bristled appendages of
small organisms. Journal of Theoretical Biology 129:17–39.
Cowles, D.L. 1994 . Swimming dynamic of the mesopelagic vertically migrating penaeid shrimp Sergestes
similis: Modes and speeds of swimming. Journal of Crustacean Biology 14:247–257.
Crisp, D.J. 1955 . The behavior of barnacle cyprids in relation to water movement over a surface. Journal of
Davis, A.D., T.M. Weatherby, D.K. Hartline, and P.H. Lenz. 1999. Myelin-like sheaths in copepod axons.
Nature 398:571.
Denhardt, G., B. Mauck , and W. Hanke, 2001. Hydrodynamic trail-following in harbor seals (Phoca
vitulina). Science 293:102–104.
De Robertis, A., C. Schell, and J.S. Jaffe. 2003. Acoustic observations of the swimming behavior of the
euphausiid Euphausia pacifica Hansen. Journal of Marine Science 60:885–898.
Doall, M.H., S.P. Colin, J.R. Strickler, and J. Yen. 1998. Locating a male in 3D: the case of Temora longi-
cornis. Philosophical Transactions of the Royal Society of London Series B 353:681–689.
Doall, M.H., J.R. Strickler, D.M. Fields, and J. Yen. 2002. Mapping the free-swimming attack volume of a
planktonic copepod, Euchaeta rimana. Marine Biology 140:871–879.
Fernandez , M., O.O. Iribarne, and D.A. Armstrong. 1994 . Swimming behavior of Dungeness crab, Cancer
magister Dana, megalopae in still and moving water. Estuaries 17:271–275.
Fields, D.M., and M.J. Weissburg. 2005 . Evolutionary and ecological significance of mechanosensor mor-
phology: Copepods as a model system. Marine Ecology Progress Series 287:269 –274.
Fields, D., and J. Yen. 1993. Outer limits and inner structure: The 3-dimensional flow field of
Pleuromamma xiphias (Calanoida: Metridinidae). Bulletin of Marine Science 53:84–95.
Fields, D.M., and J. Yen. 1997a . The escape behavior of marine copepods in response to a quantifiable
fluid mechanical disturbance. Journal of Plankton Research 19:1289 –1304.
Fields, D.M., and J. Yen. 1997b. Implications of the feeding current structure of Euchaeta rimana, a
carnivorous pelagic copepod, on the spatial orientation of their prey. Journal of Plankton Research
19:79 –95.
Fields, D.M., and J. Yen. 2002. Fluid mechanosensory stimulation of behavior from a planktonic marine
copepod Euchaeta rimana. Journal of Plankton Research 24:747–755.
Folt, C., and C.R. Goldman. 1981. Allelopathy between zooplankton: A mechanism for interference
competition. Science 213:1133–1135.
Forward, R.B., Jr., R.A. Tankersley, and J.S. Burke. 1996. Endogenous swimming rhythms of larval
Atlantic menhaden, Brevoortia tyrannus Latrobe: Implications for vertical migration. Journal of
Frost, B.W. 1972. Effects of size and concentration of food particles on the feeding behavior of the marine
planktonic copepod Calanus pacificus. Limnology and Oceanography 17:805–825.
Branchiopoda). Philosophical Transactions of the Royal Society of London 321:27–124.
Gill, C.W., and C.J. Crisp. 1985 . Sensitivity of intact and antennules amputated copepods to water distur-
bance. Marine Ecology Progress Series 21:221–227.
Gilmanov, A., and F. Sotiropoulos. 2005 . A Hybrid cartesian/immersed boundary method for simu-
lating flows with 3D geometrically complex moving bodies. Journal of Computational Physics
207:457–492.
Holzman, R., and P.C. Wainwright. 2009. How to surprise a copepod: Strike kinematics reduce hydro-
dynamic disturbance and increase stealth of suction-feeding fish. Limnology and Oceanography
54:2201–2212.
Hwang , J.-S ., J.H. Costello, and J.R. Strickler. 1994 . Copepod grazing in turbulent flow: Elevated forag-
ing behavior and habituation of escape reactions. Journal of Plankton Research 16:421–431.
Huys, R., and G.A. Boxshall. 1991. Copepod evolution. Ray Society, London.
Jiang , H., and T. Kiørboe. 2011. The fluid dynamics of swimming by jumping in copepods. Journal of the
Royal Society Interface 8:1090 –1103.
Jiang , H., and G.A.Paffenhöfer. 2008. Hydrodynamic signal perception by the copepod Oithona plumif-
era. Marine Ecology Progress Series 373:37–52.
Kils, U. 1981. Swimming behaviour, swimming performance, and energy balance of Antarctic krill,
Euphausia superba. BIOMASS Scientific Series 3:1–122.
Kiørboe, T., A. Andersen, V.J. Langlois, H.H. Jakobsen, and T. Bohr. 2009. Mechanisms and feasibility of
prey capture in ambush-feeding zooplankton. Proceedings of the National Academy of Sciences of
the USA 106:12394–12399.
Koehl, M.A.R. 2001. Transitions in function at low Reynolds number: Hair-bearing animal appendages.
Mathematical Methods in Applied Sciences 24:1523–1532.
Kohlhage, K., and J. Yager. 1994 . An analysis of swimming in remipede crustaceans. Philosophical
Lenz , P.H., A.E. Hower, and D.K. Hartline. 2004 . Force production during pereiopod power strokes in
Calanus finmarchicus. Journal of Marine Systems 49:133–144.
Lenz , P.H., and J. Yen. 1993. Distal setal mechanoreceptors of the first antennae of marine copepods.
Bulletin of Marine Research 53:170–179.
Liu, J. 1996. Effects of morphology on the biomechanics of the high speed escape reaction of copepods:
Developmental and species differences. MS thesis, State University of New York , Stony Brook .
Malkiel, E., J. Sheng , J. Katz , and J.R. Strickler. 2003. The three-dimensional flow field generated by a
feeding calanoid copepod measured using digital holography. Journal of Experimental Biology
206:3657–3666.
Mauchline, J. 1998. The biology of calanoid copepods. Advances in Marine Biology 33:1–710.
Michels, J., and S.B. Schnack-Schiel. 2005 . Feeding in dominant Antarctic copepods- does the morphol-
ogy of the mandibular gnathobases relate to diet? Marine Biology 146:483–495.
Moore, P.A., D.M. Fields, and J. Yen. 1999. Physical constraints of chemoreception in foraging copepods.
Morris, M.J., G. Gust, and J.J. Torres. 1985 . Propulsion efficiency and cost of transport for copepods: A
hydromechanical model of crustacean swimming. Marine Biology 86:283–295.
Morris, M.J., K. Kohlhage, and G. Gust. 1990. Mechanics and energetics of swimming in the small cope-
pod Acanthocyclops robustus (Cyclopoida). Marine Biology 107:83–91.
Nishida, S., and S. Ohtsuka. 1996. Specialized feeding mechanism in the pelagic copepod genus
Heterorhabdus (Calanoida: Heterorhabdidae), with special reference to the mandibular tooth and
labral glands. Marine Biology 126:619 –632.
Ohtsuka, S., and R. Huys. 2001. Sexual dimorphism in calanoid copepods: Morphology and function.
Ohtsuka, S., H.Y. Soh, and S. Nishida. 1997. Evolutionary switching from suspension feeding to carnivory
in the calanoid family Heterorhabdidae (Copepoda). Journal of Crustacean Biology 17:577–595.
Pohlmann, K., F. Grasso, and T. Breithaupt. 2001. Tracking wakes: The nocturnal predatory strategy of
piscivorous catfish. Proceedings of the National Academy of Science of the USA 98:7371–7374.
Poulet, S.A., and G. Ouellet. 1982. The role of amino acids in the chemosensory swarming and feeding of
marine copepods. Journal of Plankton Research 4:341–361.
Schabes, M., and W. Hamner. 1992. Mysid locomotion and feeding: Kinematics and water-flow patterns
of Antarctomysis sp., Acanthomysis sculpta, and Neomysis rayii. Journal of Crustacean Biology 12:1–10.
Schmitt, F.G., and L. Seuront. 2001. Multifractal random walk in copepod behavior. Physica A
301:375–396.
Sensenig , A.T., K.T. Kiger, and J.W. Shultz. 2009. The rowing-to-flapping transition: Ontogenetic
changes in gill-plate kinematics in the nymphal mayfly Centroptilum triangulifer (Ephemeroptera,
Baetidae). Biological Journal of the Linnean Society 98:540 –555.
Singarajah, K.V. 1969. Escape reactions of zooplankton: The avoidance of a pursuing siphon tube. Journal
of Experimental Marine Biology and Ecology 3:171–178.
Strickler, J.R. 1982. Calanoid copepods, feeding currents, and the role of gravity. Science 218:158 –160.
Strickler, J.R. 1984 . Sticky water: A selective force in copepod evolution. Pages 187–239 in D.G. Meyers
and J.R. Strickler, editors. Trophic interactions within aquatic ecosystems. Westview Press,
Boulder, CO.
Sulkin, S.D. 1984 . Behavioral basis of depth regulation in the larvae of brachyuran crabs. Marine Ecology
15:181–205.
Tiselius, P. 1992. Behavior of Acartia tonsa in patchy food environments. Limnology and Oceanography
37:1640–1651.
Titelman, J., and T. Kiørboe. 2003. Motility of copepod nauplii and implications for food encounter.
Marine Ecology Progress Series 247:123–135.
van Duren, L.A., and J.J. Videler. 2003. Escape from viscosity: The kinematics and hydrodynamics of
copepod foraging and escape swimming. Journal of Experimental Biology 206:269 –279.
Vogel, S. 1994 . Life in moving fluids, 2nd ed. Princeton University Press, Princeton, NJ.
Walker, G. 2004 . Swimming speeds of the larval stages of the parasitic barnacle, Heterosaccus lunatus
(Crustacea: Cirripedia: Rhizocephala). Journal of Marine Biological Association of the UK 84:
737–742.
Weissburg , M.J., M.H. Doall, and J. Yen. 1998. Following the invisible trail: Kinematic analysis of mate
tracking in the copepod Temora longicornis. Philosophical Transactions of the Royal Society of
London Series B 353:701–712.
Wiggert, J.D., A.G.E. Haskell, G.A. Paffenhöfer, E.E. Hofmann, and J.M. Klinck. 2005 . The role of feed-
ing behavior in sustaining copepod populations in the tropical ocean. Journal of Plankton Research
27:1013–1031.
Williams, T.A. 1994 . A model of rowing propulsion and ontogeny of locomotion in Artemia larvae.
Biological Bulletin 187:164–173.
Williamson, C. 1981. Foraging behavior of a freshwater copepod: Frequency changes in looping behavior
at high and low prey densities. Oecologia 50:332–336.
Wilson, S.E. 2001. Predator-prey interactions in the plankton: Escape responses of three calanoid cope-
pod species from a juvenile fish. MS thesis, State University of New York , Stony Brook .
Yen, J. 1985 . Selective predation by the carnivorous marine copepod Euchaeta elongata: Laboratory
measurements of predation rates verified by field observations of temporal/spatial feeding patterns.
Limnology and Oceanography 30:577–595.
Yen, J. 1988. Directionality and swimming speeds in predator-prey and male-female interactions of
Euchaeta rimana, a subtropical marine copepod. Bulletin of Marine Science 43:175–193.
Yen, J. 2000. Life in transition: Balancing inertial and viscous forces by planktonic copepods. Biological
Bulletin 198:213–224.
Yen, J., J. Brown, and D.R. Webster. 2003. Analysis of the flow field of the krill, Euphausia pacifica. Marine
and Freshwater Behaviour and Physiology 36:307–319.
Yen, J., A. Prusak , M. Caun, M.H. Doall, J. Brown, and J.R. Strickler. 2004 . Signaling during mating in
the pelagic copepod, Temora longicornis . Pages 149–159 in L. Seuront and P. Strutton, editors. Scales
in aquatic ecology: Measurements, analysis, modeling. CRC Press, Boca Raton, FL .
Yen, J., and J.R. Strickler. 1996. Advertisement and concealment in the plankton: What makes a copepod
hydrodynamically conspicuous? Invertebrate Biology 3:191–205.
Yen, J., M.J. Weissburg , and M.H. Doall. 1998. The fluid physics of signal perception by a mate-tracking
copepod. Philosophical Transactions of the Royal Society of London Series B 353:787–804.
Yule, A.B. 1982. The application of new techniques to the study of planktonic organisms. PhD disserta-
tion, University of Wales, Bangor.
Zaret, R.E., and C.W. Kerfoot. 1980. The shape and swimming technique of Bosmina longirostris.
12
SWIMMING FAST AND FURIOUS: BODY AND LIMB
PROPULSION AT HIGHER REYNOLDS NUMBERS
Michel A. Boudrias
Abstract
In swimming crustaceans, a cascade of forces at different Reynolds numbers affect bodies,
propulsive limbs, and their setae and setules. This chapter reviews major examples of crus-
taceans swimming at moderate to high Reynolds numbers (103 to 105) by defining the three
major modes of locomotion used by crustaceans that either have the size (centimeters to
meters) or the velocity (tens of centimeters per second or more) to swim at higher Reynolds
numbers. The modes they use to achieve fast and furious swimming include (1) drag-based
swimming with setose flagellar or paddle-shaped limbs (thoracic exopodites, modified fifth
pereopods, pleopods) in many crustacean classes, (2) lift-based sculling in portunid crabs, and
(3) jet propulsion using strong abdominal flexion and morphological modifications of the tail
fan and anterior limbs in a wide variety of malacostracans. This chapter describes the modes of
swimming that lead to motion at higher Reynolds numbers and analyzes the functional mor-
phology of propulsive limbs and the body design modifications that enhance streamlining.
This chapter concludes with major challenges related to the need for more systematic and inte-
grated studies of (a) propulsive and directional limbs, body design, and feeding behaviors; (b)
physiology and neurobiology affected by functional morphology; and (c) kinematics and fluid
dynamics of locomotion. This review should lead to a more comprehensive approach to the
study of crustacean body and limb design to further enhance our understanding of swimming
at higher Reynolds numbers in Crustacea.
INTRODUCTION
The large size range of crustaceans, the wide array of modes of locomotion, and the differ-
ent types of propulsive limbs responsible for locomotion mean that crustaceans encounter
319
physical forces on a variety of scales in all aquatic realms. In particular, swimming crus-
taceans move their bodies at moderate to high Reynolds numbers (Re = 10,000–100,000),
their propulsive limbs at intermediate Re values (100–10,000), and the setae and setules of
the pereopods, pleopods, and/or uropods at very low to low Re values (0.01–10). This cas-
cade of forces affecting locomotion leads to design constraints and affects the size, shape,
and functional morphology of the whole body: the anterior nonswimming limbs (anten-
nae, antennules, chelipeds), the thoracic propulsive limbs (especially exopodites), and the
main abdominal swimming appendages (pleopods, uropods, and telson). The Malacostraca
encompass the vast majority of crustacean swimmers that have either the size (centimeters to
meters) or the velocity (tens of centimeters per second or more) to swim at higher Reynolds
numbers. The modes they use to achieve fast and furious swimming include (1) drag-based
propulsion, typically using either the exopodite of their thoracic limbs (Neil et al. 1976, Ford
et al. 2005, Mehrtens et al. 2005) or modified posterior sets of pereopods (Munnidopsidae);
(2) drag-based propulsion using three or more pairs of pleopods, or swimmerets with meta-
chronal beat patterns (virtually all crustaceans); (3) lift-based propulsion using modified
fifth pereopods (Portunidae); and (4) jet propulsion using strong abdominal f lexion and
morphological modifications of the tail fan (uropods and telson) for propulsion and modi-
fications of the antennae, rostrum, and/or chelipeds for directional control (e.g., lobsters,
crayfish, and many shrimp).
This chapter reviews crustaceans that swim at intermediate Reynolds numbers by analyz-
ing the functional morphology of main propulsive limbs with a particular focus on pleopods,
the body design modifications that enhance streamlining, and the modes of swimming that
lead to motion at higher Reynolds numbers. This chapter uses the diversity of form and func-
tion in amphipod pleopods as the model for propulsive limbs and concludes with a challenge to
expand the study of crustacean body and limb design to further understand swimming at higher
Reynolds numbers in Crustacea.
Though crustacean swimming limbs are frequently mentioned in taxonomic descriptions,
there are very few detailed morphological analyses of swimming limbs and body design modi-
fications related to swimming and hydrodynamic forces. This is particularly true for larger
(centimeters or more) crustaceans and for those that swim at higher Reynolds numbers. In
order to systematically review limb-based propulsion for higher-Reynolds-number swim-
mers, each primary mode of locomotion is presented here separately, with pleopod propul-
sion analyzed more thoroughly. The first section is dedicated to the most commonly used,
drag-based propulsion, and the second section focuses on other modes (lift-based and escape
locomotion).
DRAG-BASED SWIMMING: THORACIC PROPUL SORS
Crustacean body design typically leads to regional specialization (tagmosis) even for locomo-
tion. In most large crustaceans, the thoracic limbs are modified and specialized as walking
limbs, but several groups have evolved thoracic swimming structures that can propel the ani-
mal rapidly and smoothly in midwater. There are three distinct propulsive modes: (1) rowing
thoracic exopods, (2) paddling phyllopodous thoracopods, and (3) pedaling specialized pos-
terior pereopods.
Rowing Thoracic Exopods
Though many of the more advanced malacostracans have uniramous pereopods, some groups
have biramous thoracic limbs with setose exopodites that can create currents using a metachronal
Body and Limb Propulsion at Higher Reynolds Numbers 321
Antennule
Antenna
Eye
Exopod
Endopod
Telson
Uropod
Fig. 12.1.
Drawing of Praunus showing main anatomical features and limb positions of thoracic locomotory append-
ages. The exopodites have been drawn in their correct phase relationship to one another and show the
wide setal fan on the power stroke and feathering on the return stroke. From Laverack et al. (1977), with
permission from the Royal Society of London.
beat pattern. Early work by Laverack et al. (1977) focused on mysid swimming using high-speed
film, comparing them to larval lobsters. They described the metachronal rowing and elliptical
paths needed for propulsion with multiple limbs and illustrated the typical design of crustacean
propulsive limbs: a muscular basis (enlarged and flattened in Praunus flexuosus) and an annu-
lated flagellum fringed with a setose distal fan of setae (Fig. 12.1). Additional analysis showed
similar patterns for euphausiids, which enhance their pleopod-driven locomotion with swing-
ing motions of their thoracic exopodites (Kils 1981). The spectacular images of Antarctic krill
swimming show multiple limbs with a clear coordination along the body from the exopodites of
the thorax to the pleopods of the abdomen (Kils 1981). The most systematic analysis of thoracic
limb motion was presented by Hessler (1985), with a particular emphasis on the lophogastrid
Gnathophausia ingens. Again, the motion is oarlike rowing but with a combination of thoracic
exopods and well-developed abdominal pleopods. The limb design here is no different than
mysids and euphausiids, but G. ingens is larger and swims faster and at a higher Reynolds number
(almost 105). Hessler (1985) provided the first detailed functional analysis of the muscles that
control the limbs and simple but elegant drawings of the swimming limbs. Of particular impor-
tance in Hessler’s paper is the survey of swimming structures in Crustacea (Table 12.1) listing
several groups that use thoracic exopods: Anaspidacea, Pancarida, Decapoda, Lophogastrida,
Mysida, Cumacea, and Mictacea. However, the comparison was based primarily, and almost
exclusively, on morphological design and not on kinematic and/or fluid dynamic analysis of
swimming; in fact, many of the groups listed were never observed swimming (see “Future
Challenges,” below).
Table 12.1. Survey of morphology of swimming structures in Crustacea (haphazard

sampling from within taxa, representing only major kinds of sustained swimming).
Taxon Swimming Structure of Ratio of Area of Setules

structure distal shaft peduncle setal fan
to limb vs. shaft
length
Various nauplii A2, A1, Md Flagellar 0.4–0.6 Equal, +, –
large
BRANCHIOPODA
Anostraca Thoracic Foliaceous 0.6 Small +
protopod and
rami
Notostraca Thoracic Foliaceous 0.5 Small +
protopod and
rami
Diplostraca A2 Flagellar rami 0.4 Large +
REMIPEDIA Trunk Foliaceous 0.3 Equal +
protopod and
rami
COPEPODA A2 Flagellar 0.6–0.7 Large +
exopods
Thoracic Foliaceous 0.3 Equal, +
rami large
BRANCHIURA Trunk Flagellar rami 0.5 Large +
OSTRACODA A1, A2 Flagellar shaft 0.7 Large +
and rami
ASCOTHORACICA Trunk, furca Foliaceous 0.4 Large +
rami
CIRRIPEDIA Trunk Slender rami ? Large +
(cypris larva)
MALACOSTRACA
Leptostraca Pleopods Slender rami 0.5 Large +
Hoplocarida Pleopods Foliaceous 0.3 Smaller +
rami
Syncarida Pleopods Flagellar 0.2 Large +
exopods
Anaspidacea Thoracic Flagellar 0.3 Large +
exopods
Pancarida Thoracic Flagellar 0.5 Equal, +
exopods large
Euphausiacea Pleopods Slender, semi- 0.4 Large +
flagellar rami
Decapoda Thoracic Semiflagellar 0.4 Large +
exopods
Pleopods Foliaceous or 0.5 Equal, +
flagellar rami large
(Continued)
Taxon Swimming Structure of Ratio of Area of Setules

structure distal shaft peduncle setal fan
to limb vs. shaft
length
Occasionally Flagellar ? Large +
thoracic
exopods
Mysidacea Pleopods Foliaceous 0.3 Large +
rami
Lophogastrida Thoracic Flagellar 0.4 Large +
exopods
Mysida Thoracic Flagellar 0.3 Large +
exopods
Cumacea Thoracic Flagellar 0.5 Large +
exopods
Tanaidacea Pleopods Foliaceous 0.4 Equal, +
rami large
Mictacea Thoracic Flagellar 0.5 Large +
exopods
Spelaeogriphacea Pleopods Foliaceous 0.5 Equal +
rami
Isopoda Pleopods Foliaceous 0.3 Small, large +
rami
Amphipoda Pleopods Flagellar rami 0.5 Large +
A1, first antenna; A2, second antenna; Md, mandible.

From Hessler (1985), with permission from the Royal Society of Edinburgh.
Paddling Phyllopodous Thoracopods
Hessler (1985) presented other examples of crustaceans that use thoracic limbs to swim, such as
the anostracans, notostracans, and conchostracans in the class Branchiopoda. They use phyllo-
podous thoracic limbs to swim, though typically at low to moderate Re values because they either
are small (millimeters to a few centimeters) or move relatively slowly or infrequently (see chapter
11 in this volume). But there are a few exceptions in the Branchiopoda, notably Branchinecta gigas,
B. ferox, and B. raptor, that reach sizes >10 cm and swim at Reynolds numbers on the order of
several thousands and even at Re = 10 4 using a metachronal beat of phyllopodous thoracic limbs
(Boudrias and Pires 2002). The design of phyllopodous limbs allows them to act like full paddles,
with the setae adding additional surface area, thus producing more thrust on the power stroke,
while on the recovery stroke the limbs bend and flex, reducing the surface area and the negative
drag. This design is quite different from the thoracic propulsors, which were tapered flagellar
limbs with setose distal articles. But the locomotion is still based on coordinated metachronal
rowing of limbs with a beat cycle that starts at the posterior end and moves anteriorly, creating
an undulating wave of limbs and a continuous flow of water used for generating locomotory, res-
piratory, and feeding currents. Of particular interest, these three largest branchiopods show no
morphological modifications in their swimming limbs compared to smaller branchiopods that

swim at lower Re values, demonstrating the robustness of the paddle design. The major differ-
ences for these three very large Branchinecta species are behavioral and connected to their preda-
tory lifestyle: (1) they feed primarily on other branchiopods (mainly other anostracans), so they
need to swim in more frequent rapid bursts and thus at higher Reynolds numbers, and (2) they are
capable of twisting and turning to pursue and capture prey, displaying an unusual body flexibility
for Crustacea (Boudrias and Pires 2002).
Pedaling with Posterior Pereopods
One family of deep-sea isopods uses a mode of swimming completely different from all other
arthropods, including the swimming insects: they use the last three pairs of modified thoracic
appendages to propel themselves backward. The asellote isopods of the family Munnidopsidae
have modified fifth, sixth, and seventh pereopods that use a modified drag-based propulsion.
When analyzing swimming in Eurycope , Hessler (1993) described how the paddle-shaped
last three pairs of pereopods sweep through the water with extended setae, propelling the
deep-sea isopod backward. The swimming motion is restricted to the most posterior thoracic
limbs, without any assistance from the pleopods or the other pereopods. The propulsive force
is generated by large extrinsic muscle bundles that move the limbs and change the profile of
the body but otherwise do not provide additional streamlining or more effective drag reduc-
tion. The pereopods are modified at the distal end with enlarged, f lattened, paddle-shaped
propodus and dactylus, each fringed by plumose setae. Eurycope are described as reluctant
swimmers by Hessler (1993), but when they do swim, their size and speed lead to moderate
Reynolds numbers.
Other deeper water asellote isopods use their modified pereopods to effectively “walk” in
water at relatively low speed (but still at moderate Re ~ 2000) and their last pair of pereopods
coupled with abdominal flexion to propel themselves more quickly backward (Re ~ 15,000)
(Wilson et al. 1989). In a detailed study using extensive video of swimming in deep-sea isopods,
Marshall and Deibel (1995) described the swimming behavior, kinematics, and basic morphol-
ogy of two species of Munneurycope and Munnopsis. They defined four modes of swimming: for-
ward striding, slow backward pedaling, fast backward pedaling, and escape. The slower modes
of swimming resemble a walking gait and do not really reach high-Reynolds-number swimming
speeds. But the unique way of “walking” in water does lead to extreme modifications of pere-
opods 2–4, which have long, flexible setae concentrated at the distal end, making the equivalent
of an oar. The faster modes of swimming (fast backpedaling and escape) use the last three pairs
of pereopods to produce the necessary thrust and are clear examples of higher-Re swimming.
These pereopods are paddle shaped, with flattened limb segments fringed with long plumose
setae (Fig. 12.2). This morphological design blends a full paddle structure, which can function
like a fin or solid surface, with the more typical crustacean design incorporating plumose setae
either along the full ramus or as a fringe along the edge of a paddle. More thrust is thus pro-
vided on the power stroke due to the larger surface area, but the motion of the recovery stroke is
more complicated, leading to more negative drag and a reduction in propulsive efficiency. These
deep-sea isopods do not have a large body, nor do they move quickly (in most cases), but the
long thoracic limbs, the paddle-shaped last three pairs of pereopods, and the potential to move
quickly backward are all modifications that relate to swimming at higher Reynolds numbers.
In fact, the ability to tuck in the other pereopods and elongate the antennae to establish a more
streamlined shape is the epitome of fast and furious swimming because it leads to reduced form
drag on the body, produces more laminar flow around the whole organism, and results in more
efficient locomotion overall (Boudrias 1992, Tulipani 2005).
Fig. 12.2.
Drawings of isopods observed and recorded on videotape from the submersible Johnson Sea-Link II.
(A) Munneurycope sp. I in characteristic “hanging” or parachuting pose. (B–D) M. longiremis, viewed lat-
erally (B) and dorsally (D) during slow backward pedaling and during fast backward pedaling or escape
(C), during which the long pereopods and antennae are swept behind the animal. Scale bar, 25 mm. From
Marshall and Deibel (1995), with permission from the Company of Biologists, Ltd.
DRAG-BASED SWIMMING: ABDOMINAL PROPUL SORS
Pleopods
The vast majority of crustaceans, either in their larval form or as adults, have functional abdom-
inal swimming appendages, called swimmerets or pleopods. The shape, number, and function
of these abdominal limbs may differ, but some constants in pleopod design are typically con-
tained in general statements or in basic taxonomic descriptions. Pleopods exhibit a multiplicity
of roles by generating currents with major impacts on several key biological functions, such as
respiration, locomotion, feeding, and reproduction. Research on pleopod function and impor-
tance varies greatly, including analysis of their kinematics, their impact on physiology, and even
some sophisticated analyses of the fluid dynamics generated by the metachronal beat pattern.
Yet we still know very little about detailed pleopod morphology, functional design, or phyloge-
netic importance. Even the name pleopod reflects this bias since the Greek pleo can mean either
“more” or “swim.” The role of pleopods in swimming and respiration alone should warrant more
than passing reference and simple descriptions.
Only a handful of papers have analyzed pleopods at a level detailed enough to explain their
role in swimming at moderate to high Reynolds numbers. For nonamphipod malacostracans,
there are only two publications on pleopod musculature. Kils (1981) described swimming in
euphausiids with a combination of morphological analysis of the pleopods and a kinematic
analysis of the motion of the first three pairs of abdominal limbs. Hessler (1985) thoroughly
described pleopod skeletomusculature in Gnathophausia ingens, illustrating the extrin-
sic muscles that provide the propulsive forces of remotion and promotion, and the intrinsic
A B C
CO AP 2 5
4 7
BA 6
AP 1
FU
AP 3 IAM
EN 5 8
EX 7 9
6 10
3
4 12
D
i ii iii iv
Fig. 12.3.
(A) Base of a thoracic limb of Gnathophausia ingens in anterior and posterior views and showing extrin-
sic musculature. Abbreviations: AP 1–3, apodemes for insertion of muscles 1–3; BA, basis; CO, coxa; EN,
endopod; EX, exopod; FU, fulcrum; IAM, intrinsic arthrodial membrane; 2, 3, first layer of extrinsic mus-
cles. (B) Musculature of thoracic exopodal peduncle of G. ingens from right side: ventral view showing lay-
ering of muscles 4–8. (C) Musculature of thoracic exopodal flagellum from left side: dorsal view showing
layering of muscles 5–12. (D) Diagram of exopodal flagellum showing orientation of the setae during the
power stroke (i, ii) and the recovery stroke (iii, iv). Multiple views show different angles of motion with
setae drawn to scale. Composite figure modified from Hessler (1985), with permission from the Royal
Society of Edinburgh.
muscles that control the spreading of the rami and the flexion of the rami during the recovery
stroke (Fig. 12.3). Hessler (1985) also provided some of the earliest and complete kinematic
analyses of pleopod metachronal beat in larger crustaceans several centimeters in length.
Alexander (1988) described pleopod beat and force production in isopods that use the full
paddle-shaped pleopods to generate propulsive forces. Cowles and Childress (1988) studied
the swimming speed and oxygen consumption in Gnathophausia and showed that swimming
efficiency increased with speed. Cowles (1994, 2001) followed with a more detailed kinematic
analysis of pleopod-driven locomotion in sergestid shrimp. The pattern is essentially the same
for all these organisms: a 3–2–1 metachronal beat pattern for the pleopods, adduction of uro-
pods either close to the wall of the abdomen or tucked in a concave space below the telson,
retraction and/or adduction of pereopods, and positioning of the anterior limbs and antennae
to create a streamlined shape. The pleopods are biramous with an almost rectangular pedun-
cle and tapered, annulated, highly setose rami; they extend as wide paddles during the power
stroke and collapse and overlap with highly reduced area on the recovery stroke. This multi-
limbed rowing propels the animal forward at velocities on the order of 5–10 cm/s, producing an
Re for the whole body on the order of several thousands (5,000–30,000). The pleopods them-
selves operate at Re values of several hundreds to several thousands during the power stroke,
as determined by the surface area of the paddle and the velocity of the sweep. But despite these
common morphological and kinematic analyses, there are few systematic studies of pleopods
and fewer still that go beyond morphological descriptions. The most complete analyses are
found in the amphipods.
Amphipod Swimming
Amphipods are ubiquitous in virtually every aquatic habitat and frequently dominate the
macrofauna both in shallow coastal waters and in the deep sea. They are among the most
effective scavengers of food falls and are known to travel long distances to reach their food
(Sainte-Marie and Hargrave 1987, Premke et al. 2006). Many are excellent swimmers, ranging
in size from a few millimeters to giant deep-sea species, such as Eurythenes gryllus (mature
adults of 15 cm) and Alicella gigantea (captured specimens of ~30 cm). Most amphipod swim-
mers exhibit a streamlined body (Boudrias 1991). Propulsion is achieved by three pairs of
abdominal pleopods and directional control by a combination of fourth and fifth pereopods
and three pairs of uropods. With pleopods being the key propulsors for amphipods (and many
other moderately sized crustaceans), it is important to understand their design and function
(e.g., Boudrias 1992, 2002).
In my doctoral thesis studying swimming in the deep-sea lysianassid Eurythenes gryl-
lus (Boudrias 1992), I described in detail the functional morphology, kinematics, and f luid
dynamics of pleopods in this highly efficient swimmer and deep-sea scavenger. The genesis of
that work was strongly inf luenced by the paucity of research on pleopods, especially in amphi-
pods. Prior to 1992, research on pleopods in amphipods consisted of (1) studies of pleopod
beat frequency as a measure of respiratory rates (Waterman 1961, Yayanos 1978, 1981, George
1979), (2) a few morphological drawings in some major amphipod taxonomic works (Sars 1895,
Bousfield 1973), and (3) four papers on pleopod musculature and biomechanics. The four
musculature papers span almost 100 years, from Stebbing’s (1888) illustration of basic intrin-
sic musculature to Brusca’s (1981) simple account of extrinsic and intrinsic pleopodal muscles
in hyperiids and the companion papers by Vogel (1985, 1986) with data on the biomechanics
and kinematics of talitrids and drawings of musculature and scanning electron microscopy
of joints. None of these works defined the functional arrangement of joints and muscles or
examined in detail the ancillary skeletal structures or the interaction of f luid dynamics and
limb construction.
Boudrias (1992, 2002) describes the standard pleopod design, which consists of (1) two sets
of extrinsic muscles for promotion and remotion, respectively; (2) an intrinsic flexor for recov-
ery stroke movement; (3) intrinsic support muscles that affect the shape of the peduncle; (4)
two intrinsic muscles, a long straplike one (M11) and a small diagonally inserting fan-shaped
one (M12), responsible for abduction of the exopod; (5) a large complex of muscles attaching
along an apodeme acting as a powerful adductor for the exopod (M13); and (6) a long flexor
running the length of each ramus that acts to curl the ramus on the recovery stroke and possibly
provide stiffening on the power stroke (Fig. 12.4). Some species add additional structures to
this plan, for example, exopodal hooks holding the two peduncles together on the power stroke
(De Broyer and Klages 1991, Boudrias 2002), long setae on the anterior and posterior face of
the peduncles that flex differentially depending on force of the pleopod beat (personal observa-
tion), or differences in shape of the peduncle (personal observation). The functional design of
amphipod pleopods represents the typical model of abdominal propulsors. The kinematics of
drag-based propulsion (metachronal beat pattern, and a rowing motion) in crustaceans can lead
A Dorsal B
Intracuticular i ii
ridges
Peduncle
M7
M5
M8 Anterior Posterior
M4
Anterior Posterior
Exopodal
Large hook
plate
Exopod Endopod Exopod Endopod
M9
Ventral
C D
i ii
i ii
M10
M11 Peduncle
Peduncle M13
M12
M10
M12 Exopod Endopod
Coupling
hooks
Exopod Endopod
Fig. 12.4.
(A) Medial view of extrinsic musculature showing multiple layers of promotors and remotors and the
ridges on the cuticle in Eurythenes gryllus. Top muscles layer are removed to reveal deeper layers and ridges.
(B) Intrinsic peduncle support muscles with pleopod extended in power stroke: lateral view (i) and dorsal
view (ii) to illustrate the dense packing of muscles in the peduncle on all sides. (C) Exopodal and endopo-
dal control muscles M10–13: muscles that control adduction and abduction with origins and insertion (i),
and details of insertion sites for ramal control muscles and origin of flagellar flexor (ii). (D) Pleopod pair:
anterior view showing the overlap of setae and width of propulsive setal fan on power stroke (i) and lateral
view showing collapsed setal fan, flexed and stacked rami, and a contracted peduncle on recovery stroke
(ii). Composite figure modified from Boudrias (1992).
to moderate- to high-Reynolds-number swimming for larger crustaceans and/or fast swimmers

such as predators and scavengers.
Though drag-based swimming is most common, there are two major exceptions that are
great examples of high-Reynolds-number swimming. The first exception is limited primarily to
one family of brachyuran crabs, while the other specialty mode is critical to survival of several
crustaceans, though it can be used for some distance locomotion. The following two sections
detail these two fast-swimming modes: lift-based swimming in crabs and escape locomotion in
a diverse group of small to large malacostracans.
LIF T-BASED SWIMMING: SCULLING WITH THORACIC LIMBS IN CRABS
One group of Crustaceans has taken the modification of thoracic limbs in a completely dif-
ferent direction. The portunid crabs, the family of brachyurans that are commonly defined as
swimming crabs, have the body size and the swimming speed to move at high Reynolds num-
bers, but their mode of propulsion is significantly different from that of most other crustaceans.
Rather than row, paddle, or pedal through the water, they move their propulsive limbs, the
highly modified fifth pereopods, in a figure-8 pattern, creating a lift-based mode of propulsion.
Furthermore, the crabs swim sideways, so the body design must adjust to this direction of
locomotion. Hartnoll (1971) compared all crab families from a morphological perspective and
clearly demonstrated the need for flattened and setose limbs to generate swimming thrust. The
Portunidae family has the most complete modifications for swimming, with flattened, paddle-
shaped fifth pereopods fringed with plumose setae and a body design that allows for streamlin-
ing when swimming sideways. In a more detailed analysis, Spirito (1972) described swimming
in the blue crab Callinectes sapidus, relying mainly on morphological characteristics and basic
video footage of their sideways swimming. Several key components allow blue crabs to swim at
speeds of 0.24–0.77 m/sec (Re > 40,000), taking hydrodynamic advantage of a very streamlined
body and clean lines of flow. The sharp spines on either side and a slightly elliptical carapace
provide the basis of a streamlined shape; the folding of the chelipeds along the spines and in
tight formation with the front edge of the carapace leads to a rounded anterior edge and an
elongated posterior edge (trailing cheliped); the rowing of the second, third, and fourth pere-
opods at the leading edge (adding to the rounded shape needed at the front of the streamline)
combined with straightening those three thoracic limbs on the trailing edge produce the termi-
nal point for the streamline; and the sculling of the fifth pereopods through the water generates
the propulsive thrust. The most comprehensive analysis of lift-based swimming in portunids
was done by Plotnick (1985), who quantified the kinematics (details of motion) and the dynam-
ics (forces on limb and body) of swimming in Callinectes sapidus using more of an engineer-
ing approach (Fig. 12.5). By using high-speed film, which permitted a more detailed analysis
of locomotion, he determined swimming speeds closer to 1.0 m/sec and Reynolds numbers
B
Body
Animal
Anterior
Coxa
Carpus
Merus Basi-ischium
Leg
Dorsal
Propodus
Leg
Ventral
Dactylus
Fig. 12.5.
(A) Drawing of swimming position of Callinectes sapidus showing the streamlining when moving in the
lateral direction, extension of contralateral limbs, and position of the fifth pereopods. U = velocity. (B)
Close-up of fifth pereopod showing flattened paddle and potential for sculling motion. From Plotnick
(1985), with permission from the Royal Society of Edinburgh.
ranging from 63,000 to 190,000 for the body and around 18,000 for the fifth pereopod paddle.
Though this analysis did not fundamentally change the earlier descriptions, it provided a more
quantitative perspective and allowed for comparisons with other crustaceans and with other
moderate to high Re swimmers such as fish. Plotnick even used the combination of a morpho-
logical approach and a dynamic analysis of thrust and drag to propose how large animals, such
as the fossil eurypterids, could swim. His predictions were that eurypterids used their enlarged
chelipeds to create propulsive thrust, keeping their body streamlined with a rounded anterior
end and pointed telson directing the flow posteriorly.
ESCAPE LOCOMOTION IN CRUSTACEANS: JET PROPUL SION

AND RAPID ACCELERATION
The fastest mode of locomotion in Crustacea and the one that achieves the highest Reynolds
numbers, though almost always for a very short time, is typically defined as escape locomotion.
Crustaceans as a whole, but especially advanced malacostracans, have evolved a stereotypical way
to escape from predators: they jump backward (posterior end as leading edge) or sideways to get
away from an oncoming predator. The morphological details (the design of directional limbs and
the grooves, ridges and setation pattern of the body) vary among groups, and several different per-
spectives could be used to review escape locomotion (evolutionary, neurological, morphological,
behavioral, hydrodynamic). In the following section I summarize the similarity of the motion across
all crustaceans that use it, describe the underlying functional morphology, and then briefly review
the diversity of groups using escape locomotion based on full descriptions of their kinematics.
Basics of Crustacean Jet Propulsion
The initial description of crustacean escape locomotion can be found in an analysis of the
mechanics of escape response in crayfish (Webb 1979). Essentially, when a moderate to large
crustacean engages in escape locomotion, several things happen: (1) the animal will rapidly flex
the abdomen and move it anteriorly very rapidly; (2) the tail fan, typically composed of one
pair of uropods and the telson (frequently flattened and setose), will expand and create a large
paddle/surface area to generate thrust; (3) the thoracic limbs will be tucked into the body, in
some cases tightly stacked against each other and tightly held against the carapace with a com-
bination of concave and convex faces that fit into each other; (4) the anterior limbs (antennae,
antennules, and/or chelipeds) will be extended to create the “tail” end of the streamlined shape
and become the directional controllers; and (5) the organism will flex the abdomen + tail fan
multiple times, squeezing water out of the space between the tail fan and the abdomen, creating
a jet with each contraction and propelling the animal backward (in some cases sideways) very
rapidly. This series of muscular and behavioral actions is then repeated a few to several times,
propelling the organism very rapidly away from its previous location and usually away from a
predator (Fig. 12.6).
Subsequent research on escape locomotion has added details on the morphology of the
propulsors or directional limbs, on the neuronal control of tail-f lips, on the kinematics of
tail-f lips and even on the hydrodynamic forces produced by the propulsive limbs or encoun-
tered by the organism. Further studies in crayfish by Cooke and MacMillan (1985) recognized
three distinct classes (linear, pitching, and twisting f lips) of tail-f lips with more fine-tuned
neuronal control than the typical giant axon power f lip for rapid escape. Some of the behav-
ioral analysis of escape locomotion in scyllarid lobsters by Jacklyn and Ritz (1986) showed
complex behaviors connected to fine-tuned directional control by the f lat second antennae,
allowing the organisms to turn rapidly or even perform a barrel roll or a loop. Newland et al.
B
i ii C
1 cm
1 mm
iii iv D
1 mm
1 cm
Fig. 12.6.
(A) Streamlined position of Pleuroncodes planipes in full escape locomotion position showing tight stack-
ing of pereopods and extension of chelipeds. (B) Sequential positioning of P. planipes during the propulsive
sequence of tail fan with extension and contraction (ventral and lateral views): i, the tail fan is completely
closed at the end of the power stroke; ii, the tail fan begins its extension; iii, the tail fan reaches maximum
extension away from the body, creating maximum drag; iv, the tail fan begins the power stroke and starts
moving back toward the ventral side of the abdomen, which will return it to the first position (i). (C) Tail
fan (uropods and telson) in full extension just prior to propulsive thrust, with outlined area showing extent
of setal fan. (D) Close-up of chelipeds showing grooves and ridges that are used to control flow at poste-
rior end (when organism is swimming) to affect direction of movement. Composite figure from Tulipani
(2005) with original drawings by Vanessa Ruiz.
(1988) showed that Nephrops norvegicus respond differently based on the initiation of the stim-
uli, with a greater lift above the bottom when touched on the abdomen and the escape locomo-
tion controlled by giant neuronal fibers. Daniel and Meyhöfer (1989) employed sophisticated
kinematic and hydrodynamic analysis in caridean shrimp using theoretical analysis to sug-
gest that as either the relative length of the propulsive appendage increases or the absolute
body size increases, rotational motions become disproportionately greater than translational
motions and escape performance decays. Spanier et al. (1991) investigated the Mediterranean
slipper lobster Scyllarides latus, which uses escape locomotion for a short duration combining
rapid acceleration with initial tail-f lip with powerless gliding to avoid predation. Newland
et al. (1992), in a more detailed analysis of Nephrops norvegicus, showed that stimulus laterality
inf luences steering and rigidity of the body, and the duration of jet swimming is determined
by a combination of neuronal and metabolic factors. Kinematic analysis for the brown shrimp
Crangon crangon (Arnott et al. 1998) and in spiny lobsters (Panulirus interruptus) (Nauen and
Shadwick 1999, 2001) determined that maximum acceleration of the body of free-swimming
animals occurs when the tail is positioned approximately normal to the body, and acceleration
declines steadily to negative values as the tail continues to close. Nauen and Shadwick (2001)
also showed that full f lexion of the tail to the body probably increases the gliding distance
by reducing drag and possibly by enhancing f luid circulation around the body. Heitler et al.
(2000) showed that in the stomatopod Squilla mantis the maximal response is sufficiently vig-
orous to pull the animal into a tight vertical loop away from the stimulus but with less overall
power than the full caridoid escape response. In squat lobsters Pleuroncodes planipes, Tulipani
(2005) showed that when the red crabs are in their pelagic phase, they can use their thoraco-
pods to create a parachute to slow sinking, their tail fan for rapid, powerful propulsion, and
their chelipeds for directional control when swimming over distance and to maintain vertical
position in the water column. Olesen et al. (2006) studied the thermosbaenacean Tethysbaena
argentarii , and the behavioral analysis showed two successive tail-f lips: first a ventral move-
ment, which brings the tail region close to the thorax, and then a dorsal motion, which causes
the thorax/head region to f lip backward because of greater propulsive drag in the tail fan.
This type of escape reaction in T. argentarii is different from the “jet stream” type of escape
reaction seen in various shrimps, euphausiids, and mysids, but it bears some resemblance to
that seen in stomatopods. Finally, an analysis of pleopod swimming and tail-f lipping escape
in the kuruma shrimp, Marsupenaeus japonicus, found that exercise to fatigue led to severe loss
of glycogen concentrations in hepatopancreas and muscle, whereas the plasma lactate concen-
tration increased significantly (Yu et al. 2009).
Depending on whether the animal is benthic before take-off or already in the water column,
the initiation of the escape locomotion may be different, and the order of the motions may
change, but escape locomotion requires modification in (1) abdominal musculature (complex,
multidirectional, thick), (2) tail fan (flat, setose, capable of fanning out to create a wide surface
area for thrust generation), (3) thoracic limbs and carapace (limb design to reduce drag and
help create a streamlined shape, e.g., bumps, tubercules, and/or grooves to channel flow from
posterior [leading edge] to anterior of body [trailing edge]), and (4) modifications in most
anterior limbs (flat antennules used as ailerons, grooved and flattened chelipeds to channel
flow and control direction). The abdominal musculature necessary for escape locomotion and
its associated jet propulsion is critical and has been used as an important evolutionary char-
acter (Hessler 1983) to determine which malacostracans are capable of a full caridoid escape
motion. The musculature includes multiple layers and key oblique patterns leading to an
abdomen almost completely filled with striated muscles capable of short, repeated, powerful
contractions. Tail fan modifications repeat one of the common patterns seen in all previous
propulsors: they are flat, paddle shaped, fringed with plumose setae, and capable of expansion
to produce a wide surface area for maximum thrust generation and contraction/folding (in
some cases with concave spaces to fold in and away) to reduce area when not in propulsion
mode. Detailed morphological analysis of the body and thoracic limbs by Tulipani (2005) in
Pleuroncodes planipes showed grooves, bumps, and body setae arranged to direct flow around
the body that enhance streamlining. In fact, the pereopods had a combination of concave and
convex faces that allowed them to fit into each other and to be held tightly against the body to
produce a well-defined streamlined shape (Fig. 12.6). Modifications of the most anterior limbs
can best be seen in scyllarids (Jacklyn and Ritz 1986), where the flattened second antennae act
as ailerons and not only control direction of flow at the trailing edge of the streamline shape
but also permit such complex escape maneuvers as loops and body rolls. Similarly, Tulipani
(2005) and Tulipani and Boudrias (2006) showed that squat lobsters have chelipeds that are
constructed to direct flow anteriorly, control flow direction by bending or twisting, and direct
the jet to control vertical motion.
In all cases, the escaping crustaceans generate very large accelerations, very fast velocities
(0.3–1.5 m/sec), and moderate to large Reynolds numbers (typically from 10 4 to almost 106). This
is a mode of locomotion that typically does not last long and can be produced only occasion-
ally but that propels crustaceans at velocities and accelerations that rival fast-swimming fish
and squids. This mode of fast and furious swimming is best understood for the larger malacos-
tracans (lobsters, crayfish, shrimps) but has been observed in other crustaceans without any
detailed analysis of the morphology, kinematics, or dynamics.
FUTURE CHALLENGES
This chapter has attempted to review all major examples of crustaceans swimming at high
Reynolds numbers by defining the three major modes of locomotion used by moderate to large
crustaceans swimming several centimeters to a few meters per second: (1) drag-based swim-
ming with setose flagellar or paddle-shaped limbs, (2) lift-based sculling in portunid crabs, and
(3) jet propulsion in a wide variety of malacostracans. Despite the inclusion of research on mor-
phology of propulsive limbs, kinematics of multiple appendage motion, and even fluid dynamic
forces on limbs and bodies, several challenges still need to be addressed for a complete view of
crustacean locomotion.
The first major challenge is the need for a truly systematic analysis of locomotion, includ-
ing functional morphology of swimming and directional limbs, detailed descriptions of body
design, and determination of the fluid dynamics of swimming for most Crustacea. Much of
the existing literature describes swimming appendages almost as an afterthought and often
for reasons other than a comprehensive analysis of locomotion. This is particularly true for
pleopods, which are often barely mentioned in taxonomic descriptions and are rarely studied
in enough detail (musculature, shape of peduncle, special features, pattern of setation, forces
produced on power and recovery stroke) to provide the necessary descriptive and quantitative
perspectives for a full analysis of swimming. Thus, a systematic analysis of pleopod functional
morphology and attention to morphological details, such as setation pattern of the rami and
peduncle, shape and musculature of the peduncle, and ancillary characters such as hooks and
spines, could lead to pleopods being used as important taxonomic characters in comprehensive
phylogenetic analyses of classes, families and orders, could provide descriptive data to under-
stand more about swimming appendages, and could allow for quantitative comparisons of the
hydrodynamic forces related to swimming at high Reynolds numbers.
The second major challenge is related more to body design than to propulsive appendages.
Crustaceans have bodies covered in ornamentation and have arrangements of appendages that
give them an ungainly and unsightly appearance. However, as the dominant taxon in aquatic
realms and as both key predators (both primary and secondary consumers) and key prey, they
are definitely highly effective swimmers. Very little analysis has been done on the body design
modifications that allow crustaceans to go from wild shapes with limbs at all angles or even
high drag shapes like parachutes (see Tulipani 2005) to tightly compact, streamlined shapes
capable of gliding through the water generating very low values of profile and induced drag. The
functional morphology of the body, using observations and scanning electron microscopy, the
specific details of appendage design (spines, setae, shape of the segments, design of the joints),
and the calculation of dynamic forces on the body in nonswimming, sustained swimming, and
acceleration poses (escape locomotion), needs to be studied for the most effective swimmers
first and then systematically for groups (classes, families, orders, genera) that are defined as
frequent and important swimmers.
Finally, systematic analysis of swimming, including functional morphology, kinemat-
ics, and fluid dynamics, needs to be integrated with studies of behavior, feeding modifica-
tions, physiology of locomotion, and even analysis of nervous system control to provide a truly
comprehensive analysis of swimming. We can almost arrive at this complete picture for a few
groups (portunid crabs, lobsters, shrimps, some amphipods) but only by combining disparate
studies with individual objectives. Much of the analysis of swimming, especially for crustaceans
swimming at moderate to high Reynolds numbers, is a few to many years old, and an integrated
view combining classical functional morphology, innovative engineering approaches, and
multiple objectives (behavior, morphology, phylogenetics) will lead to a more complete picture
of crustacean swimming.
REFERENCES
Alexander, D.E. 1988. Kinematics of swimming in two species of Idotea (Isopoda: Valvifera). Journal of
Arnott, S.A., D.M. Neil, and A.D. Ansell. 1998. Tail-flip mechanism and size-dependent kinemat-
ics of escape swimming in the brown shrimp Crangon crangon. Journal of Experimental Biology
201:1771–1784.
Boudrias, M.A. 1991. Methods for the study of amphipod swimming: Behavior, morphology, and fluid
dynamics. Hydrobiologia 223:11–25.
Boudrias, M.A. 1992. The biomechanics, kinematics, and fluid dynamics of swimming in the deep-sea
lysianassid amphipod Eurythenes gryllus (Lichtenstein). PhD dissertation, Scripps Institution of
Oceanography, University of California, San Diego.
Boudrias, M.A. 2002. Are pleopods just “more legs”? The functional morphology of swimming limbs in
Eurythenes gryllus (Amphipoda). Journal of Crustacean Biology 22:581–594.
Boudrias, M.A., and J.A. Pires. 2002. Unusual sensory setae on the antennae and cercopods of the rapto-
rial Branchinecta gigas (Branchiopoda: Anostraca). Hydrobiologia 486: 19 –27.
Bousfield, E.L. 1973. Shallow-water gammaridean Amphipoda of New England. Cornell University Press,
London.
Brusca, G.J. 1981. On the anatomy of Cystisoma (Amphipoda: Hyperiidae). Journal of Crustacean Biology
1:358 –375.
Cooke, I.R.C., and D.L. MacMillan. 1985 . Further studies of crayfish escape behaviour I. The role of the
appendages and the stereotyped nature of non-giant escape swimming. Journal of Experimental
Biology 118:351–365.
Cowles, D.L. 1994 . Swimming dynamics of the mesopelagic vertically migrating penaeid shrimp Sergestes
similis: Modes and speeds of swimming. Journal of Crustacean Biology 14:247–257.
Cowles, D.L. 2001. Swimming speed and metabolic rate during routine swimming and simulated diel
vertical migration of Sergestes similis in the laboratory. Pacific Science 55:215–226.
Cowles, D.L., and J.J. Childress. 1988. Swimming speed and oxygen consumption in the bathypelagic
mysid Gnathophausia ingens. Biological Bulletin 175:111–121.
Daniel, T.L., and E. Meyhöfer, E. 1989. Size limits in escape locomotion of caridean shrimp. Journal of
De Broyer, C., and M. Klages. 1991. A new Epimeria (Crustacea: Amphipoda, Paramphithoidae) from the
Weddell Sea. Antarctic Science 3:159 –166.
Ford, M.D., M.J. Schuegraf, M.S. Elkink , and E.M. DeMont. 2005 . A comparison of swimming struc-
tures and kinematics in three species of crustacean larvae. Marine and Freshwater Behaviour and
Physiology 38:79 –94.
George, R.Y. 1979. What adaptive strategies promote immigration and speciation in deep-sea environ-
ments? Sarsia 64:61–65.
Hartnoll, R.G. 1971. The occurrence, methods and significance of swimming in Brachyura. Animal
Heitler, W.J., K. Fraser, and E.A. Ferrero. 2000. Escape behaviour in the stomatopod crustacean
Squilla mantis, and the evolution of the caridoid escape reaction. Journal of Experimental Biology
203:183–192.
Hessler, R.R. 1983. A defense of the caridoid facies: Wherein the early evolution of the Eumalacostraca is
discussed. Pages 145–164 in F.R. Schram, editor. Crustacean phylogeny. Crustacean Issues, Vol. 1.
Balkema, Rotterdam.
Hessler, R.R. 1985 . Swimming in Crustacea. Transactions of the Royal Society of Edinburgh 76:115–122.
Hessler, R.R. 1993. Swimming morphology in Eurycope cornuta . Journal of Crustacean Biology
13:667–674.
Jacklyn, P.M., and D.A. Ritz. 1986. Hydrodynamics of swimming in scyllarid lobsters. Journal of
Kils, U. 1981. The swimming behavior, swimming performance, and energy balance of Antarctic krill
Euphausia superba. SCAR Biomass Scientific Series No. 3. Texas A&M University, College Station .
Laverack , M.S., D.M. Neil, and R.M. Robertson. 1977. Metachronal exopodite beating in the mysid
Praunus flexuosus: A quantitative analysis. Proceedings of the Royal Society of London Series B
198:139 –154.
Marshall, N.J., and C. Deibel. 1995 . “Deep-sea spiders” that walk through the water. Journal of
Mehrtens, F., M. Stolpmann, F. Buchholz, W. Hagen, and R. Saborowski. 2005 . Locomotory activity and
exploration behaviour of juvenile European lobsters (Homarus gammarus) in the laboratory. Marine
Nauen, J.C., and R.E. Shadwick. 1999. The scaling of acceleratory aquatic performance: Body size and
tail-flip performance of the California spiny lobster Panulirus interruptus. Journal of Experimental
Biology 202:3181–3193.
Nauen, J.C., and R.E. Shadwick. 2001. The dynamics and scaling of force production during tail-flip
escape response of the California spiny lobster Panulirus interruptus. Journal of Experimental
Biology 204:1817–1830.
Neil, D.M., D.L. MacMillan, R.M. Robertson, and M.S. Laverack. 1976. The structure and function of
thoracic exopodites in the larvae of the lobster Homarus gammarus (L.). Philosophical Transactions
of the Royal Society of London Series B 274:53–68.
Newland, P.L., C.J. Chapman, and D.M. Neil. 1988. Swimming performance and endurance of the
Norway lobster Nephrops norvegicus. Marine Biology 98:345–350.
Newland, P.L., D.M. Neil, and C.J. Chapman. 1992. Escape swimming in the Norway lobster. Journal of
Olesen, J., S.T. Parnas, and J.F. Petersen 2006. Tail flip and escape response of Tethysbaena argentarii
(Malacostraca: Thermosbaenacea). Journal of Crustacean Biology 26:429 –432.
Plotnick , R.E. 1985 . Lift based mechanisms for swimming in eurypterids and portunid crabs.
Transactions of the Royal Society of Edinburgh 76:325–337.
Premke, K., M. Klages, and W.E. Arntz. 2006. Aggregations of arctic deep-sea scavengers at large food
falls: Temporal distribution, consumption rates and population structure. Marine Ecology Progress
Series 325:121–135.
Sainte-Marie, B., and B.T. Hargrave. 1987. Estimation of scavenger abundance and distance of attraction
to bait. Marine Biolology 94:431–443.
Sars, G.O. 1895 . An account of the Crustacea of Norway, Vol. 1, Amphipoda. Cammermeyer, Christiania,
Norway.
Spanier, E., D. Weihs, and G. Almog-Shtayer. 1991. Swimming of the Mediterranean slipper lobster.
Journal of Experimental Marine Biology and Ecology 145:15–31.
Spirito, C.P. 1972. An analysis of swimming behaviour in the portunid crab Callinectes sapidus. Marine
Stebbing , T.R.R. 1888. Report of the Amphipoda collected by the H.M.S. Challenger during the years
1873–1876. Report Voyages Challenger 1873–1876 (Zoology) 29:1–1737.
Tulipani, D. 2005 . The functional morphology and fluid dynamics of swimming in the pelagic red crab,
Pleuroncodes planipes. MS thesis, University of San Diego.
Tulipani, D.C., and M.A. Boudrias. 2006. Behaviors of the pelagic red crab Pleuroncodes planipes
(Decapoda: Anomura: Galatheidae) observed in captivity. Pages 67–79 in A. Asakura, editor.
Biology of the Anomura II. Proceedings of the Symposium organized by Rafael Lemaitre and
Christopher Tudge, Sixth International Crustacean Congress, Glasgow, Scotland. Crustacean

Research, Special Number 6. Carcinological Society of Japan, Tokyo.
Vogel, F. 1985 . Das Schwimmen der Talitridae (Crustacea, Amphipoda): Funktionsmorphologie,
Phä nomenologie und Energetik. Helgolä nder Meeresuntersuchungen 39:303–339.
Vogel, F. 1986. Die abdominale muskulatur von Orchestia cavimana Heller 1865 (Amphipoda: Talitridae).
Waterman, T.H., editor. 1961. The physiology of Crustacea. Vols. 1 and 2. Academic Press, New York.
Webb, P.W. 1979. Mechanics of escape responses in crayfish (Orconectes virilis). Journal of Experimental
Biology 79:245–263.
Wilson, G., M. Boudrias, R. Miller, and G.R. Harbison. 1989. A unique form of swimming in the deep-sea
isopod crustacean genus Munneurycope: Walking [abstract]. American Zoologist 29:289.
Yayanos, A.A. 1978. Recovery and maintenance of live amphipods at a pressure of 580 bars from the ocean
depth of 5700 m. Science 200:1056 –1059.
Yayanos, A.A. 1981. Reversible inactivation of deep-sea amphipods (Paralicella capresca) by a decom-
pression from 601 bars to atmospheric pressure. Comparative Biochemistry and Physiology
69A:563–565.
Yu, X., X. Zhang , P. Zhang , and C. Yu. 2009. Critical swimming speed, tail-flip speed and physiological
response to exercise fatigue in kuruma shrimp, Marsupenaeus japonicus. Comparative Biochemistry
and Physiology A 153:120 –124.
13
ADAPTIVE MODIFICATION OF APPENDAGES FOR GROOMING
(CLEANING, ANTIFOULING) AND REPRODUCTION IN THE
CRUSTACEA
Raymond T. Bauer
Abstract
Appendages used primarily for feeding and locomotion have become secondarily modified
for grooming and reproductive purposes in many crustaceans. Grooming (preening, clean-
ing) of the body and its appendages has evolved because, particularly in marine habitats, the
settling stages of microbial organisms, algae, and sessile invertebrates use the hard, nonliving
exoskeleton of crustaceans as a substratum. These epibionts (fouling organisms), as well as sus-
pended sediment and other particulate matter, may cover and impair sensory and respiratory
surfaces, as well as impede limb movement and swimming efficiency. Crustaceans use special-
ized brushes and combs composed of setae with a complex microstructure for scraping surfaces
clean. Decapod crustaceans have the best-described cleaning behavior, with gill cleaning by a
variety of mechanisms necessitated by enclosure of gills in a branchial chamber. Cleaning of
olfactory antennules, general body surfaces, and incubated embryos by the third maxillipeds,
specialized chelae in caridean shrimps and anomuran crabs, and other pereopods is common.
Other crustaceans, particularly stomatopods, some peracarids, and ostracods, groom fre-
quently. Ablation experiments have demonstrated that deleterious fouling does occur in the
absence of grooming. Some crustaceans avoid algal fouling by frequent molting, burrowing in
abrasive sediments, or nocturnal behavior.
In many species, appendages have also experienced specializations for reproductive purposes.
The immobile sperm of crustaceans must be actively transferred by the male in crustaceans, and
a variety of appendages have become modified for this task. In various malacostracans, the first
two pleopods are often modified as gonopods to either inject or deposit sperm or spermato-
phores in or on the female. In other crustaceans, gonopores are elaborated into papillae (penes)
that insert directly into female gonopores, or other various appendages may be modified for
337
sperm transfer. Many male crustaceans use appendages equipped with hooks or spines to attach
to females during copulation. Some very elaborate reproductive appendages might serve as
courtship rather than sperm transfer devices. In many taxa, female appendages may be modified
to form brood chambers to incubate embryos. The actual mechanics of reproductive append-
ages in crustaceans are still poorly known and remain a fertile topic for study.
INTRODUCTION
In most animals, appendages molded by selection for one basic function are often secondar-
ily modified, either completely or partially, for another adaptive role. In crustaceans, two such
functions are grooming (preening, cleaning) and reproduction (mating, insemination, sperm
storage, incubation of embryos). Appendages or structures evolved primarily for feeding or
locomotion are often later adapted for grooming or reproduction. This chapter provides an
overview of grooming and sexual appendages in crustaceans, with emphasis on major morpho-
logical and phylogenetic trends in these structures. The consensus classification of Martin and
Davis (2001) is used here.
GROOMING
A major selection pressure on crustaceans, especially those in marine habitats, is fouling of body
and appendage surfaces (Fig. 13.1). One major source of fouling is from particulate matter (sedi-
ment and detritus) suspended in the water column or on the substratum over which benthic
organisms crawl or burrow. The other major source is the growth of other living organisms
(epibionts), both microbial (e.g., bacteria, fungi, sessile protists) and macroscopic (e.g., bryo-
zoans, hydroids, barnacles, ectoparasites), on the organism’s surface. Suitable hard substrata for
the settlement of both microbial and macroscopic sessile organisms are often in short supply
in aquatic habitats, especially in the sea. Crustaceans are encased in a hard, nonliving, chiti-
nous/calcareous exoskeleton with cuticular outgrowths (setae) that can be ideal sites for the
accumulation of particulate matter and fouling organisms. Particles and epibionts may cover
and foul respiratory surfaces (impeding gas exchange), sensory structures (preventing receptor
contact with stimuli), and appendages and setae (hindering such activities as locomotion and
feeding). Similar to fouling by organisms on a ship’s hull, fouling on the cuticle of swimming
crustaceans increases drag and decreases swimming efficiency. Although all crustaceans have
a newly secreted, clean exoskeleton upon molting, significant deleterious fouling can and does
occur between molts. This fouling must be removed, and most crustaceans and other arthropods
have evolved behaviors for this function (Bauer 1975, 1981, 1989). Appendages and other struc-
tures used in grooming bear brushes and combs composed of complex setae (Fig. 13.2). In the
many crustaceans that incubate embryos, grooming and cleaning of embryos by the female are
important for successful development and hatching.
Decapoda
Sensory Structures
Appendages with high concentrations of sensory structures are frequently and thoroughly
cleaned by decapod crustaceans (Bauer 1989). Foremost among these are the antennules (first
antennae = A1), which bear thin-walled olfactory setae or sensilla, the aesthetascs, on their
outer (lateral) flagella (Hallberg and Skog 2011). Frequent A1 preening by the third maxillipeds
Modification of Appendages for Grooming and Reproduction 339
Selective Pressures:
Particulate Settlement of
fouling fouling organisms
Impedes gas, ion Fouling of Hinders appendage,

exchange via gills crustacean setal function
Reduces sensory exoskeleton
Increases drag
perception during swimming
Adaptive solutions:
Molting Grooming
Avoidance
Burrowing
behaviors
Cuticular
properties ?
Fig. 13.1.
Summary of fouling pressures and adaptive solutions in Crustacea.
(M3), primarily a food-handling appendage, is ubiquitous in decapods. Typically, an A1 is

brought to the midline in front of the body and lowered between the outstretched M3 pair,
which clamp on it with the setal grooming combs. As the A1 is raised, the M3 are lowered so
that the A1 is drawn through the setal combs (Fig. 13.3A,B). Each M3 bears, on one or more of its
distal articles, dense rows or combs (Fig. 13.3C) of medially placed, complex specialized setae
that scrape the asthetascs and other A1 surfaces. The A1 may also be grasped and scrubbed
with a rubbing action between the M3 setal combs. Each A1 cleaning seta on the M3 usually
bears at least a double row of toothed branches (setules) and often bears spiny denticles or
scales as well. A bout of A1 grooming is usually followed by a bout of “autogrooming” by the M3
(Fig. 13.3D). In autogrooming, limbs clean each other by rubbing against one another several
times. The setal tips are oriented distally, resulting in movement of debris toward the limb tip,
where it drops off.
Amputation experiments on various decapods have tested the hypothesis that A1 preening
cleans the antennules and that a lack of grooming is deleterious to the animal. Bauer (1975, 1977)
performed M3 ablation experiments on two caridean shrimps. The aesthetascs of the shrimp
Pandalus danae are rather sparsely distributed on the A1 outer flagella, which are arhythmically
flicked to circulate water through sensory setae. Heptacarpus sitchensis, on the other hand, has
aesthetascs in a thick tuft on the outer flagella, which are rapidly and repeatedly spun through
180° in periodic bouts. In P. danae, the flagella became noticeably discolored within several
days of ablation, while in H. sitchensis noticeable darkening occurred within two to three days,
followed by obvious breakage and complete loss of the aesthetascs within 2 weeks of ablation.
Flicking of the outer flagella imposes hydrodynamic forces upon the aesthetascs (Koehl 2011).
Breakage of aesthetascs probably occurred in H. sitchensis because of the increased drag (due
to fouling) on these delicate setae as they are fluttered rapidly back and forth. The fouling con-
sisted of sediment particles, microbial growth (filamentous bacteria, diatoms, ciliates, other ses-
sile protists), and budding colonies of fouling organisms such as bryozoans.
The second antenna (A2) flagellum of decapods is an important chemotactile append-
age, and it is usually groomed. In the decapod shrimps (Penaeoidea, Sergestoidea, Caridea,
A B
C D E
F G H
I b J
Fig. 13.2.
Setal microstructure of grooming appendages. (A and B) Lateral and medial views of the first maxilliped
grooming brushes in the stomatopod Gonodactylus oerstedii (modified from Bauer 1987, used with permis-
sion). (C) Serrate setae of the fifth pereopod propodal grooming brush of the caridean shrimp Pandalus danae
(from Bauer 1975, with permission from John Wiley and Sons). (D and E). Setal ultrastructure of stomatopod
grooming brushes, showing multidenticulate scale setules (modified from Bauer 1987). (F) Portion of seto-
branch seta with multidenticulate scale setules of the caridean shrimp Heptacarpus sitchensis (from Bauer
1979, with permission from John Wiley and Sons). (G) Portion of seta with multidenticulate scale setule from
first pereopod chela grooming brushes of the caridean shrimp Palaemon ritteri (from Bauer 1979, with per-
mission from John Wiley and Sons). (H) Serrate seta of third maxilliped antennular cleaning combs of H.
sitchensis (Bauer 2004, with permission from University of Oklahoma Press). (I and J) Grooming append-
ages of the ostracod Vargula hilgendorfii (courtesy of Jean Vannier): distal end of grooming appendage with
distal terminus (t) and bristles (b) (I) and higher magnification of terminus showing small comb composed
of recurved serrate setae (J).
A1
Mx3
C B
CP DB
CP PD
PD
1 2 3 4
2 3
4 5
C
1 E
Fig. 13.3.
Grooming of first (A1) and second antennae. (A) The third maxillipeds (Mx3) grasp and groom an anten-
nule (at arrowhead) in a hermit crab (from Bauer 1981, with permission from John Wiley and Sons). (B–D)
Grooming in the caridean shrimp Pandalus danae: first antenna (B, thick arrows) grooming (thin arrows);
third maxilliped, with dense rows (C, arrows) of serrate grooming setae; and third maxilliped autogrooming
(D, arrows). CP, carpus; DB, debris; PD, propodus-dactylus (from Bauer 1975, with permission from Wiley
Blackwell). (E) Second antenna grooming: 1, first pereopod carpal (cp) and propodal (pd) grooming brushes
for second antenna (from Bauer 1981, with permission from John Wiley and Sons); 2–5, second antenna
grooming by the first pereopod carpal and propodal brushes (from Bauer 1975, with permission from John
Wiley and Sons).
Stenopodidea), the long A2 flagellum is usually cleaned by a specific pair of brushes sur-
rounding the carpal-propodal (CP) joint of the first pereopod (P1) (Bauer 1978, De Grave and
Goulding, 2011). Bauer (1978) termed these the P1–CP antennal cleaning brushes (Fig. 13.3E).
The P1–CP brushes are often V-shaped and arched over the CP joint; the propodal brush is
variously composed of rows of serrate setae. During A2 grooming, the shrimp reaches up with
one P1 and catches the base of the ipsilateral A2 flagellum between the CP brushes; the flagel-
lum is then quickly drawn through and cleaned by the brushes (Fig. 13.3E). In other decapods,
where the antennal flagellum is often shorter and/or stouter and the P1 often much larger and
more robust, these brushes are not present. In such decapods, for example, astacideans, anomu-
rans, and brachyuran crabs, the antennal flagella are simply brought between the M3, which
scrub them with the serrate setae used to groom the antennules. In the stenopodidean shrimp
Stenopus hispidus, the A1 flagella are also quite long. Interestingly, a pair of brushes surrounding
the M3 propodal-dactylar joint cleans these flagella in a fashion similar to P1–CP cleaning of the
A2 flagella (Bauer 1989).
Gill Cleaning
The selective pressure to maintain clean gills and prevent their fouling is high in crustaceans,
as it is in all aquatic animals. In animals without an exoskeleton, that is, fishes and soft-bodied
invertebrates, epidermal tissues can secrete mucus in which sediment particles and other foul-
ing materials are entrapped and carried off the body by ciliary currents. In crustaceans, the
cuticular gills have no such autocleaning mechanism.
In decapod crustaceans, the potential for fouling of the highly branched gills is particularly
great because of their enclosure within a chamber by the branchiostegite (gill cover), forming a
sediment trap (Bauer 1989). Most decapods are capable of back-flushing some particulate foul-
ing by periodic reversals of the respiratory flow (“cough reflex”). Many have a dense array of
complex setae along the margins of the branchiostegite and/or the thoracic limb coxae that can
filter out some particulate fouling before it enters the gill chamber. However, these setal filters
cannot have too fine a mesh or they will block the respiratory flow of water. Therefore, gill foul-
ing occurs and must be eliminated.
A variety of mechanisms have evolved in decapods to prevent or remove fouling from the
gill chamber (Table 13.1) (Bauer 1981, 1989, Suzuki and McLay 1998, Batang and Suzuki 2003a,
2003b). Gill-cleaning mechanisms all involve the jostling, scraping, or brushing of complex
setae (with multidenticulate, toothed, or hooked setules) among and against the gills. Gill-
cleaning mechanisms might be categorized on a continuum from passive to active. Passive
gill cleaning (PGC) occurs more or less automatically as the cleaning setae are jostled over
and among the gills during ordinary movements of the locomotory, feeding, or respiratory
structures that bear them.
One such PGC mechanism is composed of setobranchs, papillae on thoracic coxae of M3 and
P1–P4 from which multidenticulate gill-cleaning setae project up into the gill chamber (Figs.
13.4A, 13.5A–D). These setobranch setae are found in many caridean shrimps, crayfishes (asta-
coideans, parastacoideans), and many thalassinideans (Thalassinidae, Laomedidae, Axiidae,
Calocarididae). Another important PGC device is a complex of setiferous epipods on some or all
of the thoracic limbs that extend up among the gills. Setiferous epipods have been described in
a variety of decapods: penaeoidean shrimps (Figs. 13.4B,C, 13.5E–H) (Bauer 1999), astacideans
(clawed lobsters, crayfishes) (Bauer 1998, Batang and Suzuki 2000), palinurans (e.g., spiny and
slipper lobsters) (Bauer 1989), and various thalassinideans (e.g., mud lobsters, Thalassinidae; mud
shrimps, Laomediidae) (Batang and Suzuki 1999, 2003, Batang et al. 2001). They are the major
gill-cleaning mechanism in the “true” crabs (Brachyura) (Bauer 1989, Batang and Suzuki 2003a).
Table 13.1. Gill-cleaning mechanisms in decapod crustaceans reported in the litera-

ture (Bauer 1981, 1989, Suzuki and McLay 1998, Batang and Suzuki 2003a, 2003b).
Mechanism/Taxon Setiferous Setobranch Scaphognathite Branchiostegal Cheliped

epipods setae setae setae brushing
DENDROBRAN-
CHIATA:
Penaeoidea ± – – ± –
Sergestoidea – – – – –
PLEOCYEMATA:
Caridea – ± ± – ±
Stenopodidea – – – – +
Astacidea ± ± ± ± –
Palinura + – – – –
Thalassinidea ± ± ± – ±
Anomura – – – – +
Brachyura + – ± – –
Symbols: +, present; –, absent or no observations reported; ±, present in some species examined but not in others. See the
text and above citations for details.
In brachyurans, an epipod projecting back from the first maxilliped lies above the gills, while the
epipods of the second maxilliped and M3 lie below them (Fig. 13.4D). When these maxillipeds
are moved during feeding or other activities, their setose epipods are swept back and forth over
the gills. In the primitive Brachyura (Dromiacea), setiferous epipods may also be present on the
anterior pereopods.
Other PGC mechanisms may play a complementary or minor role in gill cleaning
(Table 13.1). Long multidenticulate scaphognathite setae project backward from the posterior
border of the “gill bailer,” or scaphognathite, the exite of the second maxilla. As the scaphog-
nathite beats, moving water through the gill chamber, these setae simultaneously sweep over
the lateral surface of the gills. In some crayfishes, the inside of the branchiostegite is studded
with multidenticulate setae that project inward into the outer layer of gills (Bauer 1998, Batang
and Suzuki 2000). When these podobranch gills, attached to the limb coxae, move up and down
during limb movements, they are brushed by the branchiostegal setae. In the penaeid shrimp
Rimapenaeus similis, setiferous exopods sweep over the lateral surface of the gills, cleaning
them (Bauer 1999). In some of the dromiacean crabs, groups of setae arising from the body wall
project into the gills and may clean them.
Although setiferous epipods, setobranchs, and branchiostegal setae are generally described
as PGC, cleaning may not be entirely passive. In crayfishes (Bauer 1998, 2002, Batang and
Suzuki 2000) and some carideans (Bauer 1975), there may be bouts of “limb rocking.” While
the animal is otherwise at rest; the pereopods are rocked to and fro. These movements, which
have no other apparent function, move the setobranch setae and/or setiferous epipods within
the gill chamber, presumably cleaning the gills. Similarly, the maxillipeds of brachyuran
crabs may move repeatedly when the animal is at rest, but not feeding, brushing their epipods
against the gills.
PGC, like active gill cleaning (see below), is very effective in keeping gill filaments clean
of sediment (Fig. 13.6A,B). The sweeping action of multidenticulate scaphognathite setae,
SS
5 4
3
2 1 m3
e
m3
e e x
x e x 1
x x 2
SS 3
4
5
e
A
e e x
x e x
x x
B
gcs
e
1
gcs
c 2
3
g
x
C D
Fig. 13.4.
Passive gill-cleaning morphology in decapods. (A) Top, crayfish Procambarus clarkii, cephalothorax with
gill cover removed; bottom, all gills removed to show the many setobranch setae (ss) arising from limb
coxae. m3, basal segments of third maxilliped; 1–5, coxae of pereopods 1–5 (modified from Bauer 1998, his
fig 1, with permission from John Wiley and Sons). (B) Penaeid shrimp Rimapenaeus similis: with gill cover
removed to show gills (top); magnification of outlined area above, showing gills, epipods, and exopods of
third maxilliped (m3) and pereopods 1–5 (middle); and with gills removed to show gill-cleaning setae on
epipods (e) and exopods (x) (bottom) (from Bauer 1999, with permission from John Wiley and Sons). (C)
Setiferous pereopodal epipod of the penaeid shrimp Farfantepenaeus brevirostris. Abbreviations: b, basis;
c, coxa; e, epipod; gcs, gill-cleaning setae; x, exopod (from Bauer 1981, with permission from John Wiley
and Sons). (D) Exposed right branchial chamber (dashed line) of brachyuran crab Pachygrapsus crassipes
showing gills with epipod 1 dorsal to gills (g) and epipods 1–3 below the gills. gcs, gill-cleaning setae (from
Bauer 1981, with permission from John Wiley and Sons).
A B
C D
E F
G H
Fig. 13.5.
Scanning electron micrographs of passive gill-cleaning mechanisms in two decapods. (A–D) crayfish
Procambarus clarkia (modified from Bauer 1998, with permission from John Wiley and Sons). (A) Exposed
gill chamber with outer layer of gills (podobranchs) removed to show setobranch setae (arrows). (B)
Coxae of pereopods with setobranchs (sb) and their setae (ss) extending up into the arthrobranch gills.
(C) Setobranch setae (ss) among gill filaments (f). (D) Microstructure of setobranch setae (ss) with multi-
denticulate scale setules (sc) lying against a gill filament (f). (E–H) Penaeid shrimp Rimapenaeus similis
(from Bauer 1999, with permission from John Wiley and Sons). (E) Basal segments of pereopods with the
exopod (x) cleaning setae lying on gills, and proximal part of epipods (e) with cleaning setae lying between
gills. (F) Tip of an epipod (e) and its setae between adjacent gills. (G) Epipod seta (es) lying among gill
filaments (f). (H) Small portion of epipod seta with multidenticulate scale setules.
A. Crayfish Setobranch Gill-Cleaning Experiment

Control (clean) gill
40
Experimental (fouled) gill
35
Percent Transparency
30
25
20
15
10
5
0
AAU-S AAU-P AAL-S AAS-P PAU-S PAU-P PAL-S PAL-P
Gill Type--Experiemental Location
B. Lithodid Crab P5 Gill-Cleaning Experiment

50
40
Percent Reflectance
30
20
10
0
P4AR P4PL P3 P2 P1 M3
Gill Position
Fig. 13.6.
Quantitative measures of gill fouling amputation experiments. (A) Transparency of crayfish (Procambarus
clarkii) gills to transmitted light after exposure to fouling (medians and 95% confidence limits) (Bauer
1998, with permission from John Wiley and Sons). Control gills were in contact with setobranchs, whereas
experimental gills were not. Abbreviations: AA, anterior arthrobranchs; PA, posterior arthrobranchs; L,
lower half of gill; U, upper half of gill; P, commercial crayfish pond experiment; S, natural swamp experi-
ment. (B) Light ref lectance from gills of lithodid crabs with the fifth pereopod (P5) grooming limbs intact
(control) or amputated (experimental) (means ± SD, from data in Pohle 1989). Abbreviations: P4AR and
P4PL, arthro- and pleurobranchs of fourth pereopod; M3 and P1–P3, arthrobranchs of third maxilliped
and pereopods 1–3.
setiferous epipods, and other PGC may afford some protection against settlement of macrofoul-
ing organisms on some gill surfaces (Batang and Suzuki 2003a). However, PGC appears rather
ineffective against epibiotic fouling by microbes. In experiments with the crayfish Procambarus
clarkii and the penaeid shrimp Rimapenaeus similis (Bauer, 1998, 1999, respectively), microbial
growth of various kinds occurred, similar to microbial fouling on ungroomed aesthetascs of the
stomatopod Gonodactylus oerstedii (Fig. 13.7A,B). Removal of the setobranchs in P. clarkii from
one branchial chamber but not the other resulted in significant and measurable sediment foul-
ing on most of the experimental gills (Figs. 13.6A, 13.7C,D). The lateral surfaces of the outer gills
(podobranchs), which are cleaned by setae on the inside of the branchiostegite, remained clean
in both the experimental and control chambers. Likewise, an inner layer of gills in the penae-
oid shrimp Rimapenaeus was fouled when the gill-cleaning setiferous epipods were removed
(Fig. 13.7E,F)
Fig. 13.7.
Fouling of structures by the experimentally induced absence of cleaning mechanisms. (A and B)
Stomatopod Gonodactylus oerstedii (from Bauer 1987, used with permission): clean aesthetascs, groomed
by first maxilliped (A), and aesthetascs fouled (first maxilliped removed) by filamentous bacteria (B). (C
and D) Crayfish Procambarus clarkii (from Bauer 1998, with permission from John Wiley and Sons): clean
gills (C; setobranchs present) and sediment-fouled gills (D; setobranchs removed). (E and F) Penaeid
shrimp Rimapenaeus similis (from Bauer 1999, with permission from John Wiley and Sons): clean (E; setif-
erous epipods present) and fouled (F; epipods removed) gill filaments.
Active Gill Cleaning
Other decapods lack PGC; instead, they actively brush and pick at the gills by periodically
inserting grooming chelae equipped with complex setae into a gill chamber (Fig. 13.8A–D)
(Bauer 1989, Pohle 1989). Grooming chelipeds in shrimps may also be used in probing the
surroundings and in feeding. Cheliped brushing of gills is found in some families of caridean
shrimps (Bauer 1979), all anomurans, and upogebiid, callianassid, and ctenochelid thalassi-
nideans (Bauer 1981, Batang and Suzuki 2003b). Cheliped gill brushing allows the animal to
devote variable, specific time and attention to cleaning different areas of the gills, presumably
stimulated by particular fouling or irritation. Gill brushing often takes a significant amount of
the animal’s time and energy (Bauer 1977).
In caridean shrimps, the smaller or less robust of the two pairs of chelipeds (P1 or P2,
Fig. 13.8B) is usually devoted to gill and general body grooming (GBG). In addition to setal
G
P1-CP
A B
C D
E F
Fig. 13.8.
Gill and general body grooming in decapods. (A) Gill (G) cleaning by grooming chelipeds (arrows) in the
caridean shrimp Heptacarpus sitchensis (from Bauer 1981, with permission from John Wiley and Sons). (B)
Cheliped 2 (left) of H. sitchensis, with multiarticulated carpus (C), and cheliped 1 (right, CP) of Palaemon
ritteri, unsegmented carpus; note the setal grooming brushes on chelae of both species and the antennal
cleaning brushes on cheliped 1 of the first pereopod (P1-CP) (from Bauer 1979, with permission from John
Wiley and Sons). (C) Anomuran (galatheid) crab Pleuroncodes planipes showing the fifth pereopod groom-
ing appendages (arrowheads) (from Bauer 1981, with permission from John Wiley and Sons). (D) Fifth
pereopod grooming appendage of the galatheid P. planipes (from Bauer 1981, with permission from John
Wiley and Sons). (E and F) General body grooming in P. ritteri (from Bauer 1978, used with permission):
pleopods (E) and abdomen and carapace (F).
grooming brushes on the chelae, these chelipeds may have adaptations for increasing limb
f lexibility during grooming. In most caridean shrimps in which P2 is the gill-grooming
cheliped (pandalids, hippolytids, alpheids, processids), the limb obtains increased distal
f lexibility by subdivision of the carpal (prechela) article into few to many articulating subu-
nits (Figs. 13.8B, 13.9A) (Bauer 1975, 1979). The multiarticulated grooming chelipeds may
be asymmetrical, in which the cheliped on one side is longer and more slender (left in pan-
dalids, Fig. 13.9A; right in processids), with a greater number of carpal subarticles and thus
more specialized for grooming (Bauer 2004). Stenopodidean shrimps also groom the gills
with both the first and second chelipeds, but their grooming setae are not multidenticulate
as in carideans (Bauer 1989).
Other taxa with active gill cleaning include the anomuran crabs (e.g., porcelain, sand,
hermit, and king crabs; squat lobsters) and the upogebiid, callianassid, and ctenochelid tha-
lassinideans (mud shrimps, ghost shrimps). In these decapods, it is the last pereopod (P5),
usually a walking leg in other decapods, that is adapted for grooming. In anomuran crabs,
the P5 is more slender and shorter than in the thalassinideans and bears a small chela, allow-
ing them not only to brush but also to pick at small objects on the gills. In anomurans, these
grooming limbs are often carried partially or completely within the gill chamber when not
in use (e.g., aeglid crabs, Martin and Felgenhauer 1986; lithodid or king crabs, Pohle 1989).
The P5 cleaning setae are complex and adapted for rasping, but unlike the setae used in
caridean gill brushing and in PGC, their ultrastructure is quite varied, for example, serrate,
plumose, or smooth, but not equipped with multidenticulate scales (Pohle 1989, Fleischer
et al. 1992).
Experiments in which gill-cleaning chelipeds are removed or disabled clearly show both
the antifouling function and the superior effectiveness of cheliped gill brushing compared
with PGC. Bauer (1979) removed the second (grooming) chelipeds of the hippolytid caridean
shrimp Heptacarpus sitchensis in an experimental group and the first walking legs (P3) in con-
trols. Trauma of amputation was reduced by removing a limb at its natural basal autotomy
plane, which immediately closes the wound. Within a few days of ablation, the gills of experi-
mental shrimps became visible through the branchiostegite because of sediment fouling,
while those of controls remained clean. Particulate fouling (sediment, detritus) was measured
quantitatively using a light meter to record the relative transmission of light through gills
mounted on slides and viewed with a light microscope (Bauer 1979). Additionally, microbial
organisms (diatoms, sessile ciliates, filamentous long-chained bacteria) were found attached
to gill lamellae of experimentals. Only very light epibiotic fouling occurred in controls.
Shrimps with fouled gills showed distress or died in low-oxygen water, but control shrimps
did not (Bauer 1979).
Pohle (1989) experimentally investigated the effectiveness of gill brushing in the
anomuran crab Lithodes maja by either immobilizing or amputating the P5 grooming limbs.
As with the caridean shrimps, heavy epizoic and sediment fouling was observed qualitatively
and measured quantitatively on experimental crabs, with little fouling on control crabs (see
above). Abdomens of some fouled crabs, which later died, became swollen by water uptake,
possibly because of interference with ion regulation caused by gill fouling. Ritchie and Høeg
(1981) showed with amputation experiments that the P5 grooming chelae of a porcelain crab are
extremely effective at preventing infestation by a serious pest, a rhizocephalan barnacle, whose
infective larval stages first settle on the gills.
Active gill cleaning by grooming chelipeds is clearly a more effective gill-cleaning mech-
anism than PGC because not only can particulate matter be brushed away but also attached
epizoites can be grasped and picked off. As a result, active gill cleaning and PGC are generally
GB
A B
C D
E F
Fig. 13.9.
General grooming in decapod shrimps. (A) Unequal left and right second (grooming) chelipeds of
Pandalus danae , both with multiarticulated carpus (C) (from Bauer 1975, with permission from John
Wiley and Sons). (B) Distal articles of fourth pereopod of the crayfish Procambarus clarkii with propodal
grooming brush (GB) (from Bauer 1981, with permission from John Wiley and Sons). (C) General body
grooming (arrows) of the abdomen with the grooming brush (GB) (from Bauer 1975, with permission
from John Wiley and Sons). (D) Carapace in P. danae with the fifth pereopod propodal grooming brush
(from Bauer 1975). (E) Grooming of posterior carapace (arrow) (from Martin and Felgenhauer 1986, with
permission from Wiley-Blackwell). (F) Incubated embryos with the fifth pereopod grooming append-
age in the freshwater anomuran crab Aegla (from Martin and Felgenhauer 1986, with permission from
Wiley-Blackwell).
mutually exclusive; decapods with grooming chelipeds have neither PGC nor branchiostegal
margin or limb base setal filters. Likewise, the thalassinideans with P5 gill cleaning lack PGC
present in other taxa of the group (Batang and Suzuki 2003b). All anomurans have P5 cheliped
brushing but lack PGC of any kind. PGC has been shown to be the primitive and active gill
cleaning the derived method of gill cleaning in decapods (Bauer 1989).
General Body Grooming
Decapods groom their general body surfaces, including appendages and eyes, to varying degrees
(Figs. 13.8E,F, 13.9B–E). In many decapods, setal brushes and combs on various appendages
have evolved for GBG (Bauer 1978, 1981, 1989). In caridean shrimps, either the first or second
chelipeds, whichever is the smaller, more slender pair, groom the body. In carideans with active
gill grooming, the same pair of chelipeds is also used in GBG. Likewise, in anomurans, the
specialized P5 chelate grooming limbs used in gill cleaning also perform GBG. In several other
decapod groups, P4 and especially P5, which are nonchelate walking legs, have GBG brushes
or combs of serrate grooming setae on the distal articles (Fig. 13.9B) (Bauer 1981, 1989: many
caridean shrimps, astacidean crayfishes and lobsters, palinuran lobsters, thalassinideans but
not dendrobranchiate and stenopodidean shrimps or brachyuran crabs). These P4 or P5 GBG
brushes generally clean the abdomen and posterior cephalothorax (Fig. 13.9C–E)
The hypothesis that GBG prevents fouling of the general body surfaces has been tested
experimentally. Bauer (1975, 1978) showed that marine shrimps with ablated grooming limbs
suffered significant microbial (e.g., ciliate) and even macroscopic (e.g., hydroids) fouling while
control shrimps did not. On the other hand, similar experiments done on freshwater crayfishes
(Bauer 2002) showed little fouling when grooming was prevented. Although GBG by the minor
chelipeds and last walking legs does take place in crayfishes, its frequency and duration are sig-
nificantly less than in shrimps studied. Bauer (1989) showed that GBG behavior is most highly
developed in decapod shrimps such as Caridea and Stenopodidea and generally reduced or lost
in the primarily benthic decapods, in which adaptations for forward swimming with pleopods
and the backward escape are reduced or lost. Fouling produces drag (resistance to movement
through the water), and this selective pressure is important in decapod shrimps but less so
in decapods primarily adapted for crawling or running (e.g., crayfishes, lobsters, brachyuran
crabs). Some anomuran crabs have highly developed GBG using the P5; they are an exception
to this evolutionary trend.
Embryo Care
Females of all decapod taxa except the dendrobranchiate shrimps incubate fertilized eggs
throughout their development to hatching. After spawning and fertilization, the incipient
embryos are attached to the pleopods (swimmerets) below the abdomen. Incubation includes
“aeration,” in which the pleopods beat or the whole abdomen flaps (brachyuran crabs) to cir-
culate water through the embryos, facilitating oxygenation and removal of wastes from the
embryos. Additionally, many decapods use grooming limbs to preen and groom the embryos.
Embryo cleaning is well developed in those taxa with active gill cleaning. Thus, the stenop-
odidean and caridean shrimps also employ the grooming chelipeds to brush and pick among
the embryos (Bauer 1979, 1981), as do decapods with P5 gill-grooming chelipeds (anomurans:
Martin and Felgenhauer 1986, Förster and Baeza 2001) (Fig. 13.9F). However, minor chelipeds
and/or nonchelate P5 walking legs with distal brushes and combs of some decapods (e.g., cray-
fishes, lobsters) can also pick at and brush the embryos, although not as efficiently as in the
carideans and anomurans. Brachyuran crabs may pick and probe among the embryo mass with
chelipeds (Baeza and Ferná ndez 2002), but these limbs are usually too robust relative to embryo
size to do much good and may actually cause embryo mortality.
Observations and experiments on some carideans and anomurans show that significant
embryo mortality results in the absence of embryo cleaning (Bauer 1979, Pohle 1989, Förster and
Baeza 2001). Buildup of sediment and detritus within the embryo mass may create anoxic areas.
Bacterial growth on the embryos may prevent gas exchange and excretion (Bauer 1979); how-
ever, the deleterious effect of bacterial fouling on embryos is controversial (Kuris 1991). Small
egg predators, such as nemertean worms, may infest the decapod embryo mass, causing signifi-
cant embryo mortality prior to hatching. Such predators are much less prevalent in decapods
using grooming chelipeds to actively clean the embryos (caridean shrimps, anomurans) than
in those without such cleaning, especially the brachyuran crabs, in which high infestation and
serious embryo mortality are common (Kuris and Wickham 1987).
Other Antifouling Mechanisms
Although many decapod and other crustaceans groom frequently and intensely, others groom
little or not all. Morphological specializations for grooming are not apparent in many taxa.
Nonetheless, species of such taxa suffer little or no fouling. What prevents the cuticle of such
crustaceans from being fouled? All crustaceans molt periodically, bestowing them with a new,
unfouled exoskeleton. Molting is energetically expensive, and it is doubtful that molting rates
have evolved in response to fouling. However, in many small crustaceans, frequent molting dur-
ing growth may effectively eliminate the need for specific antifouling mechanisms.
Other factors may explain the low intensity or lack of grooming and their morphological spe-
cializations. Fouling pressures may vary among environments. For example, fouling pressure by
macroscopic fouling organisms may be much lower in freshwater than in marine environments,
given the much higher diversity of settling organisms in the latter. The lifestyle of a crustacean
may impede fouling, for example, direct burrowing into mud or sand substratum (e.g., Becker
and Wahl 1996). The abrasive action of sediment particles on the exoskeleton may preclude foul-
ing by other organisms. Consistent exposure to strong currents (high flow) may reduce fouling
pressure on crustaceans (Wolff 1959). In very turbid or deep-sea environments, algal fouling
pressure is absent. Isopods may be plagued by epibiotic fouling, and various mechanisms may
operate to reduce this fouling, such as burrowing (Ólafsdóttir and Svavarsson 2001) or noctur-
nal behavior, which avoids algal fouling (Glynn 1970).
Physical and chemical characteristics of the exoskeleton surface, such as texture, surface
boundary properties (e.g., hydrophilic vs. hydrophobic), and chemical defenses, may have
evolved against fouling. Bauer (1981) suggested that the tegumental glands, which open onto
the surface of the cuticle, could secrete antifouling compounds. However, there is no evidence
of this to date. Becker and Wahl (1996) investigated the role of cuticular surface tension and
bioactive compounds, which were not found to be important antifouling mechanisms in sev-
eral brachyuran crabs. They concluded that behavioral activities, such as burying in sediment,
aerial emersion, and nocturnal activity, were the primary antifouling mechanisms of the crabs
studied. Becker et al. (2000), based on a study of fouling properties of 45 crustacean species,
concluded that hydrophobic/-philic properties (“wettability”) of cuticles, which might impede
settlement of fouling organisms, had little relationship to fouling susceptibility.
Grooming in Other Malacostracans
Stomatopoda
The stomatopods are another crustacean group in which grooming is highly developed (Bauer
1987). A single pair of specialized appendages, the first maxilliped, is adapted for grooming,
with a high density and diversity of rasping and brushing setae. The first maxillipeds groom all
parts of the body but concentrate, in the few species studied, on the chemosensory appendages
(antennules) and the masses of gill filaments located on the pleopods (Fig. 13.10A). The unat-
tached embryo mass is held by the maxillipeds of females in their burrows, and it is constantly
kneaded and brushed during embryo development. Ablation experiments in the tropical species
a1
a2
c
g1
g2
A B
h pb h
le 7(r') pb
le
r 7(r)
r
7(l)
7(l)
4
C feg 3 D
2 T
1 f
r 7(r)
0 h
7(r)
7(l)
E le F
f 7(l)
h 7(I)
fre
le
st
G H
Fig. 13.10.
Grooming in some nondecapod crustaceans. (A) The stomatopod Gonodactylus oerstedii cleaning gills
(arrowhead) with the first maxillipeds (black) (from Bauer 1987, with permission from John Wiley and
Sons). (B) First and second antenna (a1, a2) grooming (arrow) by the first gnathopods (g1) in the gamma-
rid amphipod Paraceradocus gibber. c, carpus; g2, gnathopod 2 (from Coleman 1989, used with permission).
(C–H) Grooming behavior by the vermiform, multiarticulate seventh (grooming) appendage in Vargula
hilgendorfii (from Vannier and Abe 1993, with permission from the Journal of Crustacean Biology): posi-
tion of right and left seventh appendages within the shell (C), generalized grooming movements within and
outside of the shell (D–F; different gray shades show time series of limb movements), grooming of embryos
within the brood chamber (G), and sweeping moments by tip of grooming appendage (H). Abbreviations:
f, furca; feg, fertilized eggs in ovaries; fre, embryos free within brood chamber; h, heart; le, lateral eye; pb,
posterior part of body; r, rostrum; st, stomach; 7(l) and 7(r), left and right seventh appendages.
Gonodactylus oerstedii demonstrated that first maxilliped grooming protects the gills and anten-
nular aesthetascs from microbial fouling (Bauer 1987).
Peracarida
Both terrestrial and aquatic amphipods (Malacostraca: Peracarida) actively groom with the
first two pereopods, the subchelate (prehensile) gnathopods 1 and 2 (Caine 1976, Coleman 1989,
Holmquist 1989). The distal segments of these appendages may be equipped with dense fields of
multidenticulate cuticular scales or complex setae. Gnathopods brush and scrape appendages,
especially the long chemosensory antennae (A1, A2). A gnathopod may individually brush the
long flagellum, proximal to distal, of an A1 or A2 flagellum (Fig. 13.10B). Antennae may also be
pulled to the mouthfield by a gnathopod 1, where it is cleaned by chewing of the maxillae and
other mouthparts. In the Antarctic gammarid Paraceradocus, gnathopod 2 propodal brushes
clean the uropods and pleopods by flexion of the body so that gnathopod 2 can grasp the append-
age; the body is straightened out and gnathopod 2 moved forward (Coleman 1989). Gnathopods
of a pair often autogroom, that is, clean each other by reciprocal rubbing. In females, incubated
embryos and the ventral marsupium that contains them are brushed, cleaned, and jostled by the
gnathopods.
Most isopods are also subject to epibiotic fouling (Glynn 1970, Ólafsdóttir and Svavarsson
2001). In the Isopoda (Holmquist 1989), the pereopods are cleaned by complex cuticular
scales and setae of the mouthparts (mandibles, both pairs of maxillae, maxillipedal palps).
A pereopod is typically brought up into the mouthparts, which grasp it; as the pereopod is
withdrawn to its normal position, its distal segments are chewed and scraped by the mouth-
parts and their cuticular scales and setae. The P1 appears to be a major grooming appendage
in isopods, with a specialized grooved carpal brush of setae, used in frequent cleaning of the
A2 f lagellum. Both the cleaning brush and grooming movement are very similar to P1–CP
antennal brushing of decapod shrimps (Holmquist 1989); a P1 is cleaned by the mouthparts
before it cleans an A2.
Mysids are shrimplike crustaceans often grouped with the peracarids primarily because
females have marsupia formed by oostegites. Given their active swimming lifestyle, it is not
surprising that grooming behavior may be well developed. The single in-depth study on a
mysid species (Acosta and Poirrier 1992) demonstrated preening, especially of the chemo-
sensory A1 and A2. In Mysidopsis bahia, the mandibular palps and thoracic endopod 2 (T2)
cooperate in cleaning A1 and A2. All the other thoracic endopods, except for T1 (specialized
for feeding), clean and comb their corresponding exopods, which are setose swimming struc-
tures. T8 cleans the outside, at least, of the marsupium (brood pouch); cleaning of incubated
embryos was not observed. All the cleaning appendages, especially the mandibular palp and
T2, are distally equipped with complex rasping or brushing setae. Paradoxically, GBG, which
might be expected to be important in a swimming animal to prevent drag by epibiont fouling,
was not reported.
Grooming in Other Crustaceans
Remipedia
In members of the primitive class Remipedia, grooming is a frequent and noticeable behavior
(Carpenter 1999, Koenemann et al. 2007). These elongate wormlike animals are composed
of many similar somites with paddlelike limbs. They occur in the anchialine environment,
that is, submerged caves with inland surface openings and subsurface connections to the sea
(Yager 1991). The olfactory aesthetascs, located at the base of A1, are combed at each stroke
of the incessantly beating pair of A2. Material groomed off the aesthetascs is directed toward
the mouth and may be a form of suspension feeding on detritus. The A2 pair and the (pur-
portedly sensory) frontal appendages periodically groom each other. The A1 flagella are peri-
odically groomed during the forward power strokes of the anterior trunk appendages during
metachronal swimming. Mouthparts (both pairs of maxillae and especially the maxillipeds)
clean each other and the trunk (swimming) limbs; the posterior part of the body may be curled
forward to accommodate limb grooming. Grooming becomes more frequent as remipedians
are stressed during laboratory observations, especially as they are nearing death (Koenemann
et al. 2007), emphasizing the importance of grooming to this crustacean. Frequent grooming
in remipedes may occur in response to their constant secretion of mucus, in which particulate
matter accumulates.
Ostracoda
This is a group of small-sized, ecologically important, diverse, and usually benthic crustaceans
in which the carapace forms a bivalved shell around the body from which the appendages can
be extruded. During their activities just above or within the bottom, the appendages and inside
of shell may become fouled with detritus and sediment. Grooming in this class, composed of
two subclasses, the Myodocopa and Podocopa, has been best summarized by Vannier and Abe
(1993), with extensive observations on the myodocopid Vargula hilgendorfii (Fig. 13.10C–H). The
last (seventh) pair of appendages are the grooming limbs in most myodocopid ostracods and are
modified into long multiarticulate (vermiform), flexible limbs, very much convergent in struc-
ture and function to the multiarticulate second chelipeds described above for many caridean
species. The terminal 20 articles of the grooming limbs are equipped with setal bristles used
to brush various surfaces within the shell on the appendages and, in females, the developing
embryos. The terminal segments also bear a number of structures, such as combs, pegs, and
hooks, which aid in scraping and rasping the body surface. This very active, flexible grooming
limb may also reach outside the shell to clean its outer surfaces and appears stimulated to groom
after burrowing. Grooming of embryos (Myodocopa only) appears to keep them relatively
free from fouling. Embryos are also rotated by grooming, perhaps to increase water circulation
among them. Vannier and Abe (1993) report that in podocopan ostracods, the seventh limb has
many fewer articles and may either be a walking leg or a grooming appendage; in some ostra-
cods, the limb is vestigial or absent.
Branchiura
Members of the maxillopodan subclass Branchiura (“fish lice”) are common ectoparasites that
live on the mucus-covered bodies of fishes but that freely swim about and among hosts. Thus, it
is not surprising that grooming adaptations have evolved. Martin (1932) reported that the spines
and hooks of the maxillae groom the thoracopods (T1–T4), the adult swimming appendages.
Additionally, Overstreet et al. (1992) reported that a posterior process (flabellum) on the exo-
pods of T1 and T2 groom the other thoracopods. The T1 endopod bears at its tip forcepslike
claws that probably clean the underside of the body.
Mystacocarida
These tiny interstitial maxillopodans show morphological structures indicative of grooming,

but this has not yet been observed (e.g., Lombardi and Ruppert’s 1982 study on locomotion).
Boxshall and Defaye (1996) describe a number of complex telsonic combs composed of finely
digitate scale setae that, along with the pincerlike caudal furcae, might groom appendages raised
toward them by flexion of the body. However, Lombardi and Ruppert (1982) hypothesized that
these structures serve as important posterior contact points for the mystacocaridan’s turning-
escape response.
Copepoda
Few reports on grooming have been made in the maxillopodan taxon Copepoda, indicating
that it may not be a particularly frequent or important behavior in this relatively well-observed
group. Costello et al. (1990) reported that the A1 of the calanoid Centropages hamatus is cleaned
by passing it through the feeding appendages. Price et al. (1983) mentioned A1 grooming by
basal segments of the maxillipeds in Eucalanus pileatus, as well as a rare scraping of the swim-
ming legs by the maxillae, a behavior apparently not related to feeding. Carman and Dobbs
(1997) reported microbial fouling on the body surface of copepods along with a lack of grooming
and morphological specializations for it. McAllen and Hannah (1999) observed heavy microbial
fouling on the harpacticoid Tigriopus brevcornis, which they characterized as lacking special-
ized grooming appendages. Biofouled individuals showed lower overall swimming rates than
unfouled individuals, which might result in lower capture rates of females for mating (McAllen
and Scott 2000).
Other Crustacea
Reports and indications of grooming structures in other Crustacea are few. Many of these crus-
taceans are small, with rapid molting rates during most or all of their life history (e.g., copepods
or most branchiopods) that may preclude grooming. Moderate or even heavy fouling may sim-
ply be tolerated, as in many branchiopods such as anostracans (D.C. Rogers, personal commu-
nication, 2011) and cladocerans, in which heavy epibiotic fouling of the carapace may increase
visibility of the cladocerans to predators and clog the setal filters of the feeding appendages
(Amoros 1996). Some barnacles periodically delaminate the outer layers of their calcareous shell,
a possible antifouling adaptation (W.A. Newman, personal communication, 2011). As indicated
previously, fouling pressures may be low enough in some habitats that there is little selection for
specific grooming morphology and behavior. Finally, an apparent lack of grooming behavior in
many crustaceans may simply be due to a lack of extensive observation of living animals.
REPRODUCTIVE APPENDAGES AND STRUCTURES
In many crustaceans, appendages are modified for particular reproductive purposes, mainly
gamete transfer and embryo incubation. Crustaceans produce sperm or eggs in gonads empty-
ing into ducts that lead to gonopores, from which the gametes exit to the exterior (see chapter 15).
In most crustaceans, broadcast spawning of sperm and unfertilized eggs into the water, so com-
mon in many invertebrate groups, is unknown. The sperm cells are immobile (Pochon-Masson
1994) and need to be delivered by the male to the female to fertilize the eggs. In some crusta-
ceans, insemination and fertilization are truly internal, with sperm deposited directly within
the female reproductive tract (oviduct). In others, sperm deposition and subsequent fertiliza-
tion are external. Sperm deposition may be internalized but not truly internal; that is, sperm or
packets of sperm (spermatophores) are deposited and protected within cuticular invaginations,
termed spermathecae (= sperm receptacles). Spermatophores may be deposited directly on or in
the female by external extensions of the male ducts (genital papillae; penes) extending out from
the male gonopores. However, in many crustaceans, papillae or penes cannot extend far enough
to reach the appropriate location on the female. Thus, appendages with some other primary
function (e.g., locomotion) may be modified or may evolve exclusively as sexual appendages for
spermatophore transfer. Limbs may also be modified to incubate (brood) eggs or developing
embryos. Although females of a few crustacean species release fertilized eggs into the water for
development (broadcast or free spawners), most others retain and incubate the embryos during
some or all of their development.
Malacostraca
Reproductive biology of the class Malacostraca, especially the Decapoda (superorder

Eucarida), has received much attention compared to that of other taxa. In all Malacostraca,
the male gonopores are located on the limb coxae or the sternum of the last thoracic segment.
As a result, the inner branches (endopods) of the first two abdominal appendages (pleopods)
are often modified as gonopods in males to aid in transport of spermatophores to the female
during copulation and insemination (Bauer 1986). In two decapod groups, the cambarid cray-
fishes (Astacidea) and brachyuran crabs, the endopods of the first and second pleopods (PL1,
PL2) have independently evolved into a complex injection system for transferring spermato-
phore material into female spermathecae. An external extension of each male ejaculatory duct
(genital papilla or penis) is inserted into the base of the ipsilateral, enrolled, tubelike PL1 endo-
pod (“barrel” of the “syringe”) (Fig. 13.11A) that narrows at its tip (“syringe needle”). The PL2
endopod and/or its process, the appendix masculina (AM) (Fig. 13.11B), also fits into the base
of the PL1 endopod, either sealing it off or serving as a “syringe plunger,” or both. Seminal
material from the penes is injected with thrusting movements through the PL1 endopod into
the female seminal receptacles (Andrews 1911, Hartnoll 1975, Beninger et al. 1991, Diesel 1991).
Hartnoll (1975) has proposed three evolutionary grades (Fig. 13.11A,B) in the evolution of the
first and second pleopods from primitive nephropidean (lobster) to dromiacean brachyuran to
a derived branchyuran injection system.
In another malacostracan superorder, the Peracarida, somewhat analogous pleopodal
injection systems for sperm transfer have evolved in many of the Isopoda (Wilson 1991).
Isopod females may store sperm in the terminal end of the oviducts, which are elaborated into
cuticle-lined spermathecae (Fig. 13.11C). In some isopods, either one or both anterior pleopods
form a funnel or other complex system serving as an extension conduit from the male genital
papillae (penes) into the female gonopores (Fig. 13.11D). In other isopods, the PL2 bears a stalk-
like AM whose exact role in sperm transfer is unknown. Interestingly, in other members of the
diverse Peracarida (e.g., mysidacean, amphipods, cumaceans, tanaidaceans), male modification
of pleopods for sperm transfer is rare or absent. In these peracarids, male genital papillae may
be paired or may be fused into a single genital cone or penis (Fig. 13.11D). The genital papil-
lae or cone may simply deposit sperm near the female gonopores or elsewhere within the mar-
supium (female brood pouch) where spawned eggs later make contact with deposited sperm.
Alternately, males may directly insert the penes into female gonopores (Wilson 1991, Johnson
et al. 2001). The actual mode of insemination is rarely known with great confidence; copulation
is often quite rapid, and the interplay of male and female genitalia is obstructed from view dur-
ing mating.
In other malacostracans, modification of the anterior male pleopods as gonopods varies from
none to complex. The PL1 endopods of males in the shrimplike anaspidacean syncarids, male
euphausiaceans and dendrobranchiate decapod shrimps (penaeoideans and sergestoideans) are
modified and joined to form a complex, intricate structure termed the petasma (Figs. 13.12A,D,F,
13.13A,B,D). As in many malacostracans, the PL2 endopods of males bear less intricate AM
ov
g1
od
p
o
m
c
sp
g2
A C
e
e
b
e
b
a
a
e x a
e
b e b
p
b p11 p12
B D
a
Fig. 13.11.
Male sperm-injection systems. (A) Ventral view of posterior thorax and anterior abdomen of a male
crab, Chionoecetes opilio (Brachyura), showing the syringelike insemination complex of first and second
gonopods (g1, g2), with the penes (p) inserted within the bases of the first gonopods. c, coxa of poste-
riormost pereopod (from Beninger et al. 1991, used with permission). (B) Morphological grades of male
first (above) and second (below) pleopods from a simple to complex sperm-injection system in astacidean
lobster Nephrops norvegicus (left), the primitive brachyuran Dromia personata (center), and more advanced
brachyuran Carcinus maenas (right). Abbreviations: a, appendix masculina; b, basipod of pleopod; e, endo-
pod; x, exopod (from Hartnoll 1975, used with permission). (C) Female reproductive system in the isopods
Epipenaeon (Bopyridae, above) and Sphaeroma (Oniscidae, below) from cross section of thoracic segment
6. Abbreviations: o, oostegite; od, oviduct; ov, ovary, m, marsupium; sp, spermatheca (from Wilson 1991,
with permission from Columbia University Press). (D) Male insemination morphology in the oniscid iso-
pod Porcellio, showing the “funnel” variation of injection system. Abbreviations: a, appendix masculina; p,
fused penes; pl1, pl2, first and second pleopods (from Wilson 1991, used with permission).
ai
am
e ai
e
x
A B C
p5
D E
e e
p5
F G H
Fig. 13.12.
Genitalia of decapod shrimps. (A) Posterior view, right half of petasma in the euphausiid Nematobrachion
flexipes (from Boden et al. 1955, with permission from Scripps Institution of Oceanography, UC San Diego).
(B and C) Caridean Rhynchocinetes albatrossae (from Chace 1997, used with permission): appendix interna
(ai) on the medial edge of the first pleopod endopod (e) (B) and appendices masculina (am) and interna
(ai) on medial edge of the second pleopod endopod (e) (C). x, exopod. (D–G) Petasma (D, F) and closed
thelycum (E, G) of the penaeid shrimp Melicertus kerathurus (D and E) and Macropetasma africanus (F and
G). p5, basal articles of the fifth pereopod (from Pérez Farfante and Kensley 1997, with permission from the
Muséum National d’Histoire Naturelle, Paris). (H) First pleopods of the caridean Campylonotus vagans,
with petasma-like fusion of endopods (e) (from Torti and Boschi 1973, used with permission).
Fig. 13.13.
Scanning electron micrographs of penaeoid shrimp genitalia. (A–D) Male Sicyonia dorsalis (from
Bauer 1996, with permission from Taylor and Francis, Ltd.): ventrolateral view of posterior thorax and
anterior abdomen showing the petasma (pt) and appendices masculinae (am) in situ (A), petasma
from posterior (ventral, B) and anterior (dorsal, D) views, and appendices masculinae (am; C).
Abbreviations: b1, b2, basipods of first and second pleopods; p5, basal articles of fifth (last) pereopod.
(E–H) Female Rimapenaeus similis (from Bauer and Min 1993, with permission from the Biological
Bulletin): thelycum of uninseminated (E) and inseminated (F) female (with protruding male mating
plug [pg]), internal view of sternum behind thelycum with baglike spermathecae (G), and sperm
packets within a spermatheca (H).
(Figs. 13.12C, 13.13A,C). In euphausiaceans, saclike spermatophores are attached to the female
thelycum just posterior to the female gonopores under the cephalothorax. In penaeoidean and
sergestoidean shrimps, single or twin sternal plates (Figs. 13.12E, 13.13E,F) comprise a “closed
thelycum” behind which a single or paired spermathecae (Fig. 13.13G) are located and into which
relatively simple spermatophores (Fig. 13.13H) may be deposited. Alternately, the female may
have an intricately sculptured “open thelycum” (Fig. 13.12G) to which a complex external sper-
matophore can be attached.
Although the petasma and PL2 AMs are often referred to as “copulatory organs,” their
actual role in sperm transfer is problematic (Burkenroad 1934, Brinton 1978, Bauer 1991,
Coineau 1996). An alternative hypothesis based on experimental work (Bauer 1996) suggested
that the complex petasma serves to anchor the male in position while male genital papillae
are directly inserted into the opening of female spermathecae. The species-specific petasma
morphology of euphausiaceans and dendrobranchiates is suggestive of a “lock-and-key”
mechanical role in copulation. However, the female thelyca of most species do not show a cor-
responding complex “lock” morphology to a male petasma “key.” Eberhard (1985) proposed
that male genitalia of many animals appear more complicated than necessary to carry out
insemination. Their complexity might arise if serving as genitalic courtship devices subject
to sexual selection.
In most caridean shrimps, the PL1 endopods are little to somewhat modified from a basic leaf-
like swimming ramus, linked together (unlike the females) by appendices internae (Fig. 13.12B).
Only in the campylonotid carideans are the PL1 endopods joined, dendrobranchiate style, all
along their inner edges by cincinnuli (small curled setae) (Fig. 13.12H). The second pleopods of
caridean males bear AM that vary greatly in size and shape (Bauer 2004). The role of caridean
male “gonopods” in sperm transfer is controversial. Mating experiments have been conducted
with caridean species (Bauer 1976, Berg and Sandifer 1984) in which males were deprived of
gonopods or their rami in different combinations. In these matings, spermatophores were either
not transferred or not correctly placed on the female. The model proposed was that gonopod
appendices catch the adhesive spermatophores emitted by the male that were then pressed onto
the female without entanglement on the male. Although the results of these studies are concord-
ant with a hypothesis of spermatophore transfer function by PL1 and PL2, they do not reject
other possible hypotheses, for example, that the gonopods are stimulating/courtship devices or
perhaps sensory structures orienting the male to the female during copulation. Evidence refut-
ing the model comes from numerous mating observations on the caridean Lysmata wurdemanni
in which both male-phase (with AM) and simultaneous hermaphrodite (without AM) individu-
als are successful in mating as males (e.g., Bauer 2006).
In many decapods, such as stenopodidean shrimps, parastacid and astacid crayfishes, tha-
lassinideans, palinurid lobsters, and anomurans, the first two pleopods are only slightly, if at all,
modified as apparent gonopods (Bauer 1986). One example of moderate modification is found
in galatheid crabs (Anomura), in which Kronenberger et al. (2004) hypothesized that purported
male gonopods pick up a spermatophore ribbon before separation and placement of spermato-
phores onto the female. However, Hess and Bauer (2002) found no sperm transfer role by pleo-
pods in the hermit crab Clibinarius vittatus (Anomura, Diogenidae). In some hermit and aeglid
crabs (Tudge 2003), the male genital papillae are quite long (“sexual tubes”) and may function
in placement of spermatophores on the female during copulation (Tudge and Lemaitre 2006).
In lithodid, galatheid, and aeglid crabs, the male fifth pereopods may assist in spermatophore
attachment (Almerão et al. 2010). Clearly, there is much diversity in insemination mechanics
that needs to be investigated in the Decapoda.
In stomatopods, appendages appear to be little modified for insemination (Caldwell 1991,
Wortham-Neal 2002). The male has elongated genital papillae or penes that are inappropriately
termed “gonopods” because these structures are not modified appendages. During copulation,
the male inserts these penes into a genital slit on the female’s sixth thoracic sternite and, via
separate ducts within the penes, transmits sperm cords and secretions of accessory glands into a
median seminal receptacle. The accessory gland secretion appears to be a sperm plug to prevent
insemination by other males (Wortham-Neal 2002).
Remipedia
In some crustacean classes, there is little or no modification of appendages for reproduction.

The primitive wormlike, cave-dwelling remipedians are simultaneous hermaphrodites with
serially homologous biramous swimming limbs. None appear modified for reproductive pur-
poses. The male and female sexual systems are recognized externally only by placement of their
respective gonopores on different trunk somites (Yager 1991).
Cephalocarida
These small marine epibenthic crustaceans are also simultaneous hermaphrodites lacking spe-
cialized male intromittent organs (e.g., Hessler and Elofsson 1996). However, the epipods and
exopods of the sixth thoracic limbs, upon whose protopods the gonopores open, are modified,
possibly to concentrate or guide sperm during the presumed copulation (Hessler et al. 1995).
Branchiopoda
This class of crustaceans with phyllopodous limbs used in locomotion and feeding has various
male mechanisms for inseminating females. In the Anostraca (fairy or brine shrimps), the male
gonopods, thought to be modified thoracic limbs (Rogers et al. 2007), are located just anterior to
the abdomen (Fig. 13.14A). The basic mating system of anostracans is a “scramble competition”
(“pure searching”) in which males constantly search for receptive females (Belk 1991). Upon
encountering a female, the male interacts with her and, if allowed, grasps the female body with
its two-jointed A2 around either her brood pouch or genital segment (Fig. 13.14B) just behind
her last pair of appendages (amplexial groove; Rogers 2002). One of the gonopods introduces
sperm through the terminal male gonopore into the female’s brood pouch via the latter’s poste-
rior pore, stimulating the release of unfertilized eggs into the brood pouch, where fertilization
occurs. The A2 of male anostracans (fairy shrimps) are much larger and different in structure
than those of females, often bizarrely so, with much variation among species (Belk 1991, Dodson
and Frey (1991), Thiéry 1996, Rogers 2002) (Fig. 13.14C,D). In many species, the male antennal
claspers form a species-specific “key” that matches the female amplexial-groove “lock” (Rogers
2002). The A2 may be very elaborate in structure, with a variety of surface textures, spines,
knobs, and intricate antennal or frontal appendages that function as tactile premating court-
ship devices. Females appear to evaluate these antennal processes in choosing among males,
leading Belk (1991) to the conclusion that male A2 intricacy is a result of sexual selection.
Unlike the anostracans, males of the Notostraca (tadpole shrimps) have little appendage
modification for reproduction (Thiéry 1996), although male phyllopod (trunk limb) 11 serves as
a male gonopod in some species. However, in another major branchiopod group, the “concho-
stracans” or clam shrimps (Order Diplostraca: Laevicaudata, Spinicaudata, and Cyclestherida),
phyllopods 1 and 2 of males terminate in prehensile or subchelate claspers for grasping the female
carapace during pairing and copulation. In the diplostracan suborder Cladocera (water fleas),
the first trunk appendage of the male may similarly be prehensile or hooked for grasping the
female. The A1 flagella of males in some species are elongated, with hooks and spines to aid in
Fig. 13.14.
Anostracan sexual appendage morphology. (A) Male (above) and female (below) of Branchinecta cornig-
era. bp, brood pouch; gp, male gonopods (modified from Lynch 1958, used with permission). (B) Amplexus
in Linderiella occidentalis (female at left, male at right). A2, second antenna; bp, brood pouch (modified
from Dodson and Frey (1991), with permission from Elsevier). (C) Polyartemiella hazeni: frontal (left) and
lateral (right) views of male head with second antenna (A2) gripping the female brood pouch (bp) (modi-
fied from Rogers 2002, used with permission). (D) Anterior view of male Thamnocephalus platyrus (left)
with frontal appendage (fa) and Streptocephalus texanus (right) with antennal appendages (aa). A2, second
antenna (modified from Dodson and Frey (1991), with permission from Elsevier).
clinging to the female during mating (Thiéry 1996). In Daphnia pulex, the male seizes the female
legs with T1 and long setae of A1 (Fig. 13.15A) Dodson and Frey (1991).
Ostracoda
In this species-rich class, sexual morphology has been described for various species, although
complementary observations on mating and copulation are relatively few. However, some
generalizations can be made about the diverse reproductive appendages in the group, based
primarily on the excellent reviews by McGregor and Kessling (1969) and Cohen and Morin
(1990). The paired male copulatory organs, often complex and oversized in these small crus-
taceans, may have evolved from an eighth pair of appendages (Cohen and Morin 1990) and
therefore are located just posterior to the other appendages and anterior to the caudal furcae.
In the podocopans, the copulatory organs or hemipenes may be incredibly large and intricate
structures (Fig. 13.15B), occupying much of the body volume. Ostracod mating appendages
A1
cf
A B hp
t
sv
m
f
cl
C D
f
A1
E F
ch
sp ac
ch e
x pc
G H I
Fig. 13.15.
Sexual appendages and behavior of selected nondecapod crustaceans. (A) Copulation in the cladoceran Daphnia
pulex (male below) (modified from Strickler 1998, after Jurine 1820, used with permission from the Royal Society
of London). (B) Male of podocopan ostracod Candona suburbana, with right valve removed to show the left hemi-
penis rotated out in copulatory position. Abbreviations: A1, first antenna; cf, caudal furca; hp, hemipenis (modi-
fied from Morin and Cohen 1991, after McGregor and Kessling 1969, used with permission). (C) Mating of C.
suburbana male (m) and female (f) (from McGregor and Kessling 1969, used with permission). (D) Male genitalia
of myodocopan ostracod Spinacopa sandersi. Arrow shows penis. Abbreviations: cl, clasping limb; sv, seminal vesi-
cles; t, testis (modified from Morin and Cohen 1991, after Kornicker 1969, used with permission). (E) Mating in
cyclopoid copepod Cyclops: male (m) grasps female (f) with both first antennae (A1) prior to copulation (modified
from Strickler 1998, after Jurine 1820, used with permission from the Royal Society of London). (F) Copulation in
calanoid copepod Diaptomus: male (m) grasps female (f) urosome with his chelate fifth swimming leg prior to
spermatophore placement (modified from Strickler 1998, after Jurine 1820), used with permission from the Royal
Society of London). (G) Calanoid copepod Centropages typicus: chelate (ch) male fifth pereopod (above) and
nonchelate female fifth pereopod (below) (from Blades 1977, used with permission). (H) Copulatory position in
calanoid Labidocera aestiva: posterior body of male (upper, stippled) and female (lower, nonstippled). The female
urosome is gripped by chela (ch) of the male right fifth pereopod while the endopod (e) of the left fifth pere-
opod strokes female sensory pit-pore area as its exopod (x) brushes and probes her genital plate (from Blades and
Youngbluth 1979, used with permission). (I) Spermatophore (sp) attached to female urosome by anterior (ac) and
posterior (pc) couplers in the calanoid C. typicus (from Blades 1977, used with permission).
are sexually dimorphic, and those of males are claspers or other devices for grasping and hold-
ing the female during copulation (Fig. 13.15C). The A1 or A2 may bear suckers or hooks with
which the male grasps the female (Vannier and Abe 1993). In one podocopan species, the fifth
limbs are asymmetrical, with the thicker right one serving to rotate the grasped female into
copulatory position (Abe and Vannier 1991). In some ostracod males, the fifth (first “thoracic”)
limbs have the endopod or palp modified into a pincer for holding the female carapace during
copulation (McGregor and Kessling 1969). In the myodocopans, the male ducts end in a single
penis situated between two variously sized and shaped copulatory or clasping organs (limbs)
(Fig. 13.15D).
Maxillopoda
Within the subclass Thecostra, the infraclass Cirripedia includes the familiar barnacles
(Thoracica), ubiquitous filter-feeding sessile epifauna on hard substrata of marine environ-
ments. In these hermaphrodites, the intromittent organ of functional males is a long, remark-
ably mobile and flexible penis that introduces a sperm mass into the mantle cavity of another
individual serving as a functional female. The penis, arising from between the bases of the pos-
terior cirri, develops from the terminal body sclerite, which is a remnant of the larval abdomen
(Walker 1992). The penis functions in precopulatory searching and copulation; no appendages
are involved. A similar long penis may be present in the acrothoracicans (Klepal 1990), small cir-
ripedes that burrow in limestone substrata, as well as in members of the infraclass Ascothoracida
(Grygier 1996), free-swimming thecostrates that are endo- and ectoparasitic on coelenterates
and echinoderms.
Sexual biology has been fairly well studied in two genera of the maxillopodan subclass
Branchiura. In Dolops ranarum, the male deposits a single large spermatophore from its median
gonopore; female spermathecal spines release sperm so that it flows into her spermathecal
ducts (Fryer 1960). In Argulus japonicus, the spermathecal spines directly penetrate through
the male body wall into blind ejaculatory ducts during copulation, releasing sperm that flows,
driven by a pressure differential, directly into the female spermathecae (Avenant-Oldewage
and Swanepoel 1993). In neither species are male appendages used to transfer sperm or sper-
matophores. However, in mating of D. ranarum, the female is initially seized by the male using
its maxillulary hooks. The male then moves so as to grip the female abdomen with T2 and T3
and then presses the spermatophore against the female genital region using T4 (Fryer 1960). In
Argulus, in addition to T2 and T3 clasping hooks and scales (setae), the male has a T4 “peg” and
T3 “socket” arrangement for clasping the posterior thoracic legs of the female during copula-
tion (Martin 1932, Avenant-Oldewage and Swanepoel 1993). Avenant-Oldewage and Swanepoel
(1993) discounted earlier reports that this “peg and socket” was involved in the actual sperm
transfer.
The Copepoda is a taxonomically and ecologically diverse taxon with considerable varia-
tion in morphology and mating behavior. In cyclopoids, the fifth swimming legs are rudimen-
tary, and the male, after seizing the female with both A1 (Fig. 13.15E), simply sways its body to
the correct position next to the female for spermatophore transfer (C. Jersabek, personal com-
munication, 2011). In the calanoids, the copepod group in which mating has been best studied
(Blades-Eckelbarger 1991, Ohtsuka and Huys 2001), the major appendages modified for repro-
ductive purposes are the male (A1) and last (thoracic) swimming leg (P5). Asymmetry of male
reproductive structures is common in copepods. The right male A1 is often jointed (geniculate)
and prehensile, with the segments on either side of the hinge equipped with gripping teeth and
sensory setae. During mating in calanoids, the male initially grasps the female with its A1 and
then swings its body around so as to seize the female with (usually) the right P5, modified for
gripping the female urosome (Fig. 13.15F–H). The left P5 may first stroke and/or examine the
female genital region (Blades and Youngbluth 1979). A spermatophore is then emitted from the
male genital pore and attached to the genital somite of the female (Fig. 13.15I), where sperm
will be discharged from the spermatophore into the female genital opening and then into the
spermathecae for storage. The gripping morphology of the right P5 is quite variable but often is
a large intricate chela. The left male P5 exopod is modified for seizing the spermatophore and
placing it on the female, while its endopod may serve both for tactile examination of the female
genital segment (Blades-Eckelbarger 1991), as well as cleaning it of debris and spermatophores
from previous broods and matings (Fig. 13.15H). The fifth pereopod of females is also modified
in some calanoid families to clean off discharged spermatophores, using the exopods and coxal
serrations for that purpose (Ohtsuka and Huys 2001).
Tantulocarids are tiny parasites of deep-sea crustaceans that are included in the Maxillopoda
in the Martin and Davis (2001) classification. The ultimate (seventh) thoracic appendages are
modified into an intromittent organ or penis (Boxshall 1996). In another maxillopodan group,
the mystacocaridans, small members of the interstitial fauna, there are no obvious modifica-
tions of appendages for reproduction.
Incubatory Appendages
In many crustaceans, appendages are modified to aid incubation of brooded embryos or to help
store eggs prior to fertilization and release. Embryo grooming and other incubatory activities of
limbs are described above. Here, a brief review is given of appendages that form brood chambers
or to which embryos are attached during incubation. Except for the dendrobranchiate shrimps,
all other decapod crustaceans (suborder Pleocyemata) incubate the embryos below the abdo-
men until hatching. Embryos are attached to pleopods and each other to form an embryo mass.
In decapods in which pleopodal swimming is reduced (e.g., lobsters, crayfishes) or absent
(brachyuran crabs), the pleopods of females may function principally or only for embryo attach-
ment. After a reproductive (parturial) molt, pleopods may undergo changes related to incuba-
tion. In caridean shrimps, for example, the protopods elongate and develop a flange that in part
forms the sides of a spawning chamber that keeps fertilized eggs under the abdomen so that they
can attach. The pleopod rami may have long pinnate setae that form the floor of the spawning
chamber (Höglund 1943, Bauer 2004). Pleopods of reproductive female decapods bear naked
“ovigerous” setae; newly spawned embryos attach to the ovigerous setae and each other to form
the embryo mass that will be incubated prior to hatching.
In the malacostracan superorder Peracarida, a brood pouch (marsupium) is usually formed
by medial lamellar outgrowths from the coxae, termed oostegites, on a variable number of tho-
racopods (McLaughlin 1980). Oostegite size and shape may vary greatly. In amphipods, there
are two general types of oostegites. Broad oostegites with short marginal setae are character-
istic of species with small eggs. In species with large eggs, a common condition in freshwater
ampipods, the oostegites are narrow, with long marginal setae forming the ventral basket of the
marsupium. This allows the necessary greater circulation of water around the large eggs (Steele
1991). The latter author concluded that oostegite shape and size is more a function of environ-
mental adaptation than ancestry. In bopyrid isopods parasitic in the gill chambers of caridean
shrimps, oostegites are little to highly reduced (J. Markham, personal communication, 2011). In
Probopyrus pandalicola, the host shrimp’s gill cover functionally serves as the floor of the female
isopod’s marsupium; consequently, the female parasitic isopod’s oostegites are highly reduced
(Cash and Bauer 1993). However, in other decapod taxa with branchial bopyrids, female bopyrid
oostegites are not reduced (J. Markham, personal communication, 2011). In some peracarids,
the oostegites themselves are invaginated, forming individual brood pouches (Johnson and
Attramadal 1982).
In the malacostracan subclass Phyllocarida (leptostracans), the bivalved carapace encloses

the embryo mass for brooding. However, the endopods from the thoracic limbs of females are
elongate and bear special recurved pinnate setae when a female is sexually mature, forming a
bottom or floor of the brood pouch. These setae drop off after the embryos hatch, leaving basal
scars (Dahl and W ägele 1996).
In the class Branchiopoda, the anostracans have lateral egg sacs that are derived from
trunk limbs (D.C. Rogers, personal communication, 2011). However, their function is not to
incubate embryos but rather as temporary storage for eggs in transit to the medial brood pouch in
which eggs are fertilized and then later released into the environment for development. In repro-
ductive female notostracans, the 11th trunk appendage is an oostegopod (Thiéry 1996) in which
the endite is folded over to form a pouch where eggs are held until fertilization (D.C. Rogers,
personal communication, 2011). In the spinicaudatan and laevicaudatan diplostracans (“conchos-
tracans”), adhesive is secreted through exites of various trunk limbs so that fertilized eggs are
glued either to appendages, the trunk, or carapace flanges (Thiéry 1996; D.C. Rogers, personal
communication, 2011). In all cases, the embryo mass is enclosed by the bivalved carapace. In the
Cephalocarida (Hutchisoniella), the two large eggs are glued for brooding to the reduced ninth
thoracic legs by adhesive segmental glands (Hessler et al. 1995). Brooding of embryos may occur
in other crustaceans (e.g., ostracods, copepods), but appendages are not especially modified for
this purpose, except for limbs that groom brooded embryos (e.g., myodocopan ostracods).
COMPARISONS WITH OTHER TAXA
Grooming
Maintenance of a clean body and appendages is an important process that occurs in most ani-
mals but that has evolved under different selection pressures, resulting in somewhat different
functions, depending on the group. Some animals have no appendages for cleaning and use other
mechanisms to prevent or rid the body of debris. Chemical defenses are important in many ses-
sile marine groups such as sponges and cnidarian corals. In many soft-bodied aquatic animals,
frequent sloughing of surface tissues or mucus secretion prevents accumulation of fouling organ-
isms and material. Some bryozoans and echinoderms have specialized structures for actively
cleaning body surfaces free of fouling. The mucus secreted by fishes impedes fouling but is sup-
plemented in some species by behaviors such as rubbing against the substratum or solicitation
of grooming by other organisms, such as cleaner fishes and shrimps (Poulin and Grutter 1996).
In birds and mammals, much time and energy may be devoted to grooming. In birds, preening
maintains feather structure for flight and insulation. In mammals, fur (hair) structure must be
maintained to prevent wetting and heat loss, especially in cool climates and aquatic habitats. In
both groups, grooming helps keep the body free of ectoparasites, dead epidermal tissues, and
other debris. In birds and especially in mammals, parent-offspring and reciprocal grooming is
common, not only for the primary purposes of cleaning but also to aid with the formation of pair
bonds between both related and nonrelated individuals. Female grooming of hatched offspring
may occur in crustaceans (Thiel 2007). However, reciprocal grooming between unrelated indi-
viduals is not well documented in arthropods. Reciprocity requires long-term memory of the
behavior of other individuals (Wilson 2000), a trait either uncommon or unreported in arthro-
pods, including crustaceans.
Unlike crustaceans, the other major arthropod groups, that is, the Hexapoda (insects),
Myriapoda, and Arachnida, are primarily or completely terrestrial animals. However, they face
fouling pressures analogous to those of crustaceans. Particulate matter suspended in air, the
medium that surrounds them, is filled with dust, pollen, and spores that can foul body surfaces
and appendages. Body surfaces are soiled during daily activities such as in locomotion over or in
soil or other substrata, as well as during feeding. As in crustaceans, modification of appendages
(mouthparts and legs: Jander 1966, Chapman 1982) for grooming (preening) has occurred as
a result of these selective pressures. As in the Crustacea, the chemoreceptive antennae are the
focus of much preening behavior. Antennal cleaning and limb cleaning are carried out primarily
by the mouthparts, especially the mandibles and maxillae, in the more primitive insects (Jander
1966). Preening of antennae, legs, and body surfaces is an important function of the forelegs in
many insects, and distal segments of these limbs are equipped with brushes, combs, and other
specializations (“toilet organs”) for that purpose (Hlavac 1975, Chapman 1982). General body
cleaning with the legs, especially the forelegs, is common, as is mutual leg rubbing. Much of the
general body preening spreads secretions (e.g., antimicrobial) of cuticular and other glands over
the exoskeleton (Hlavac 1975). Such a function of general body cleaning (spreading of secre-
tions) is unknown in Crustacea, perhaps because it has not been investigated.
Autogrooming shows striking similarities between crustaceans and insects in both behavio-
ral and structural features. Setae in cleaning combs and brushes employed in autogrooming are
similarly inclined at an angle toward the tip of the limb so that fouling material is transported
distally when the two limbs of a pair are rubbed or scraped together. Collected debris is moved
toward the limb tip and then drops off (Bauer 1975, 1977, Hlavac 1975). In insects, debris arriving
at the end of a cleaning limb in this way is often simply rubbed off onto the substratum, a behav-
ior not yet reported in crustaceans.
In her excellent study of grooming in insects and myriapods, Jander (1966) made generali-
zations about grooming that can be compared with those in Crustacea. A high frequency of
grooming is correlated with high overall activity as in decapod and stomatopod crustaceans.
However, whether this is simply a high frequency of grooming because all behaviors are fre-
quent in an active animal or a real difference in the relative frequency of grooming between
active versus less active species is a question that needs to be investigated.
Chelicerates (arachnids, xiphosurans, pycnogonids) have no antennae and thus no antennal
grooming. Aquatic arthropods other than crustaceans, mostly the marine groups (xiphosurans
or horseshoe crabs and pycnogonids) are as susceptible to epibiotic fouling as their crustacean
relatives. Horseshoe crabs become heavily encrusted, especially as they grow older and inter-
molt periods become longer; fouling is most extensive on areas of the body (dorsal carapace) not
abraded by burrowing or mating activities (Patil and Anil 2000). Prosomal limbs are relatively
short and physically unable to reach the dorsal surface if they do participate in cleaning at all. The
opisthomal (“abdominal”) book gills clean each other without the help of prosomal appendages
(Watson 1980). The usually sluggish sea spiders (Pycnogonida) are often heavily encrusted with
a variety of marine epizoites such as hydroids, sponges, and tubeworms (Arnaud and Bamber
1987). Grooming is one of the functions of two appendages arising from the cephalon, the mul-
tisegmented palps and the ovigers.
The terrestrial arachnids would seem to be susceptible to similar fouling pressures as other
terrestrial arthropods, but the literature on arachnid grooming is sparse, indicating that it is
not common or simply has been ignored. It is a common behavior in Opiliones (harvestmen),
which use the chelate chelicerae and movable coxae of the pedipalps and forelegs (Pinto-da
Rocha et al. 2007).
Reproductive Appendages
In the aquatic arthropods, there is no broadcast spawning of sperm and egg into the water as
in many aquatic invertebrates and fishes. The xiphosuran (horseshoe) crabs do release sperm
over eggs spawned in depressions in moist sand high up on sandy beaches. Many terrestrial
arthropods such as arachnids, myriapods, and primitive insects transfer sperm indirectly; that
is, male and female genital openings are not in direct contact. With the exception of harvest-
men (Opiliones) and some mites (Acari), in which males copulate with a penis, the terrestrial
arachnids use indirect sperm transfer, as do many myriapods and primitive insects such as col-
lembolans, thysanurans, and diplurans (Chapman 1982). However, in the winged (pterygote)
insects, sperm transfer occurs directly by means of penes that contain the distal ends of the male
reproductive tracts. Adult insects do not have well-developed abdominal appendages, but a few
reduced abdominal appendages may be modified in males for grasping females (claspers) or as
intromittent organs for copulation, analogous to the gonopods of crustaceans.
Although parental care of young is not common in insects in general (e.g., Tallamy 1999),
when it does occur it usually takes the form of guarding the eggs or young or providing them
with food. Similarly, care of embryos is common in arachnids, ranging from viviparity and care
of the juveniles in scorpions to eggs sacs carried by the female in several arachnid taxa (Polis and
Sisson 1990). However, there is little if any modification of appendages or other body structures
for this purpose in insects and arachnids comparable to those found in crustaceans, possibly
because they have much fewer appendages (usually only three or four pairs) available for modi-
fications beyond the primary tasks (feeding and locomotion).
FUTURE DIRECTIONS
The rather extensive work on grooming structure and function in decapod crustaceans needs
to be extended to other crustacean groups. Hypotheses on the evolution of grooming behaviors
can be tested by experiments with individual species as well as with the comparative method
with appropriate phylogenetic adjustment (mapping of characters on phylogenetic trees to iden-
tify adaptations arising from common descent or independent evolutionary origins). The role
of chemical defenses and the neuroethology of grooming are both areas that need attention, as
does the role of cleaning symbioses in many crustacean groups.
The adaptive value of complex genitalia in crustaceans is as poorly known as in other ani-
mal groups. Are genitalia complex because of mechanical function in transfer or because of a
courtship function (stimulation of females, sexual selection)? In many crustacean groups, even
basic knowledge of mating and the mechanics of insemination is lacking. The adaptive value of
appendage structures known only from taxonomic descriptions may become apparent as obser-
vation and experimentation on reproductive function is done on poorly studied taxa.
ACKNOWLEDGMENTS
My thanks to the editors of this volume for the invitation to write this chapter and to Martin
Angel, Geoffrey Boxshall, Anne Cohen, Christian Jersabek, John Markham, Joel W. Martin,
Ole Sten Møller, William Newman, D. Christopher Rogers, Rudi Strickler, and others who
have contributed information and comments about grooming and sexual appendages of vari-
ous taxa. This is University of Louisiana, Lafayette, Laboratory for Crustacean Research
Contribution No. 143.
REFERENCES
Abe, K., and J. Vannier. 1991. Mating behavior in the podocopid ostracode Bicornucythere bisanensis
(Okubo, 1975): Rotation of a female by a male with asymmetric fifth limbs. Journal of Crustacean
Biology 11:250–260.
Acosta, C., and M. Poirrier. 1992. Grooming behavior and associated structures of the mysid Mysidopsis
bahia. Journal of Crustacean Biology 12:383–391.
Almerão, M., G. Bond-Buckup, and M.S. Mendonça Jr. 2010. Mating behavior of Aegla platensis
(Crustacea, Anomura, Aeglidae) under laboratory conditions. Journal of Ethology 28:87–94.
Amoros, C. 1996. Branchiopodes. II. Ctènopodes, Anomopodes, Onychopodes et Haplopodes. Pages
353–383 in J. Forest, editor. Traité de Zoologie, Tome 7, Crustacés, Fascicule 2. Masson, Paris.
Andrews, E.A. 1911. Male organs for sperm-transfer in the crayfish, Cambarus affinis: Their structure and
use. Journal of Morphology 22:239 –297.
Arnaud, F., and R.N. Bamber. 1987. The Biology of Pycnogonida. Advances in Marine Biology 24:1–96.
Avenant-Oldewage, A., and J.H. Swanpoel. 1993. The male reproductive system and mechanisms of
sperm transfer in Argulus japonicus (Crustacea: Branchiura). Journal of Morphology 215:51–63.
Baeza, J.A., and M. Ferná ndez. 2002. Active brood care in Cancer setosus (Crustacea: Decapoda): The
relationship between female behaviour, embryo oxygen consumption and the cost of brooding.
Functional Ecology 16:241–251.
Batang , Z., and H. Suzuki. 1999. Gill-cleaning mechanisms of the mud lobster Thalassina anomala
Herbst, 1804 (Decapoda: Thalassinidea: Thalassinidae). Journal of Crustacean Biology 19:671–683.
Batang , Z.B., and H. Suzuki. 2000. Gill structure and gill-cleaning mechanisms of the redclaw cray-
fish Cherax quadricarinatus (Decapoda: Astacidea, Parastacidae). Journal of Crustacean Biology
20:699 –714.
Batang , Z.B., and H. Suzuki. 2003a. Gill-cleaning mechanisms of the amphibious freshwater crab
Geothelphusa dehaani (Decapoda, Brachyura, Potamidae). Journal of Crustacean Biology
23:230 –240.
Batang , Z.B., and H. Suzuki. 2003b. Gill cleaning mechanisms of the burrowing thalassinidean shrimps
Nihonotryphaea japonica and Upogebia major (Crustacea: Decapoda). Journal of Zoology 261:69 –77.
Batang , Z.B., H. Suzuki, and T. Miura. 2001. Gill-cleaning mechanisms of the burrowing mud shrimp
Laomedia astacina (Decapoda, Thalassinidea, Laomediidae). Journal of Crustacean Biology
21:873–884.
Bauer, R.T. 1975 . Grooming behaviour and morphology of the caridean shrimps Pandalus danae.
Zoological Journal Linnean Society 56:45–71.
Bauer, R.T. 1976. Mating behaviour and spermatophore transfer in the shrimp Heptacarpus pictus
(Stimpson) (Decapoda: Caridea: Hippolytidae). Journal of Natural History 10:315–440.
Bauer, R.T. 1977. Antifouling adaptations of marine shrimp (Decapoda: Caridea): Functional morphol-
ogy and adaptive significance of antennular preening by the third maxillipeds. Marine Biology
40:260 –276.
Bauer, R.T. 1978. Antifouling adaptations of caridean shrimps: Cleaning of the antennal flagellum and
general body grooming. Marine Biology 49:69 –82.
Bauer, R.T. 1979. Antifouling adaptations of marine shrimp (Decapoda: Caridea): Gill cleaning mecha-
nisms and grooming of brooded embryos. Zoological Journal of the Linnean Society 65:281–303.
Bauer, R.T. 1981. Grooming behavior and morphology in the decapod Crustacea. Journal of Crustacean
Biology 1:153–173.
Bauer, R.T. 1986. Phylogenetic trends in sperm transfer and storage complexity in decapod crustaceans.
Bauer, R.T. 1987. Stomatopod grooming behavior: Functional morphology and amputation experiments
in Gonodactylus oerstedii. Journal of Crustacean Biology 7:414–432.
Bauer, R.T. 1989. Decapod crustacean grooming: Functional morphology, adaptive value, and phy-
logenetic significance. Pages 49–73 in B.E. Felgenhauer , L. Watling , and A.B. Thistle, editors.
Functional morphology of feeding and grooming in Crustacea. Balkema, Rotterdam.
Bauer, R.T. 1991. Sperm transfer and storage structures in penaeoid shrimps: A functional and phyloge-
netic perspective. Pages 183–207 in R.T. Bauer and J.W. Martin, editors. Crustacean sexual biology.
Columbia University Press, New York.
Bauer, R.T. 1996. Role of the petasma and appendices masculinae during copulation and insemination
in the penaeoid shrimp, Sicyonia dorsalis (Crustacea: Decapoda: Dendrobranchiata). Invertebrate
Reproduction and Development 29:173–184.
Bauer, R.T. 1998. Gill-cleaning mechanisms of the crayfish Procambarus clarkii (Astacidea: Cambaridae):
Experimental testing of setobranch function. Invertebrate Biology 177:129 –143.
Bauer, R.T. 1999. Gill-cleaning mechanisms of a dendrobranchiate shrimp, Rimapenaeus similis
(Decapoda: Penaeidae): Description and experimental testing of function. Journal of Morphology
242:125–139.
Bauer, R.T. 2002. The ineffectiveness of grooming in prevention of body fouling in the red swamp craw-
fish Procambarus clarkii. Aquaculture 208:39 –49.
Bauer, R.T. 2004 . Remarkable shrimps: Adaptations and natural history of the carideans. University of
Oklahoma Press, Norman .
Bauer, R.T. 2006. Same sexual system but variable sociobiology: Evolution of protandric simultaneous
hermaphroditism in Lysmata shrimps. Integrative and Comparative Biology 46:430 –438.
Bauer, R.T., and L.J. Min. 1993. Spermatophores and plug substance of the marine shrimp Trachypenaeus
similis (Crustacea: Decapoda: Penaeidae): Formation in the male reproductive tract and disposition
in the inseminated female. Biological Bulletin 185:174–185.
Becker, K., T. Hormchong , and M. Wahl. 2000. Relevance of crustacean carapace wettability for fouling.
Becker, K., and M. Wahl. 1996. Behaviour patterns as natural antifouling mechanisms of tropical marine
crabs. Journal of Experimental Marine Biology and Ecology 203:245–258.
Belk , D. 1991. Anostracan mating behavior: A case of scramble-competition polygyny. Pages 112–125
in R.T. Bauer and J.W. Martin, editors. Crustacean sexual biology. Columbia University Press,
New York.
Beninger, P.G., R.W. Elner, and Y. Poussart. 1991. Gonopods of the majid crab Chionoecetes opilio (O.
Fabricius). Journal of Crustacean Biology 11:217–228.
Berg , A.B., and P.A. Sandifer. 1984 . Mating behavior of the grass shrimp Palaemonetes pugio Holthuis
(Decapod: Caridea). Journal of Crustacean Biology 4:417–424.
Blades, P.I. 1977. Mating behavior of Centropages typicus (Copepoda, Calanoida). Marine Biology
40:57–64.
Blades, P.I., and M.J. Youngbluth. 1979. Mating behavior of Labidocera aestiva (Copepoda: Calanoida).
Blades-Eckelbarger, P.I. 1991. Functional morphology of spermatophores and sperm transfer in calanoid
copepods. Pages 246–270 in R.T. Bauer and J.W. Martin, editors. Crustacean sexual biology.
Boden, B.P., M.W. Johnson, and E. Brinton. 1955 . The Euphausiacea (Crustacea) of the North Pacific.
Bulletin of the Scripps Institution of Oceanography 6:387–400.
Boxshall, G.A. 1996. Classe des Mystacocarides. Pages 399–408 in J. Forest, editor. Traité de zoologie,
Tome VII, Crustacés, Fascicule 2. Masson, Paris.
Boxshall, G.A., and D. Defaye. 1996. Classe des Mystacocarides. Pages 409–424 in J. Forest, editor. Traité
de zoologie, Tome VII, Crustacés, Fascicule 2. Masson, Paris.
Brinton, E. 1978. Observations on spermatophores attached to pleopods of preserved male euphausiids.
Burkenroad, M.D. 1934 . The Penaeidea of Louisiana, with a discussion of their world relationships.
Bulletin of the American Museum of Natural History 68:61–143.
Caine, E.A. 1976. Cleansing mechanisms of caprellid amphipod (Crustacea) from North America.
Marine Behaviour and Physiology 4:161–169.
Caldwell, R.L. 1991. Variation in reproductive behavior in stomatopod Crustacea. Pages 68–90 in R.T.
Bauer and J.W. Martin, editors. Crustacean sexual biology. Columbia University Press, New York.
Carman, K. R., and F.C. Dobbs. 1997. Epibiotic microorganisms on copepods and other marine crusta-
ceans. Microscopy Research and Technique 37:116 –135.
Carpenter, J.H. 1999. Behavior and ecology of Speleonectes epilimnius (Remipedia, Speleonectidae) from
surface water of an anchialine cave on San Salvador Island, Bahamas. Crustaceana 72:979 –991.
Cash, C.E., and R.T. Bauer. 1993. Adaptations of the branchial parasite Probopyrus pandalicola (Isopoda:
Bopyridae) for survival and reproduction related to ecdysis of the host, Palaemonetes pugio
(Caridea: Palaemonidae). Journal of Crustacean Biology 13:111–124.
Chace, F.A., Jr. 1997. The caridean shrimps (Crustacea: Decapoda) of the Albatross Philippine
Expedition, 1907–1910, Part 7: Families Atyidae, Eugonatonotidae, Rhynchocinetidae,
Bathypalaemonellidae, Processidae, and Hippolytidae. Smithsonian Contributions to Zoology No.
587:1–106.
Chapman, R.F. 1982. The insects. Structure and function. Harvard University Press, Cambridge, MA.
Cohen, A.C., and Morin, J.G. 1990. Patterns of reproduction in ostracodes: A review. Journal of
Coineau, N. 1996. Sous-classe des Eumalacostracès. Super-ordre des Syncarides. Pages 897–954 in J.
Forest, editor. Traité de zoologie, Tome VII, Crustacés, Fascicule 2. Masson, Paris.
Coleman, C.O. 1989. Burrowing, grooming, and feeding behaviour of Paraceradocus, an Antarctic amphi-
Costello, J.H., J.R. Strickler, C. Marrasé, G. Trager, R. Zeller, and A.J. Freise. 1990. Grazing in a turbulent
environment: Behavioral response of a calanoid copepod, Centropages hamatus. Proceedings of the
National Academy of Sciences of the USA 87:1648 –1652.
Dahl, E., and J.-W. W ägele 1996. Sous-classe de Phyllocarides. Pages 865–896 in J. Forest, editor. Traité de
zoologie, Tome VII, Crustacés, Fascicule 2. Masson, Paris.
De Grave, S., and L.Y.D. Goulding. 2011. Comparative morphology of the pereiopod 1 carpo-propodal
(P1-CP) antennal flagellar grooming brush in caridean shrimps (Crustacea, Decapoda).
Zoologischer Anzeiger 250:280 –301.
Diesel, R. 1991. Sperm competition and the evolution of mating behavior in Brachyura, with special
reference to spider crabs (Decapoda, Majidae). Pages 145–163 in R.T. Bauer and J.W. Martin, editors.
Crustacean sexual biology. Columbia University Press, New York.
Dodson, S.I. and D.G. Frey. 1991. Cladocera and other Branchiopoda. Pages 723–786 in J.H. Thorp and
A.P. Covich, editors. Ecology and classification of North American freshwater invertebrates.
Academic Press, New York
Eberhard, W.G. 1985 . Sexual selection and animal genitalia. Harvard University Press, Cambridge, MA .
Fleischer J., M. Grell, J.T. Høeg , and J. Olesen. 1992. Morphology of grooming limbs in species of
Petrolisthes and Pachycheles (Crustacea, Decapoda, Anomura, Porcellanidae)—a scanning
electron-microscopy study. Marine Biology 113:425–435.
Förster, C., and J.A. Baeza. 2001. Active brood care in the anomuran crab Petrolisthes violaceus
(Decapoda: Anomura: Porcellanidae): Grooming of brooded embryos by the fifth pereopods.
Journal of Crustacean Biology 21:606 –615.
Fryer, G. 1960. The spermatophores of Dolops ranarum (Crustacea, Branchiura): Their structure, forma-
tion, and transfer. Quarterly Journal of Microscopical Sciences 101:407–432.
Glynn, P.W. 1970. Growth of algal epiphytes on a tropical marine isopod. Journal of Experimental Marine
Biology and Ecology 5:88 –93.
Grygier, M.J. 1996. Sous-classe des Ascothoracides. Pages 433–452 in J. Forest, editor. Traité de zoologie,
Tome VII, Crustacés, Fascicule 2. Masson, Paris.
Hallberg , E , and M. Skog. 2011. Chemosensory sensilla in crustaceans. Pages 103–122 in T. Breithaupt and
M. Thiel, editors. Chemical communication in crustaceans, Springer, New York.
Hartnoll, R.G. 1975 . Copulatory structure and function in the Dromiacea, and their bearing of the evolu-
tion of the Brachyura. Pubblicazioni Della Stazione Zoologica di Napoli 39(suppl):657–676.
Hess, G.S., and R.T. Bauer. 2002. Spermatophore transfer in the hermit crab Clibanarius vittatus
(Crustacea, Anomura, Diogenidae). Journal of Morphology 253:166 –175.
Hessler, R.R., and R. Elofsson. 1996. Classe des Cephalocaridés. Pages 271–281 in J. Forest, editor. Traité
de zoologie, Tome VII, Crustacés, Fascicule 2. Masson, Paris.
Hessler, R.R, R. Elofsson, and A.Y. Hessler. 1995 . Reproductive system of Hutchisoniella macracantha
(Cephalocarida). Journal of Crustacean Biology 15:493–522.
Hlavac , T. 1975 . Grooming systems of insects: Structure, mechanics. Annals of the Entomological of
America 68:823–826.
Höglund, H. 1943. On the biology and larval development of Leander squilla (L.) forma typica De Man.
Svenska Hydrografisk-Biologiska Kommissionens Skrifter NY Serie, Biologie Band II 6:1–44.
Holmquist, J.G. 1989. Grooming structure and function in some terrestrial Crustacea. Pages 95–114 in
B.E. Felgenhauer , L. Watling , and A.B. Thistle, editors. Functional morphology of feeding and
grooming in Crustacea. Balkema, Rotterdam.
Jander, U. 1966. Untersuchungen zur Stammesgeschichte von Putzbewegungen von Tracheaten.
Zeitschrift f ü r Tierpsychologie 23:799 –844.
Jurine, L. 1820. Histoire des monocles, qui se trouvent aux environs de Genève. Paschoud, Genève.
Johnson, S.B., and Y.G. Attramadal. 1982. Reproductive behaviour and larval development of Tanais
cavolinii (Crustacea: Tanaidacea). Marine Biology 71:11–16.
Johnson, W.S., M. Stevens, and L. Watling. 2001. Reproduction and development of marine peracaridans.
Advances in Marine Biology 39:107–260.
Klepal, W. 1990. The fundamentals of insemination in cirripedes. Oceanography and Marine Biology
Annual Review 28:353–379.
Koehl, M.A.R. 2011. Hydrodynamics of sniffing by crustaceans. Pages 85–102 in T. Breithaupt and M.
Thiel, editors. Chemical communication in crustaceans, Springer, New York.
Koenemann, S., F.R. Schram, T.M. Iliffe, L.A. Hinderstein, and A. Bloechl. 2007. Behavior of Remipedia
in the laboratory, with supporting field observations. Journal of Crustacean Biology 27:534–542.
Kornicker, L.S. 1969. Morphology, ontogeny, and intraspecific variation of Spinacopa, a new genus of
myodocopid ostracod (Sarsiellidae). Smithsonian Contributions to Zoology 8:1–55.
Kronenberger, K., D. Brandis, K. Tü rkay, and V. Storch. 2004 . Functional morphology of the reproduc-
tive system of Galathea intermedia (Decapoda: Anomura). Journal of Morphology 262:500 –516.
Kuris, A. M. 1991. A review of patterns and causes of crustacean brood mortality. Pages 117–141 in A.
Wenner and A. Kuris, Crustacean egg production. Balkema, Rotterdam.
Kuris, A.M., and D.E. Wickham. 1987. Effect of nemertean egg predators on crustaceans. Bulletin of
Marine Science. 41:151–164.
Lombardi, J., and E.E. Ruppert. 1982. Functional morphology of locomotion in Derocheilocaris typica
(Crustacea, Mystacocarida). Zoomorphology 100:1–10
Lynch, J.E. 1958. Branchinecta cornigera, a new species of anostracan phyllopod from the state of
Washington. Proceedings National Academy of the USA 108:25–37.
Martin, J.W., and G.E. Davis. 2001. An updated classification of the recent Crustacea. Natural History
Museum of Los Angeles County Science Series 39:1–124
Martin, J.W., and B.F. Felgenhauer. 1986. Grooming behaviour and the morphology of grooming append-
ages in the endemic South American crab genus Aegla (Decapoda, Anomura, Aeglidae). Journal of
Zoology (A) 209:213–224.
Martin, M.F. 1932. On the morphology and classification of Argulus (Crustacea). Proceedings of the
Zoological Society of London 1932:771–806.
McAllen, R., and F. Hannah. 1999. Biofouling of the high-shore rockpool harpacticoid copepod Tigriopus
brevicornis. Journal of Natural History 331781–1787.
McAllen, R., and G.W. Scott. 2000. Behavioural effects of biofouling in a marine copepod. Journal of the
Marine Biological Association United Kingdom 80:369 –370.
McGregor, D.L., and R.V. Kesling. 1969. Copulatory adaptations in ostracods. Part II. Adaptations in liv-
ing ostracods. Contributions from the Museum of Paleontology University of Michigan 22:221–239.
McLaughlin, P.A. 1980. Comparative morphology of recent Crustacea. Freeman, San Francisco.
Morin, J.G., and A.C. Cohen. 1991. Bioluminescent displays, courtship, and reproduction in ostracodes.
Pages 1–16 in R.T. Bauer and J.W. Martin, editors. Crustacean sexual biology. Columbia University
Press, New York.
Ohtsuka, S., and R. Huys. 2001. Sexual dimorphism in calanoid copepods: Morphology and function.
Hydrobiologia 453/454:441–466.
Ólafsdóttir, S.H., and J. Svavarsson. 2001. Ciliate (Protozoa) epibionts of deep-water asellote isopods
(Crustacea): Pattern and diversity. Journal of Crustacean Biology 22:607–618.
Overstreet, R.M., I. Dyková, and W. E. Hawkins . 1992. Branchiura. Pages 385–414 in F.W. Harrison
and A.G. Humes, editors. Microscopic anatomy of invertebrates, Vol. 9, Crustacea. Wiley-Liss,
New York.
Patil, J.S., and A.C. Anil. 2000. Epibiotic community of the horseshoe crab Tachypleus gigas. Marine
Biology 136:699 –713
Pérez Farfante, I., and B. Kensley. 1997. Penaeoid and sergestoid shrimps and prawns of the world. Keys
and diagnoses for the families and genera. Mémoires du Muséum National d’Histoire Naturelle
175:1–233.
Pinto-da-Rocha, R., G. Machado, and G. Giribet, editors. 2007. Harvestmen. The biology of opiliones.
Harvard University Press, Cambridge, MA.
Pochon-Masson, J. 1994 . Les gamétogènesis. Pages 727–783 in J. Forest, editor. Traité de Zoologie, Tome
VII, Crustacès, Fascicule 1. Masson, Paris.
Pohle, G. 1989. Gill and embryo grooming in lithodid crabs: Comparative morphology based on Lithodes
maja. Pages 75–94 in B.E. Felgenhauer , L. Watling , and A.B. Thistle, editors. Functional morphol-
ogy of feeding and grooming in Crustacea. Balkema, Rotterdam.
Polis, G.A., and W.D. Sissom. 1990. Life history. Pages 161–223 in G.A. Polis, editor. The biology of scorpi-
ons. Stanford University Press, Stanford, CA .
Poulin, R., and A.S. Grutter. 1996. Cleaning symbioses. Proximate and adaptive explanations. Bioscience
46:512–517.
Price, H.J., G.-A. Paffenhöfer, and J.R. Strickler. 1983. Modes of cell capture in calanoid copepods.
Ritchie, L.E., and J.T. Høeg. 1981. The life history of Lernaeodiscus porcellanae (Cirripedia, Rhizocephala)
and co-evolution with its porcellanid host . Journal of Crustacean Biology 1:334–347.
Rogers, D.C. 2002. The amplexial morphology of selected Anostraca. Hydrobiologia 486:1–18.
Rogers, D.C., B.V. Timms, M. Jocquè, and L. Brendonck. 2007. A new genus and species of branchipodid
fairy shrimp (Crustacea: Branchiopoda: Anostraca) from Australia. Zootaxa 1551:49 –59.
Steele, D.H. 1991. Is the oostegite structure of amphipods determined by their phylogeny or an adapta-
tion to their environment? Hydrobiologia 223:27–34.
Strickler, J.R. 1998. Observing free-swimming copepods mating. Philosophical Transactions of the Royal
Society of London Series B 353:671–680
Suzuki, H., and C.L. McLay. 1998. Gill-cleaning mechanisms of Paratya curvirostris (Caridea: Atyidae)
and comparisons with seven species of Japanese atyid shrimps. Journal of Crustacean Biology
18:253–270.
Tallamy, D.W. 1999. Child care among the insects. Scientific American 280:50 –55.
Thiel, M. 2007. Social behavior of parent-offspring groups in crustaceans. Pages 294–318 in J.E. Duffy
and M. Thiel, editors, Evolutionary ecology of social and sexual systems. Oxford University Press,
New York.
Thiéry, A. 1996. Branchiopodes I. Ordres des Anostracés, Notostracés, Spinicaudata et Laevicaudata.
Pages 287–351 in J. Forest, editor. Traité de Zoologie, Tome VII, Crustacès, Fascicule 2. Masson,
Paris.
Torti, M.R., and E.E. Boschi. 1973. Nuevos aportos al conocimiento de los crustáceos Decápodos Caridea
del género Campylonotus Bate 1988. Physis Sección A 32:65–84.
Tudge, C.C. 2003. Endemic and enigmatic: The reproductive biology of Aegla (Crustacea: Anomura:
Aeglidae) with observations on sperm structure. Memoirs of Museum Victoria 60:63–70.
Tudge, C.C., and R. Lemaitre. 2006. Studies of male sexual tubes in hermit crabs (Crustacea, Decapoda,
Anomura, Coenobitidae). II. Morphology of the sexual tube in the land hermit crabs, Coenobita
perlatus and C. clypeatus. Crustacean Research, Special Number 6:121–131.
Vannier, J., and K. Abe. 1993. Functional morphology and behavior of Vargula hilgendorfii (Ostracoda:
Myodocopida) from Japan, and discussion of its crustacean ectoparasites: Preliminary results from
video recordings. Journal of Crustacean Biology 13:51–76.
Walker, G. 1992. Cirripedia. Pages 249–311 in F.W. Harrison and G. Humes, editors. Microscopic anatomy
of invertebrates, Vol. 9, Crustacea. Wiley-Liss, New York.
Watson, W.H. 1980. Limulus gill cleaning behavior. Journal of Comparative Physiology 141:67–75.
Wilson, E.O. 2000. Sociobiology. Belknap Press, Cambridge, MA.
Wilson, G.D.F. 1991. Functional morphology and evolution of isopod genitalia. Pages 228–244 in R.T.
Wolff, T. 1959. Epifauna on certain decapod Crustacea. Pages 1060–1061 in H.R. Hewer and N D.
Riley, editors. Proceedings: 15th International Congress of Zoology, London, 16–23 July 1958.
International Congress of Zoology, London.
Wortham-Neal, J. 2002. Reproductive morphology and biology of male and female mantis shrimp
(Stomatopoda: Squillidae). Journal of Crustacean Biology 22:728 –741.
Yager, J. 1991. The reproductive biology of two species of remipedes. Pages 271–289 in R.T. Bauer and J.W.
Martin, editors. Crustacean sexual biology. Columbia University Press, New York.
14
CIRCULATORY SYSTEM AND RESPIRATION
Christian S. Wirkner and Stefan Richter
Abstract
Circulation and respiration are vital functions in all animals, including crustaceans. This
chapter deals with the morphology of these coupled systems and the functional aspects that
can be deduced from their complex structures. Crustaceans possess an open circulatory
system or, more precisely, an open vascular system. This means that the hemolymph leaves
the vascular structures, that is, the heart and directly connected arteries, and f lows through
either lacunae (spaces between organs) or sinuses (spaces whose function is to channel hemo-
lymph). Lacunae and sinuses form the hemolymph lacunar system. In the various crustacean
taxa, the complexity of the circulatory system ranges from a complete absence of circulatory
structures to highly complex vascular and lacunar systems. Respiration, that is, the exchange
of the respiratory gases oxygen and carbon dioxide, is based on two main features: circula-
tion and ventilation. Externally, the surfaces of the respiratory structures must be ventilated
with a current of the medium, be it air or water, and internally, the circulation of hemolymph
is a prerequisite for the exchange of respiratory gases. Respiratory organs such as epipodites
and carapaces are therefore integral parts of the circulatory system, together returning the
entire hemolymph f low back to the pericardium. Often, osmoregulation takes place at the
same organs as respiration, but the ultrastructure of the epithelia differs. In this chapter we
present for all main crustacean groups an overview of the major circulatory and respiratory
structures and their functions.
INTRODUCTION
When dealing with the functional morphology and diversity of crustaceans, two functions
come to mind that (among others) are essential for the basal functioning and survival of these
organisms: respiration and circulation. Although in arthropods these two functions are not
always coupled (i.e., in Hexapoda and Myriapoda), the functional integration of respiration and
376
Circulatory System and Respiration 377
circulation is the original pattern and is also present in Crustacea. However, it is important to
keep in mind that circulated blood (or, better, hemolymph) transports not only the respiratory
gases (oxygen and carbon dioxide) but also various other molecules (e.g., hormones) and nutri-
ents. Gas exchange is generally facilitated by special respiratory structures, with oxygen and
carbon dioxide then taken to and from the tissues and organs via a circulatory system. The com-
plexity of both systems varies within Crustacea, with the size of the animal playing an important
role. The diffusion of oxygen in aqueous solution is slow, so arthropods bigger than a few mil-
limeters are dependent on a specialized system for the irrigation of tissues. In small animals, on
the other hand, circulation plays a minor role in oxygen transport, but small arthropods too are
covered by a cuticle. Differentiation into areas with a thin cuticle and epithelium, permitting
respiratory gases to diffuse rapidly, and areas with a thicker cuticle to protect the animal might
therefore generally be an advantage. In this case, even small animals need a circulatory system
for gas transport.
In Crustacea, almost all groups possess a circulatory system of some kind; even small water
fleas have a heart (but no other vascular structures) and only very few taxa (certain ostracodes)
lack a hemolymph vascular system entirely. In larger animals, particularly malacostracans, the
circulatory system is astonishingly complex, as is the structure of the respiratory organs. The
arterial system, in particular, can be highly complex. The role of the veins is taken over by a
complex system of sinuses and lacunae. Respiratory structures are mostly called gills or lungs,
depending on whether they are used for breathing in water or air. Respiratory structures are
often only recognized on a gross morphological level and sometimes histologically. However,
it has been shown that ultrastructural studies are necessary to reliably distinguish between
respiratory and osmoregulatory organs and that both functions can be fulfilled by the same
structure (though in different areas). Unfortunately, detailed physiological studies of the two
systems are available for only very few taxa, mostly decapods and/or isopods. We emphasize
those functional aspects that can be directly deduced from the structure (gross morphology
as well as histology and ultrastructure) and in only some cases refer to the physiology of the
system. In our opinion, this approach reflects the divide between functional morphology and
physiology.
It is obvious that not all gills and lungs are homologous in the animal kingdom, and this is
also the case in Crustacea. Functional anatomy, therefore, not only includes the description of
structure and function but also needs to consider the evolutionary origin of these structures. In
light of this, terminology must be used with care, and a clear distinction must be made between
functional and structural terminology, in particular. The importance of consistent terminol-
ogy has recently been highlighted again by developments in morphology. However, there are
at least two distinct schools of thought with regard to structural terms alone. One suggests that
terminology should be independent of taxa and homology (Vogt 2008); the other suggests a
test of primary homology as a criterion for the use of shared terminology (Edgecombe 2008).
The latter regards high structural and developmental correspondences to be indications of a
common evolutionary origin. Both approaches have their merits but, again, need to be distin-
guished. These are exemplified at various points in the following.
CIRCULATORY SYSTEMS
What Is an Open Circulatory System?
Not only is it difficult to separate the different but integrated functions of organisms, but
also organ systems themselves are often difficult to distinguish. While it might be possible to
identify the parts of a closed circulatory system such as the ones found in vertebrates, whose
structures are more or less distinct from other organs, in the case of the open circulatory system
of arthropods it is more difficult because the whole body has to be taken into consideration. The
integument (cuticle and epidermis) surrounds a liquid-filled space in which the different organ
systems are suspended. To provide respiratory gases, hormones, nutrients, and other molecules
and ions to the different tissues and dispose of them again, this liquid has to be circulated by
means of an open circulatory system. The system can be broken down into the hemolymph vas-
cular system (HVS) and the hemolymph lacunar system (HLS). The HVS consists of a central
pumping structure, the heart, and a varying number of vessels that are structurally connected to
the heart and supply different body regions. In analogy to the circulatory system in vertebrates,
arthropod vessels that extend from the heart and channel hemolymph centrifugally from the
heart are termed arteries. All arteries have open endings from which the hemolymph reenters
the body cavity. Therefore, the term open circulatory system more precisely relates to the HVS in
arthropods. True veins in the sense of vertebrate veins, structurally connected to the heart and
bringing hemolymph back to it, are missing in arthropods. However, some sinuses channeling
hemolymph currents into the pericardium are often confusingly termed “veins” in the litera-
ture. In the HLS, two different hemolymph spaces can be distinguished, though this distinction
is not always clear. On the one hand, lacunae are spaces between organs in which hemolymph is
moved either passively or as a by-product of the movement of organs such as the gut or muscles.
These lacunae are nonetheless distinct hemolymph spaces. Other spaces, on the other hand, act
explicitly as channels for hemolymph and are therefore termed sinuses.
In some taxa, the high degree of structural (i.e., of the arterial system and sinuses) and func-
tional (i.e., circulatory regulation and control mechanisms) complexity of the circulatory sys-
tem as a whole (i.e., HVS and HLS) is apparently comparable to that in vertebrates (for further
reading on physiological aspects of the circulatory system in crustaceans, see e.g., Maynard
1960, McMahon et al. 1997, McMahon 2001).
Heart
The shape and performance of crustacean hearts vary extensively among the different groups,
but in most cases the central part of the heart lies in the body region in which the respiratory
organs are situated to ensure that the oxygenated hemolymph has to move only a short distance
to the heart to be redistributed in the body. Histologically, hearts in crustaceans are generally
made up of two distinct cellular layers, an epicardium and a myocardium. The epicardium is
a layer of cells surrounding the myocardium, but it is not always clear whether the accumu-
lation of different cell types around the myocardium can be seen as a layer in its own right
(Tjønneland et al. 1987, Nylund and Tjønneland 1989). The myocardium is the heart muscle
proper and is made up of one muscular layer in most crustaceans. In Stomatopoda, however, two
(Alexandrowicz 1934) and in Decapoda more layers have been described (Baccetti and Bigliardi
1969, Howse et al. 1971, Burrage and Sherman 1978).
Gross Morphology of Hearts
Throughout crustacean taxa, the form and structure of hearts vary immensely (Fig. 14.1). Some
taxa (e.g., most copepods) exhibit no hearts at all, and some groups (e.g., decapods) have highly
complex and powerful hearts.
Hearts are always positioned in the dorsal midline of the body. They are ventrally connected
to the dorsal diaphragm (which constricts the pericardial sinus and is equipped with segmen-
tally arranged alary muscles; see below) and dorsally attached to the cuticle through a series
of elastic ligaments. Two distinct heart forms are observable in Crustacea. Most taxa display a
os
os
anterior
lateral ca
A B
h my
dd g
anterior
C D lateral
aa ca os pa
E
os my
h
os
dd
F os G
Fig. 14.1.
Form and structure of hearts in crustaceans. (A and B) Volume rendering of a semithin sectioning
series (from Wirkner and Richter 2008, with permission from Elsevier): Tanais dulongii (Malacostraca,
Tanaidacea), internal view (A), and Leucon nasica (Malacostraca, Cumacea), oblique frontal view (B). (C
and D) Meganyctiphanes norvegica (Malacostraca, Euphausiacea) (from Huckstorf and Wirkner 2011, with
permission from Elsevier): semithin cross section (C) and corrosion cast showing lumen of the heart (D).
(E) Squilla mantis (Malacostraca, Stomatopoda). Dashed line indicates level of cross section in Fig. 14.5C
(redrawn from Alexandrowicz 1932). (F) Heart of Calanus finmarchicus (Copepoda) (redrawn from Lowe
1935). (G) Astacus astacus (Malacostraca, Decapoda) (redrawn from Baumann 1921). Abbreviations: aa,
anterior aorta; ca, cardiac artery; dd, dorsal diaphragm; g, gut; h, lumen of the heart; my, myocardium; pa,
posterior aorta; os, ostium.
heart equipped with a spirally or circularly arranged myocardium forming a contractile tube.
This form is known as a tubular heart. In Euphausiacea and Decapoda, however, the myocar-
dium is more complex, forming a meshwork of muscular strands, some of which also run through
the lumen of the heart. Apart from this, hearts can vary in thickness and distinctness of the myo-
cardium, in length, and in the number of pairs of ostia and pairs of cardiac arteries.
Most crustaceans have tubular hearts of varying lengths. In a number of taxa, the heart
extends through most of the trunk. The longest hearts occur in Anostraca (Branchiopoda) and
Stomatopoda (Malacostraca; Fig. 14.1E) and are equipped with segmentally arranged pairs of
ostia. However, while the heart in Notostraca is described as a thin, transparent, contractile
tube, the myocardium in stomatopods is made up of two prominent layers of muscle cells. The
heart in Anostraca is also described as a thin, transparent tube, but ultrastructural studies have
shown that only the posterior end of the heart is tubular, while in the more anterior segments the
myocardium is U-shaped with the ends of the “U” attached to the dorsal integument (Økland
et al. 1982).
Other taxa exhibit hearts that extend only through most of the thorax. In most Tanaidacea,
for example, the heart extends from the third thoracic segment into the seventh or eighth tho-
racic segment. The myocardium is made up of spirally arranged muscle cells (Fig. 14.1A) and is
equipped with three pairs of ostia. The heart is even shorter in Cumacea and has therefore been
interpreted as being globular (see below). However, although the muscle bands run in different
directions (Fig. 14.1B), they are always arranged in a tube shape and therefore also resemble a
tubular heart.
The shortest tubular hearts occur in Thermosbaenacea. Short and dumbbell shaped, they
extend through just over one segment and measure only a few hundred micrometers in length.
In the anterior bulb (maximum diameter ~ 100 μm), the myocardium is made up of a number
of muscle cells that diverge starlike from a point in the ventral heart wall. Two incurrent ostia
are laterally situated in the anterior bulb. Similarly short hearts are present in some Branchiura,
Copepoda, and some Ostracoda, but in the latter two groups most representatives lack hearts,
as do Mystacocarida, Ascothoracida, and Cirripedia. The heart in the copepod Calanus finmar-
chicus takes the form of an elongated ovoid sac (Fig. 14.1F) situated beneath the dorsal body
wall of the second and third thoracic segments (Lowe 1935). It has four openings—an anterior
aortic valve situated anteroventrally and three incurrent ostia. These short hearts are sometimes
termed globular hearts (e.g., Mayrat et al. 2006) and thus homologized with decapod globular
hearts. However, as the myocardium resembles that of tubular hearts, we advocate the term short
tubular hearts.
Decapods (Fig. 14.2) and euphausiaceans (Fig. 14.1C,D), on the other hand, exhibit signifi-
cantly different myocardial arrangements. The heart in these groups is a short, globular organ
located in the posterior part of the cephalothorax (Balss 1940–1961, Huckstorf and Wirkner 2011,
S. Scholz, S. Richter, and C.S. Wirkner, unpublished observations). The heart muscles are not
arranged peripherally, as in tubular hearts, but form a meshwork of fibers running through the
interior of the heart creating cavities without muscle bands and regions with dense networks
(Fig. 14.1C,D,G). The number of pairs of ostia varies. Within Decapoda, three or five pairs of
ostia occur (Balss 1940–1961, S. Scholz, S. Richter and C.S. Wirkner, unpublished observations),
with five most probably being the ground pattern state. In Euphausiacea, two pairs of ostia are
present, although three pairs have been reported for some species (for a discussion of data, see
Huckstorf and Wirkner 2011).
From a phylogenetic point of view, it can be assumed that a tubular heart extending through
the greater part of the trunk was already present in the ancestor of Malacostraca and in that of
Branchiopoda. From a comparison with other Arthropoda, it can be clearly stated that this repre-
sents the plesiomorphic condition. The shortening of the heart took place within Branchiopoda.
1 2 3
2
3
o
fl pa
aa 1
ala
2
3
da
Fig. 14.2.
Scenario of the evolutionary condensation of the decapods globular heart, after Wilkens et al. (1997).
The original drawing has been redrawn to visualize the backward shift of the decapod heart that is
assumed in this scenario (compare Wilkens et al. 1997, their fig. 6). Redrawn from Wilkens et al. (1997).
Abbreviations: aa, anterior aorta; ala, anterior lateral arteries; da, descending artery; f l, f lap; o, ostia;
pa, posterior aorta.
While Anostraca and Notostraca have hearts that run through most of the trunk segments, the
heart in Conchostraca spans only three to four segments, and all that remains in Cladocera is
a short tubular heart. The length of the heart also changed somewhat within the Malacostraca
(see above), with a shortening taking place in various taxa. However, the evolutionary process
behind this is not wholly clear. The shortening might have been the consequence of either a
demuscularization of parts of the longitudinal tubular heart or the shortening of the heart proper
and the simultaneous prolongation of the anterior and/or posterior aortae (for discussion, see
also Mayrat et al. 2006). Wilkens et al. (1997) suggest a combination of both mechanisms for the
evolution of the decapod globular heart based on their study of the American lobster (Homarus
americanus). They view the lobster heart as having been derived, via condensation and muscular
specialization, from the first three segments of a tubular heart that folded to describe a dorsov-
entral S-shaped bend (Fig. 14.2). Although it is highly speculative, the scenario envisions the
inclusion of a number of ancestrally segmentally arranged pairs of ostia and arteries. However,
it leaves a number of questions open, such as the explanation of the specialization of the myocar-
dium, which forms a network of muscles running transversally (Fig. 14.1G), and the bend is not
evidenced by observation in any species studied so far.
Ultrastructure of the Myocardium
The ultrastructure (i.e., the cellular and subcellular composition) of the myocardium has been
described in a number of crustacean species belonging to all major lineages (for summaries,
see Tjønneland et al. 1987, Nylund and Tjønneland 1989). Each heart muscle cell is surrounded
by a cell membrane known as the sarcolemma (Fig. 14.3, sl). The sarcolemma displays a sys-
tem of distinctly arranged invaginations that are termed transverse and longitudinal tubules
(Fig. 14.3, Tz and LT tubules). Within each heart muscle cell, each myofibril is surrounded
mf
sr
Tz
bm
m
AI
M H
sl
Fig. 14.3.
Schematic of myocardial ultrastructure in Malacostraca (redrawn from W ägele 1992). Abbreviations: AI,
AI level of the sarcomere; bm, basal membrane; H, H level of sarcomere; LT, longitudinal tubule; m, mito-
chondrium; M, M level of sarcomere; mf, myofibrils; sl, sarcolemma; sr, sarcoplasmatic retuiculum; Tz,
transverse tubule; Z, Z level of the sarcomere.
by a fenestrated sarcoplasmatic reticulum (Fig. 14.3, sr). The two membrane systems (sarco-
lemma and sarcoplasmatic reticulum) interconnect at specific points in the cell, termed cou-
plings, where ions and action potentials are exchanged. The membrane systems function during
the contraction of the heart cell by transmitting the action potential into the cell (transverse
and longitudinal tubules) and storing Ca+ ions necessary for muscle activation (sarcoplasmatic
reticulum) (Nylund and Tjønneland 1989). The muscle cells are always striated, which means
that distinct H, AI, M, and Z bands can be observed (see Fig. 14.3). There are, however, vari-
ations in the ultrastructure of the heart myofibers in species from different crustacean taxa.
Eumalacostracans all have well-developed membrane systems. Couplings are present at the
AI level in Isopoda and at the H level in the remaining Malacostraca. The Z material is always
arranged in thin Z lines, and an M line is present in all malacostracans except Tanaidacea. The
membrane systems and the organization of the Z material seem not to be affected by differ-
ences in body size (large vs. small species) or ecological preferences (limnic, terrestrial, and
marine species; Nylund and Tjønneland 1989). A tubule system is present in all crustacean
heart myofibers, even in myofibers where the diameter of the cell is small and the presumed
functional need for such a system is not obvious.
Circulatory Cycle and Heart Function
Hearts are central pumping organs. When the heart contracts, hemolymph is driven through
the vascular parts—however developed they may be—of the circulatory system. In combina-
tion with a sucking action (hemolymph is sucked into the heart through slitlike openings, the
ostia; see below), this affects hemolymph movement throughout the whole body. The crusta-
cean heart can therefore generally be described as a suction-force pump (Maynard 1960).
The complete turnover of hemolymph in the crustacean body cavity is described as the cir-
culatory cycle (Fig. 14.4). We begin the description of the circulatory cycle at the point at which
hemolymph enters the heart through the ostial openings of the myocardium during diastole.
pa
ss
he
os
dd
aa
ep/b
g
pp
Fig. 14.4.
Schematic of a generalized circulatory cycle in crustaceans. Solid arrows indicate hemolymph flow in
sinuses and lacunae; dashed arrows indicate flow inside vessels. Abbreviations: aa, anterior aorta; c, cara-
pace; dd, dorsal diaphragm; ep/b, epipodite/branchiae; g, gut; he, heart; os, ostium; pa, posterior aorta;
pp, podopericardial sinus; ss, suspending strand.
Hearts are elastically attached to the dorsal cuticle and the dorsal diaphragm (Fig. 14.4, ss, dd;
see also Fig. 14.7B,C, below).
The energy stored in the suspending strands during systole combined with the contraction
of the alary muscles causes the lumen of the relaxing heart to enlarge, and negative pressure
forces hemolymph into the heart. After the full relaxation of the heart, the ostial openings are
closed through neuronal control, and the systole of the myocardium starts. When hemolymph
pressure inside the heart exceeds the pressure inside the cardiac arteries, valves at the bases of
the cardiac arteries will open, and the hemolymph leaves the heart through the arteries. In most
species, at least one artery emanates from the heart proper: the anterior aorta (see below). In
Malacostraca, which have extensive arterial systems, the hemolymph passes from major arteries
into a series of smaller secondary arteries, distributing the hemolymph to various organs and
tissues. Some of these distribution networks, for example, those in the decapod central nervous
system (Fig. 14.5E), can reach levels of complexity comparable to those in vertebrates. However,
the complexity of the distribution network varies among organs, with the hepatopancreas and
muscles being almost as well supplied as the nervous system. It is known from chelicerates that
distribution networks in the muscles can reach oxygen delivery efficiencies comparable to those
in vertebrates (Paul et al. 1991). The elasticity of arteries is reported to be quite high (McMahon
et al. 1997), and some sort of windkessel effect has been discussed at least for major arteries
(Wilkens et al. 1997). As stated above, all arteries have open endings from where hemolymph
enters the body cavity. The distribution cycle continues with the hemolymph irrigating the vari-
ous tissues and organs and then collecting in sinuses leading to either the gills or other respi-
ratory structures such as the branchiostegal lungs in terrestrial brachyuran crabs. After being
oxygenated (see “Respiratory Systems”, below), the hemolymph in most cases is channeled
os
pa he
aa
he
os
ca
ala
aa
da
vv B
h va
ca
g
D
50 μm
350 μm F
Fig. 14.5.
Arterial systems in Malacostraca. (A) Schematic of the hemolymph vascular system in Lophogaster typicus
(Lophogastrida). Arteries into the antennae are depicted by broken lines. Abbreviations: aa, anterior aorta;
ala, anterior lateral arteries; ca, cardiac artery; da, descending artery; he, heart; os, ostium; pa, posterior aorta;
vv, ventral vessel (modified from Wirkner and Richter 2007a). (B) Schematic of the hemolymph vascular sys-
tem in Spelaeogriphus lepidops (Spelaeogriphacea). Arteries into the antennae are depicted by broken lines.
Abbreviations: aa, anterior aorta; he, heart; os (modified from Wirkner and Richter 2007b). (C) Semithin
cross section through the heart and a pair of lateral cardiac arteries in Gonodactylaceus falcatus (Stomatopoda),
as shown in Fig. 14.1E. Abbreviations: ca, cardiac artery; g, gut; h, lumen of the heart; va, valve. (D) Complete
corrosion cast of the hemolymph vascular system in Paralomis granulosa (Lithodidae; Decapoda) to visualize
complexity of arterial systems in Decapoda (original by Jonas Keiler, Rostock, Germany). (E) Horizontal sec-
tion through the brain of Cherax destructor (Decapoda) visualizing dense arterial supply of the brain. Vessels
were injected with black ink prior to sectioning (from McMahon and Burnett 1990, with permission from the
University of Chicago Press). (F) Corrosion cast of the posterior aorta of the marbled crayfish (“parthenoge-
netic form” of Procambarus fallax) (Decapoda) (original by Stephan Scholz, Rostock, Germany).
through sinuses into the pericardial cavity, from where it reenters the heart through the ostia,
thus finishing the circulatory cycle.
Different heart morphologies produce varying patterns of systole. In the extended tubular
hearts in Branchiopoda, the myocardium contracts simultaneously over its whole length. Within
Malacostraca, only very few data are available on the subject. In the lophogastrid Gnathophausia
ingens, the myocardial contraction starts in the middle of the heart and proceeds in both direc-
tions (Belman and Childress 1976), thus generating a two-way flow that causes hemolymph to
leave the heart through both the anterior and the posterior aortae (and the lateral cardiac arteries).
In globular hearts, myocardial contraction forces hemolymph centrifugally into the various arte-
rial systems.
The central role of the heart in circulation requires a high degree of control. However, the
scarce information on the interconnections among regulation, control, and performance is gath-
ered from a few decapods and isopods. Generally, heart beat frequencies vary greatly according
to situation and physiological conditions. They are influenced both extrinsically and intrinsi-
cally by various factors. The main extrinsic factor is temperature. Within an ecological range,
rising temperatures will lead to higher heart beat frequencies (Schwartzkopff 1955, McMahon
et al. 1997). Changes in heart beat frequency against temperature are interpreted as changes
in metabolism in the pacemaking structures. However, physiological adaptation allows crusta-
ceans to compensate for slow temperature increase over a long period (Schwartzkopff 1955). It is
quantitatively known that the hearts of smaller species beat relatively faster, but this is difficult
to demonstrate in crustaceans, whose heart rate, in contrast to that of homoeothermic animals,
is subject to more complex correlations (e.g., temperature). Nonetheless, in a generalized com-
parison of species belonging to distantly related taxa such as cladocerans, isopods, amphipods,
and decapods, heart rate does tend to decrease as body mass increases. Intrinsically, heart beat
is controlled and regulated by nervous and hormonal influences. Heart rate in vivo is strongly
influenced by input from the ventral nerve cord via cardioregulatory nerves entering the heart
(e.g., Wilkens and Walker 1992, Guirguis and Wilkens 1995). The ventral nerve cord (i.e., the
nervi cardiaci dorsales) functions as a regulatory system in either accelerating or decelerating
the heartbeat and in modifying its amplitude (Wilkens and Walker 1992). Although heart rate is
clearly influenced by the factors mentioned above, heart stroke volume can vary independently
(for reviews, see McMahon and Wilkens 1983, McMahon et al. 1997). An interesting aspect is
that temperature change affects heart rate via metabolic effects on the nervous system (i.e., cen-
tral nervous system and/or dorsal heart nerve) but that stroke volume is unaffected, respond-
ing instead to factors related to metabolic demand within the animal (e.g., McMahon 1999). It
thus seems probable that heart rate and stroke volume are also controlled separately, at least in
decapod crustaceans.
Arterial System
As in most arthropod groups, there is a correlation between the presence and complexity of
arterial systems and the size of the animal. In small animals, a tendency toward a reduction of
artery numbers and branching pattern complexity is evident. There are exceptions, however.
For example, in Malacostraca (where the most complex arterial systems occur), small tanaid-
aceans exhibit the same number of arteries as their larger counterparts.
When it comes to the structural distinction of arteries, some features pose terminological
problems. In some taxa, arteries run into distinct tissues such as the brain, and in this case the
wall of the anterior aorta merges with the perineurium, the connective tissue surrounding the
brain; it is not clear whether to call the merging part of the aorta an artery or simply a hemol-
ymph channel. Another example occurs in Cumacea, where the anterior aorta approaches the
anterior part of the stomach chamber and the ventral part of the aorta becomes confluent with
the dorsal stomach wall.
At least one artery, the anterior aorta, emanates from the crustacean heart. Exceptions
are found in the ostracods, where the anterior part of the heart takes the form of an excurrent
he
va
m
sd
st maf c
st
maf a
br
m
A oed B C 100μm
D
maf b
oa mob
aa
maf a
maf b
ba
100μm E 50μm
Fig. 14.6.
Myoarterial formations in Malacostraca. (A and B) Generalized functional scenario of the myoarterial
formation a (maf a) in peracarids (modified from Wirkner and Richter 2007b): myoarterial formation a
with relaxed esophageal (oed) and stomach dilator (sd) muscles (A) and myoarterial formation a with con-
tracted esophageal and stomach dilator muscles (B). See text for functional details. (C) Horizontal semi-
thin section through the myoarterial formation c (maf c) in Neomysis integer (Mysida) (from Wirkner and
Richter 2007a, with permission from Wiley). (D) Corrosion cast of the anterior aorta in Lophogaster typi-
cus (Lophogastrida) visualizing the myoarterial formations a and b (maf a, b) (from Wirkner and Richter
2007a, with permission from Wiley). (E) Horizontal semithin section through the myoarterial formation
b (maf b) in Lophogaster typicus (Lophogastrida) (from Wirkner and Richter 2007a, with permission from
Wiley). Abbreviations: aa, anterior aorta; ba, brain artery; br, brain; he, heart; m, mitochondrium; maf a,
myoarterial formation a; maf b, myoarterial formation b; maf c, myoarterial formation c; mob, musculus
oculo basalis; oa, optical artery; oed, esophageal dilator; sd, stomach dilator; st, stomach; va, valve.
ostium. In the cephalocarid Hutchinsoniella macracantha, Hessler and Elofsson (2001) reported
an anteriorly closed heart that must by definition lack an anterior aorta. Some Copepoda, most
Branchiopoda, Bathynellacea, Thermosbaenacea, Spelaeogriphacea, and Mictacea possess only
this one artery. The only taxon within Crustacea that displays paired lateral cardiac arteries
emanating from the heart is Malacostraca.
All arteries have valves at their origin to ensure a one-way flow of hemolymph out of the
heart (Fig. 14.5C; labeled va in Fig. 14.6A). Cardioarterial valves contain innervated muscle
(Alexandrowicz 1932, Kuramoto and Ebara 1984, Kihara and Kuwasawa 1984) and can be induced
by either neural or neurohormonal stimulation to contract progressively so as to restrict cardiac
outflow into a particular vessel. Since the valves of the different arterial systems are innervated
separately, this provides a mechanism by which the outflow of the heart can be diverted into
particular arterial systems and thus to particular body regions (McMahon 2001).
Only very scarce information is available on the fine structure of crustacean arteries.
According to Chan et al. (2006) and Wilkens et al. (2008), lobster arteries display trilaminar
organization. The inner layer is formed by elastic connective material; the outer layer, by col-
lagenous connective material with intercalated fibroblastic cells; and the middle layer is an
aggregation of cells containing microfilaments. Arterial cells contain actin, myosin, and tro-
pomyosin. In Decapoda at least, striated muscle cells are present only in the posterior aorta
(Wilkens et al. 2008). In the following, the main arterial systems are introduced (see Fig. 14.5):
the anterior aorta, the posterior aorta, the lateral cardiac arteries, and the ventral vessel system
(which comprises the descending artery and the ventral vessel).
The anterior aorta is an always unpaired artery emanating from the anterior end of the heart.
It leads into the cephalic region, where it supplies the brain, eyes, and, in some cases, head append-
ages such as the first and second antennae and the labral hemocoel. Within Malacostraca, the
anterior aorta system can be complex, displaying several secondary branches, forming pericer-
ebral rings, or having visceral muscles internalized, thus forming myoarterial formations (Figs.
14.5A,B, 14.6A,B,D,E; see below).
A posterior aorta has been described for a number of malacostracan species. Further com-
parative investigation is needed to clarify if the posterior part of the heart in the cephalocarid
Hutchinsoniella macracantha, which is said to “telescope into the dorsoposterior channel”
(Hessler and Elofsson 2001), can be homologized to the posterior aorta in Malacostraca.
In most taxa, the posterior aorta is an unpaired artery emanating from the posterior end of
the heart. A posterior aorta is missing in Spelaeogriphacea, Mictacea, Cumacea, Tanaidacea,
and Isopoda. In Decapoda (Fig. 14.5F), Lophogastrida (Fig. 14.5A), and Mysida, lateral pairs of
arteries branching off the posterior aorta in each pleonal segment supply the pleonal muscula-
ture (and organs) and the swimmerets. The posterior aorta in Decapoda is the only artery con-
taining striated muscles. This and the fact that all lateral arteries off the posterior aorta exhibit
innervated valves at their bases gave rise to the evolutionary hypotheses that the posterior aorta
in Decapoda constitutes a transformed part of the formerly tubular heart (see also Fig. 14.2). In
Euphausiacea, a pair of cardiac arteries leads into the pleon. Taube (1914) observed the devel-
opment of these arteries from unpaired anlagen and therefore termed them “paired posterior
aortae.”
Lateral cardiac arteries are only present in Malacostraca. But also within Malacostraca,
complexity of these arterial systems varies greatly, from taxa in which lateral cardiac arter-
ies are missing entirely (Fig. 14.5B; Bathynellacea, Spelaeogriphacea, Mictacea, and
Thermosbaenacea) to taxa with just a few only slightly branching pairs of arteries (e.g.,
Amphipoda and Tanaidacea), to Decapoda, whose few pairs of arteries display highly complex
branching patterns reminiscent of vertebrate capillary beds (Fig. 14.5D,E). Stomatopoda (Fig.
14.1E), Leptostraca, and Anaspidacea exhibit, at least to some extent, the plesiomorphic condi-
tion of segmentally arranged pairs of cardiac arteries. The cardiac arteries lead to two main
destinations. In Leptostraca, Decapoda, Euphausiacea, Lophogastrida, Mysida, Amphipoda,
and Tanaidacea, the cardiac arteries supply visceral organs such as the gut and the gonads,
while in Isopoda, Cumacea, and Stomatopoda, the main stems of these arteries run into the
thoracopods. However, in the latter three taxa, branches also supply the viscera. A special case is
described for the Anaspidacea, where few anterior cardiac arteries supply viscera while the more
posterior pairs of cardiac arteries supply the pleopods (Siewing 1954). In Tanaidacea, Cumacea,
and Isopoda the last pair of cardiac arteries runs into the pleon, most probably compensating for
the lack of a posterior aorta.
A descending artery (Figs. 14.2, 14.5A; often confusingly referred to as a “sternal artery”;
see below) is an artery that emanates ventrally from the heart and connects to the ventral ves-
sel and is present only in Malacostraca. It is normally greater in diameter than other cardiac
arteries. A descending artery occurs in Decapoda, Euphausiacea, Anaspidacea, Lophogastrida,

and Mysida. However, some details vary intra- and/or interspecifically (for more information,
see Wirkner and Richter 2007a, and Vogt et al. 2009). First, the descending artery can be either
symmetric, that is, a pair of arteries connecting to the ventral vessel, or asymmetric, that is, the
more prominent of a pair of cardiac arteries (the smaller of the pair generally supplying viscera
in the trunk). Second, asymmetric descending arteries can be found on either the left or the
right side of the body (intraspecific variation; see below). Third, their segmental position may
vary in different taxa between the sixth, seventh, and eighth thoracic segment.
At present, nothing is known about the mechanisms that establish and maintain bilat-
erally symmetric descending arteries or the mechanisms involved in symmetry breaking
(Vogt et al. 2009). Based on developmental observations, it appears likely that a symmetric
descending artery can be converted into an asymmetric one through the degeneration of
either of the two dorsal branches during later development but that the reverse process is
highly improbable. This question needs to be investigated in greater depth. Despite the evi-
dent variation in the descending artery system, it is likely that it evolved only once within
Malacostraca.
A ventral vessel is described for several malacostracan taxa. In Stomatopoda, Decapoda,
Euphausiacea, Lophogastrida (Fig. 14.5A), Mysida, and some Isopoda, it runs along the ventral
side of the nerve cord (in which case it is termed a subneural vessel), while in Anaspidacea the
anterior part extends above the nerve cord (in which case it is termed a supraneural vessel; see
below). The stomatopod ventral vessel runs through the whole body and is connected to the
dorsal vessel via a number of shunts (rami communicantes) branching off from the cardiac arter-
ies. Its function is to supply the ventral nerve cord (Siewing 1956). The ventral vessel described
for some isopods (Silen 1954) shows some similarities to that of stomatopods but is a structure
acquired independently within Isopoda (see Wirkner and Richter 2004). In the remaining taxa
(Decapoda, Euphausiacea, Anaspidacea, Lophogastrida, and Mysida), however, the ventral
vessel is connected to the dorsal vessel via the descending artery (see above) and supplies the
thoracopods (and mouthparts). The part that extends anteriorly from the descending artery is
termed the sternal artery, while the part that extends posteriorly is termed the caudal artery. In
Anaspidacea, the sternal artery runs above the nerve cord, while the caudal artery pierces the
ventral nerve cord. This led Siewing (1956) to interpret the ventral vessel in Anaspidacea as hav-
ing evolved independently. We prefer to homologize it with the sternal arteries in Lophogastrida,
Mysida, and Euphausiacea, because it also supplies the thoracopods (via arteries that run down
between the connectives) and is connected to the descending artery.
A subneural ventral vessel supplying several appendages that is connected to the heart
through a descending artery evolved only once within Malacostraca. Further investigation is
required to establish whether the ventral vessel in Stomatopoda is homologous to the ventral
vessel in the other taxa.
Accessory Pumping Structures (Myoarterial Formations)
In some cases, the hemolymph pressure produced by the heart does not seem to be strong
enough to supply all the tissues or regions in the crustacean body sufficiently. To overcome this,
secondary pumping structures have developed. Although there are many accounts in the lit-
erature, and many textbooks show aortic dilations that they term cor frontale (e.g., Gruner 1993,
Brusca and Brusca 2003), detailed information (morphological or functional) is scarce, and no
comprehensive survey has ever been carried out. The most common accessory pumping struc-
tures are myoarterial formations, associations between different parts of the anterior aorta and
internalized muscles in the cephalothorax. These units are functionally interpreted as acces-
sory pumping structures because it is believed that the intrinsic muscles might act as pumping
motors. Myoarterial formations of this nature have been described in Ostracoda, Copepoda,
and Malacostraca, though data on the first two taxa are scarce and have never been confirmed.
Comparative morphological studies (Wirkner and Richter 2003, 2007a, 2007b, 2007c, 2008,
2009, 2010) in combination with the older literature point to three different kinds of myoarterial
formation in Malacostraca:
1. Myoarterial formation a: an aortic dilation within which the esophageal dilator muscles
are internalized (Fig. 14.6A,D). It is so far described only in peracarid species, and further
investigations are needed on additional malacostracan taxa.
2. Myoarterial formation b: an aortic dilation through which the musculi oculi basales poste-
riores run (Fig. 14.6D,E). This is the cor frontale described in Decapoda, Euphausiacea, and
Lophogastrida.
3. Myoarterial formation c: a voluminous dilation of the anterior aorta with internalized
stomach musculature posterior to the stomach chamber and found only in Mysida (Fig.
14.6C; Wirkner and Richter 2007a).
On the basis of the functional-morphological scenario proposed by Huber (1992), we

suggested a functional model for Mictocaris halope (Mictacea) (Wirkner and Richter 2007b).
This scenario can be extended to at least all peracarid taxa in which a myoarterial formation
a has been found (see Wirkner and Richter 2010). When the dilator muscles of the esopha-
gus and stomach are relaxed, hemolymph is pumped into the aortic dilation by the heart
(Fig. 14.6A). When the esophageal and stomach dilator muscles contract, the space between
the brain and the foregut is narrowed (Fig. 14.6B). Because the backward movement of hemo-
lymph toward the heart is prevented by the valve at the transition between the heart and the
anterior aorta, the hemolymph is pumped into the brain artery and the arteries leading into
the antennae and the labrum.
Hemolymph Lacunar System
The terms sinus and lacuna are usually used, respectively, to differentiate between hemolymph
spaces definitely bordered by a membrane and those that are formed by distinct spaces between
organs and therefore are not bordered by a uniform structure. Crustacean hemolymph passes
from arteries into interstitial lacunae and then into sinuses (Fig. 14.7A,C). The most definitively
enclosed sinuses are the branchiopericardial and/or podopericardial sinuses (Fig. 14.7B,D;
often referred to as veins) and the pericardial or dorsal sinus. The pericardial sinus is confined
by the dorsal diaphragm (or pericardial membrane) and the dorsal cuticle (Figs. 14.1C,F, 14.4,
14.7B,C). Using the analogy of the vertebrate heart, it has been interpreted as a second heart
chamber (e.g., McMahon and Burnett 1990). The podopericardial sinuses channel hemolymph
out of the legs (and gills) and into the pericardial sinus and therefore play a major role in respi-
ration (see below). They are confined by a connective tissue membrane that is attached to the
lateral cuticle. In decapods, the walls of the podopericardial sinuses may make up of two distinct
layers: an intima and a layer of endothelial cells similar to those of the arterial walls. In the
Thoracica, a channel system is often well developed, but these are nevertheless usually consid-
ered to be blood sinuses rather than vessels. Their walls are apparently formed from parenchy-
matous connective tissue cells and interlacing fibers (Cannon 1947).
Generally, sinuses interconnect but are often divided for a greater or lesser portion of their
length by membranes or septa (Fig. 14.7A). Such septa usually run the length of appendages
(legs or gills) and thus divide the hemolymph space of the limb into two channels (Fig. 14.7C).
Mostly, hemolymph passes into them from various lacunae, and in only a few taxa these are
additionally supplied through arterial branches (Fig. 14.7C). Since one of the channels usually
se
h dd
aa he
pp
g
B 100μm
h
dd
pep
dep
vv
ep
C D 200μm
Fig. 14.7.
Sinuses and lacunae. (A) Hemolymph lacunar and vascular system in Leptodora kindtii (Branchiopoda,
Cladocera). Arrows depict distinct flow patterns in the lacunar system. Abbreviations: aa, anterior aorta;
he, heart; se, septum (redrawn from Saalfeld 1936). (B) Semithin cross section through a thoracic segment
in Tanais dulongii (Malacostraca, Tanaidacea) showing a podopericardial sinus (pp) merging into the peri-
cardial sinus. Abbreviations: dd, dorsal diaphragm; g, gut; h, lumen of the heart (from Wirkner and Richter
2008, with permission from Elsevier). (C) Hemolymph flow (arrows) in a thoracic segment in Anaspides
tasmaniae (Malacostraca, Anaspidacea). Dashed arrows are arrows covered by cuticle. Dashed circles
indicate insertion sites of proximal (pep) and distal (dep) epipodites (see Fig. 14.8C). Abbreviations: dd,
dorsal diaphragm; vv, ventral vessel (redrawn from Siewing 1959). (D) Corrosion cast of the epipodites
(ep) and podopericardial (p) sinuses in Lophogaster typicus (Malacostraca, Lophogastrida). Compare with
Fig. 14.11, A and B.
opens into the lower pressure region of the pericardial sinus, and the other into the ventral sinus,
fluid flow along the pressure drop in the limb is assured (Fig. 14.7C). In certain Amphipoda, the
appendage septum may be a direct continuation of the pericardial septum, and in decapod gills,
they can become quite complex (see Fig. 14.10E, below). In flattened gill plates, the essentially
continuous septum is replaced by a lacunar network in which the oxygenation of the hemol-
ymph occurs (see below).
Hemolymph and Hemocytes
The blood of crustaceans, more properly termed hemolymph, consists of the circulatory fluid,
or plasma, and numerous blood cells, or hemocytes, that are suspended therein. The blood
cells contain no respiratory pigments, since these are extracellular. Two different respiratory
pigments are present within Crustacea. Hemoglobin occurs in Branchiopoda, Ostracoda,
Copepoda, and rhizocephalan Cirripedia and within Malacostraca only in cyamid amphipods,
while hemocyanin has been described only in Malacostraca (Terwilliger and Ryan 2001). The
structure and function of both pigments are reviewed in Terwilliger and Ryan (2001).
Crustacean hemocytes have typically been classified according to morphological criteria
such as cell size and shape and the presence or absence of cytoplasmic granules. However, it
has been pointed out that hemocytes can be reliably identified only using a combination of
morphological, cytochemical, and functional methods (Hose et al. 1990). Two or three mor-
phological types of hemocyte are generally recognized today: hyaline hemocytes, semi- or
hemigranulocytes, and granulocytes (see Johnson 1980, Bauchau 1981, Martin 1992, Martin
and Hose 1992). The traditional identification method for hyaline hemocytes relies on a lack
(or limited number) of cytoplasmic granules. Granulocytes, on the other hand, contain numer-
ous cytoplasmic granules. Granulocytes are subdivided into those containing relatively small
granules (hemi- or semigranulocytes) and those full of large, refractile granules (Martin 1992).
However, Schmitz (1992) argues that these cell class designations may not be stable for all crus-
tacean forms and may not be completely representative. Controversy also surrounds the func-
tion of hemocytes. On the one hand, hyaline cells are thought to initiate coagulation (Wood
et al. 1971, Ravindranath 1980), while others claim that this is a function fulfilled by the granu-
locytes (Toney 1958, Hearing and Vernick 1967, Madaras et al. 1979). Hyaline cells have been
suggested to be the main phagocytic cells in crustacean hemolymph (Söderhä ll and Smith 1983,
Söderhä ll et al. 1986), while Hose and Martin (1989) demonstrated that phagocytosis is solely a
function of the granulocytes. Apart from the expected functions of clotting and healing, some
authors have attributed them with an additional role in vitellogenesis, at least in Branchiopoda
(Lochhead and Lochhead 1941, see also Martin 1992).
RESPIRATORY SYSTEMS
What Is Respiration?
Respiration, that is, the exchange of the respiratory gases oxygen and carbon dioxide, is based
on two basic features: ventilation and circulation. Externally, the surfaces of the respiratory
structures must be ventilated with a current of the medium (in most cases water, but also air),
and internally the circulation of hemolymph is indispensable for oxygen uptake and carbon
dioxide transport. Respiratory organs such as epipodites and carapaces are therefore integral
parts of the circulatory system, together returning the entire hemolymph f low back to the
pericardium (Fig. 14.4). Respiratory exchange between the medium and hemolymph usually
takes place across a single epithelial and cuticular layer where the gradients are maintained by
ventilation and circulation. Oxygen uptake and carbon dioxide elimination occur by way of
passive diffusion only (McMahon and Wilkens 1983, Taylor and Taylor 1992). The high venti-
lation rates of aquatic gill breathers result from the low oxygen capacitance of seawater (~3%
of the value of carbon dioxide in seawater and ~3% of the oxygen capacitance of air; Dejours
1981). In contrast to fish, however, water-breathing decapods (and probably also other crusta-
ceans) have low ventilation:perfusion ratios, primarily because hemolymph f low is also high,
which is the consequence of the relatively low oxygen-carrying capacity of crustacean hemo-
lymph (see Taylor and Taylor 1992).
Crustaceans are enclosed by a chitinous exoskeleton principally allowing for oxygen dif-
fusion. In some groups with a thin cuticle, the general body surface is therefore a site of res-
piration. In most taxa, however, the thickness, calcification, and sclerotization of the cuticle
exclude the diffusion of gases. Only certain areas of the body surface are lined by a nonmin-
eralized cuticle that is soft and (sometimes extremely) thin to allow for the exchange of the
respiratory gases oxygen and carbon dioxide (see chapter 5 in this volume). These areas are
generally found at the epipodites (from a functional point of view often called gills, but see
below), the inner side of the lateral portions of the carapace (often referred to as branchioste-
gites), and a few other, mostly appendage-correlated structures. The high permeability of these
areas predisposes them not only to respiration but also to osmoregulation. The epipodites and
branchiostegites thus contribute to respiratory, excretory, osmotic, and acid-base homeostasis
(Taylor and Taylor 1992, Freire et al. 2008).
A spatial separation of respiratory and osmoregulatory functions has often been inferred
from differential silver staining of decapod branchiae (Pequeux et al. 1988, Taylor and Taylor
1992). Silver-stained areas indicate that the chloride ions from the tissue were captured as sil-
ver chloride precipitates on the tissue surfaces. In other words, the silver-stained area is highly
permeable to chloride ions. In the crab Eriocheir sinensis (see Taylor and Taylor 1992 for more
details), results generally correlate with regional differences in the ultrastructure of the epi-
thelium. Silver staining correlates to thick (10–20 μm) epithelial cells that display some of the
characteristics of ion-transporting cells, whereas areas that do not stain so intensely exhibit only
thin epithelial cells (total thickness of epithelium including cuticle, 2–5 μm) that are assumed
to be involved in gas exchange via diffusion only. Transmission electron microscopy is the best
way to distinguish between respiratory and osmoregulatory epithelia. Respiratory tissue has
a very thin epithelium and cuticle, as well as fewer mitochondria. An extensively folded mem-
brane system is absent. Osmoregulatory cells are identified on the basis of the presence of the
folded membranes associated with relatively high densities of mitochondria and greater cell
depth (McConnell 1987).
Respiratory Organs: Overview
Specific respiratory organs are absent in Mystacocarida, Copepoda, Remipedia, and most
Cirripedia. When respiratory organs are present, two kinds of structures are particularly
important: the inner side of the carapace and the trunk appendages (epipodites, and in certain
cases, exopods and endopods). A respiratory carapace is present in Ostracoda, Phyllopoda, and
Malacostraca (see chapter 4 in this volume). Respiratory epipodites are present in Malacostraca,
whereas the respiratory function of the epipodites in Branchiopoda is questionable (see below).
In Cephalocarida, the exopods and the pseudepipodites appear to be sites of gas exchange
(Hessler and Elofsson 1992). Respiratory pleopods are known to be present in Isopoda (W ägele
1992) and Stomatopoda (Burnett and Hessler 1973). In Spelaeogriphacea, the exopods of the
thoracopods seem to function as respiratory organs (Grindley and Hessler 1971).
In isopods and certain decapods, periodic aerial exposure in the littoral zone resulted in the
evolution of the ability to breathe air. In Oniscidea (Isopoda), the respiratory structures were
incorporated into the exopods (W ägele 1992), while in certain decapods (e.g., Birgus, Ocypode),
the branchiostegites evolved into lungs (Farrelly and Greenaway 1993, 2005). In Coenobita, the
pleon is the most important site of gas exchange (Farrelly and Greenaway 2005). In some deca-
pods (Ocypodidae, Brachyura, Porcellanidae, and Anomala), even certain areas of the legs
(part of the endopods) evolved into respiratory surfaces (Maitland 1986, Stillman 2000).
Epipodites
The terms epipodites and gills are often used interchangeably, but they actually reflect differ-
ent levels of description (see also Maas et al. 2009). Gill is a functional term that should be
restricted to any outgrowths with respiratory function, bearing in mind that other functions
(e.g., osmoregulation) might also play a role. Exact structure and position are not important
in determining whether a structure can be called a “gill.” Epipodite refers to a structure alone
and contains no information about function. As we discuss below, the respiratory function of
branchiopod epipodites is questionable. To complicate matters further, epipodite is not the only
term used: exite, preepipodite, metepipodite, and pseudepipodite are also commonly used. We
base our terminology on the recent account by Boxshall and Jaume (2009), who use exite as a
general (i.e., taxon and homology-independent) term referring to any outer lobate structure on
the protopodal part of the limb, and epipodite as a specific term referring to a specific structure
found in certain crustaceans for which structural and developmental evidence suggests homol-
ogy (for more details, see Boxshall and Jaume 2009). The presence of epipodites is most obvious
in Malacostraca and Branchiopoda. It seems unlikely, in light of its internal musculature and its
origin on the exopod (Maas et al. 2009, Boxshall and Jaume 2009), that the “pseudepipodite” in
Cephalocarida is homologous with true epipodites. Pseudepipodites probably have a respira-
tory function, as suggested by the connective tissue septa that appear to channel the hemol-
ymph flow in the limbs (Hessler and Elofsson 1992).
With respect to the Branchiopoda, most representatives of the Phyllopoda possess a single
epipodite per limb; only in the cladoceran taxa Onychopoda and Haplopoda are epipodites
entirely absent. In Anostraca, the sister group of Phyllopoda, a single “preepipodite” or a pair
of preepipodites is present in addition to the more distal epipodite. The limbs (or at least the
epipodites) have traditionally been assumed to have a respiratory function, and the constant
rhythmic beating of the thoracic limbs in most taxa has been cited as evidence of the need
to produce a constant flow of oxygenated water over the limb surfaces (Martin 1992). The
name Branchiopoda, meaning “gill footed,” already implies that the limbs, and specifically
the epipodites, are respiratory, but there is evidence that this may be at least partly incor-
rect (reviewed by Martin 1992). In Artemia salina, the cuticle of the epipodites is suitable for
osmoregulation, as demonstrated by silver staining (Holliday et al. 1990). The epithelial cells
underlying the cuticle stained in a reticulated pattern. Copeland (1967) found two cell types in
the epithelium, dark and light cells, and suggested that both types are involved in osmoregula-
tion (see review by Martin 1992). In addition, Artemia certainly does not depend on the pres-
ence of epipodites for respiration, as experiments by Croghan (1958) have shown. Kikuchi and
Shiraishi (1997) take a slightly different view. In the spinicaudatan Caenestheriella gifuensis, they
found that silver staining only correlated to the dark cells. Their suggestion was that only those
cells are involved in osmoregulation, while the light cells are primarily respiratory. Although it
seems quite clear that branchiopod epipodites are indeed the major sites for osmoregulation,
whether a respiratory function can really be excluded remains an open question.
In Malacostraca, epipodites do play a role in respiration, but osmoregulation is also involved.
Several thoracic and presumably respiratory epipodites are present in Leptostraca, Stomatopoda,
Anaspidacea, Euphausiacea, Amphipoda, Lophogastrida, and Decapoda, the latter two possess-
ing additional respiratory structures (branchiae) next to the epipodites as well (see below). The
pleopodal gills in Stomatopoda, however, are unlikely to be serially homologous to epipodites
because of their origin from the central part of the exopods (Boxshall and Jaume 2009).
Interestingly, the cuticle of these gills is even thinner than that of the epipodites (Burnett and
Hessler 1973). Ventilation in Malacostraca is assured by specific mouthparts, by the epipodite of
the first thoracopod (maxilliped), or just by movement of the limbs (Table 14.1).
Leptostraca and Stomatopoda possess a single epipodite on all or several thoracopods,
whereas Anaspidacea and Bathynellacea possess two epipodites per thoracopod (Fig. 14.8A–C).
Lauterbach (1979) suggested that the two epipodites present in Anaspidacea are the result of a
splitting event, an argument supported by the hemolymph current as reconstructed by Siewing
Table 14.1. Epipodites in Malacostraca.
Taxon Epipodites Additional respiratory struc-

tures and their ventilation
Number and position Function (evidence by Ventilation
ultrastructure)
Leptostraca A single flattened and bilobed Probably respiratory (no By metachronic movements of Carapace (Vannier et al. 1997):
epipodite on thoracopods 1–7 ultrastructural evidence) the limbs (also correlated to no ultrastructural evidence—
filter feeding) ventilation as for the epipodites
Stomatopoda A small, single epipodite present Probably respiratory (no Can be waved back and forth Pleopodal gills: no ultrastruc-
only on the thoracopods 1–5, ultrastructural evidence) independently of any other tural evidence
absent on thoracopods 6–8 movement of the limbs (Burnett Ventilation: movement of the
and Hessler 1973) pleopodal gills the result only
of the beating of the entire pleo-
pods (Burnett and Hessler 1973)
Carapace: forms a respira-
tory chamber for epipodites
(Lauterbach 1972); no evidence
for the respiratory function of
the carapace itself
Anaspidacea Two epipodites at the thoraco- Proximal epipodite primarily Movement of thoracopodal Exopod of thoracopod 1 (and
pods 1–7 respiratory, distal one primarily exopods (G. Smith in Calman in Anaspides, Paranaspides tho-
osmoregulatory (ultrastructural 1909) racopod 7) (Siewing 1959)
evidence for Allanaspides hele-
onomus, McConnell 1987)
Bathynellacea Maximum of two epipodites at Probably respiratory (no
thoracopods 1–8 (Bathynella) ultrastructural evidence)
Euphausiacea One bilobed epipodite with Two different regions on the Epipodites not covered by Carapace as indicated by a
fingerlike outgrowths on tho- epipodites, one responsible for the carapace, movement of thin cuticle on its inner side
racopods 1–8. osmoregulation, the other (at thoracopods (Zimmer and Gruner 1956)
Outgrowths increasing in size the periphery of the epipodite
and complexity from anterior to filaments) responsible for
posterior respiration (ultrastructural
At least on the more posterior evidence for Meganyctiphanes
thoracopods, outgrowths divided norvegica and Euphausia superba
into two branches (Sars 1896) by Alberti and Kils 1983)
Decapoda Epipodite-podobranch complex Epipodites (sensu stricto) Scaphognathite Arthrobranchiate,

(in maximum at thoracopods probably not contributing pleurobranchiate
1–7, Balss 1940–1961) significantly to respiration but branchiae (including podo-
fulfilling accessory roles in ven- branchia) respiratory and
tilation, gill maintenance, and, osmoregulatory (Taylor and
at least in crayfish, osmoregula- Taylor 1992)
tion (ultrastructural evidence Carapace (branchiostegites):
by Dunel-Erb et al. 1982) ventilation as for epipodites and
branchiae
Lophogastrida One bilobed complex of what Maxillipedal epipodite probably Maxillipedal epipodite and exo- Carapace (primarily osmoregu-
are assumed to be epipodites only ventilation (no ultrastruc- pod of maxilla in combination latory): ventilation as for
on thoracopods 2–7 (very small tural evidence) (Childress 1971) epipodites (Childress 1971)
one in Gnathophausia on tho- All other epipodites probably
racopod 8) respiratory
Amphipoda A single epipodite on the tho- Respiratory and osmoregula- Ventilation by beating of the Coxal plates (respiratory or
racopods 3–7 (as maximum); tory; ultrastructural evidence pleopods (Dahl 1977) osmoregulatory): no ultrastruc-
the supposed epipodite on tho- for two estuarine amphipod tural evidence
racopod 8 probably representing species: two kinds of epithelia,
an exopod; some amphipods a respiratory epithelium close
having bilobed coxal epipodites to the efferent channel, and an
comprising a small, outer acces- osmoregulatory area close to the
sory lobe, and a large, lamellate afferent channel (Kikuchi and
inner lobe (Steel and Steel 1991) Matsumasa 1993a)
(Continued)
Taxon Epipodites Additional respiratory struc-

tures and their ventilation
Number and position Function (evidence by Ventilation
ultrastructure)
Mysida Only the maxillipedal epipodite Probably only ventilation (no Maxillipedal epipodite (Cannon Carapace (Delage 1883, Wirkner
ultrastructural evidence) and Manton 1927) and Richter 2007a): ventilation
as for epipodites
Mictacea (i.e., None Thin-walled elliptical area dor-
Mictocarididae) sal to carapace (Bowman and
Iliffe 1985)
Cumacea Only the maxillipedal epipodite Probably respiratory (has Movement of the epipodite itself Carapace as indicated by
a region that is folded into (Siewing 1952) complex hemolymph channels
branchial lamellae; see Sars within the carapace (Oelze 1931,
1899–1900, Oelze 1931, Siewing Siewing 1952): ventilation of the
1952) but no ultrastructural carapace (described by Oelze
evidence 1931, Dennell 1937)
Spelaeogriphacea Only the maxillipedal epipodite Probably respiratory and ven- Movement of the epipodite itself Exopods on thoracopods 5–8
tilatory (Grindley and Hessler (Grindley and Hessler 1971)
1971) Carapace: ventilation by maxil-
lipedal epipodite + exopods
(thoracopods 2–4) (Grindley
and Hessler 1971)
Tanaidacea Only the maxillipedal epipodite Respiratory and osmoregula- Movement of the epipodite itself Carapace as indicated by hemo-
tory (ultrastructural evidence lymph channels (Calman 1909,
for Sinelobus stanfordi by Lauterbach 1970) (ultrastruc-
Kikuchi and Matsumasa 1993b) tural evidence of respiratory and
osmoregulatory function for
Sinelobus stanfordi by Kikuchi
and Matsumasa 1993b): ventila-
tion by maxillipedal epipodite
(Lauterbach 1970)
Isopoda Only maxillipedal epipodite Apparently not involved in Pleopods (in most taxa exo-
respiration (W ägele 1989) pod respiratory, endopodite
osmoregulatory): ultrastruc-
tural evidence by W ägele (1992)
In higher Oniscidea, white bod-
ies as dorsal infoldings of the
exopod
Thermosbaenacea Only maxillipedal epipodite Epipodite might be respiratory Maxillipedal epipodite Carapace as indicated by a sys-
(Barker 1962), but no ultrastruc- tem of vascular lacunae in the
tural evidence carapace epithelium that com-
municates with the perivisceral
and pericardial sinuses (Siewing
1958): ventilation by maxilli-
pedal epipodite (Barker 1962)
ep
p
en
ar
ex vs
A B
pep ec
respiratory epithelium
pc
ep
ac cx
bp
ec
en ex
dep
ac
C D
Fig. 14.8.
Hemolymph flow in the epipodites (ep) of different malacostracans. (A) Nebalia bipes (Leptostraca).
en, endopodite; ex, exopodite (redrawn from Claus 1888). (B) Hemisquilla ensigera (Stomatopoda).
Abbreviations: ar, artery; p, pericardial sinus; vs, ventral sinus (redrawn from Burnett and Hessler
1973). (C) Anaspides tasmaniae (Anaspidacea). For attachment site of both epipodites, see Fig. 14.7C.
Abbreviations: ac, afferent channel; dep, distal epipodite; ec, efferent channel; pc, pillar cell; pep, proxi-
mal epipodite (redrawn from Siewing 1959). (D) Lauterbach’s (1979) hypothesis on the evolution of paired
epipodites (ep) per thoracopod by a splitting event as concluded from the hemolymph flow. Note the
opposite hemolymph flows in leptostracan and stomatopod epipodites. Abbreviations: bp, basipodite; cx,
coxa; en, endopodite; ex, expodite (redrawn from Lauterbach 1979).
(1956): afferent channels are present on the ventral margin of the proximal epipodite and on the
dorsal margin of the distal epipodite; efferent channels are found on the opposite margins (Fig.
14.8D). This indeed corresponds to the situation that could be expected to give rise to a splitting
event of a single epipodite. Interestingly, the direction of hemolymph flow corresponds to that
in Stomatopoda, insofar as the median sinus in Stomatopoda is afferent (Burnett and Hessler
1973), but is different from that in Leptostraca, where the median sinus appears to be efferent
(Claus 1888) (Fig. 14.8C). In a detailed study of the epipodites in the anaspidacean Allanaspides
heleonomus, McConnell (1987) found differences between the epithelia in the apical region of the
proximal and distal epipodites, which are associated with respiratory and osmoregulatory func-
tion, respectively. It is interesting to note that Lauterbach (1979) speculated that the duplication
pb
ab
ep
cx
bp
pob
ex
en
Fig. 14.9.
Schematic of the origins of branchiae in decapods (adapted from Hong 1988 and Boxshall and Jaume 2009).
Abbreviations: ab, arthrobranch; bp, basipodite; cx, coxa; en, endopodite; ep, epipodite; ex, exopodite; pb,
pleurobranch; pob, podobranch.
of epipodites in Anaspidacea might be correlated to the loss of the carapace with its respiratory
and osmoregulatory function.
Euphausiacea possess one bilobed epipodite with fingerlike outgrowths on each of the
eight thoracopods. In Bentheuphausia amblyops (probably the sister taxon of all other euphau-
siaceans; Richter and Scholtz 2001), for example, the outgrowths increase in size and complex-
ity from anterior to posterior. On the more posterior thoracopods, the outgrowths are divided
into two branches (Sars 1896). Each of the outgrowths consists of a “trunk” and a number of
filaments with an afferent and efferent channel each (Mauchline 1958, Alberti and Kils 1983).
In Meganyctiphanes norvegica and Euphausia superba, two different regions are present on the
epipodites, one responsible for ionic regulation through active transcellular transport, and the
other, on the periphery of the epipodite filaments, responsible for the gas exchange by diffu-
sion (Alberti and Kils 1983).
Decapoda exhibit the most complex thoracopod exites (epipodites and branchiae) (Balss
1940–1961). They consist of a bilobed structure on the coxa, in which one lobe is lamellate
and referred to as the epipodite (which corresponds to the epipodite of other malacostracans;
Boxshall and Jaume 2009), while the other is more complex, with an outgrowth, and is referred
to as the podobranch. Additional exites (following the terminology of Boxshall and Jaume 2009),
the arthrobranchs, originate in the arthrodial membrane at the articulation between the body
and the thoracopods and are, like pleurobranchs, located on the pleuron, dorsal to the limb
origin (Fig. 14.9). We use podobranch, arthrobranch, and pleurobranch as structural terms only,
rather than gill, which has direct functional implications, and consider each of these structures
to be homologous throughout Decapoda. The distribution of the three kinds of branchiae dif-
fers between taxa and limbs (see Balss 1940–1961). The branchiae and epipodites develop during
the larval stages as series of tubular buds and become structured and ramified later (Hong 1988).
ec
ac
A B C
ac
ac ls
ec
ec
D E F G 100 μm
ac
ac
ec ec
H I J 0.2mm
Fig. 14.10.
Decapod branchiae showing afferent (ac) and efferent (ec) channels. (A–C) Dendrobranchiate branchiae.
(D–G) Trichobranchiate branchiae. (H–J) Phyllobranchiate branchiae. (A) Schematic of a complete den-
drobranchiate branchia (from Gruner 1993, with permission from Springer). (B) Single branchial lamina
(redrawn from Young 1959). (C) Single branchial filament (from Foster and Howse 1978, with permission
from Elsevier). (D) Schematic of a complete trichobranchiate branchia (from Gruner 1993). (E) Schematic
cross section. Arrows indicate hemolymph routes (redrawn from Paterson 1968). (F) Schematic of hemol-
ymph routes through an outer filament. ls, longitudinal septum (redrawn from Rogers 1982). (G) Scanning
electron micrograph of filaments in the marbled crayfish (“parthenogenetic form” of Procambarus fallax)
(Decapoda) (original by Stephan Scholz). (H) Schematic of a complete phyllobranchiate branchia (from
Gruner 1993, with permission from Springer). (I) Schematic of a single lamella. Arrows indicate hemol-
ymph routes (from Barra et al. 1983, with permission from Elsevier). (J) Corrosion cast of single lamella in
Coenobita perlatus (original by Caroline Farrelly).
Based on Taylor and Taylor (1992), three types of ramification appear in Decapoda and permit
further classification (Fig. 14.10). All of them feature a central axis with an afferent and an effer-
ent vessel. In dendrobranchiate branchiae (Fig. 14.10A–C), the primary axis bears secondary
laminae on each side that curve around and touch at their tips. Tertiary elements arise from
the laminae and typically bifurcate at least twice. This type appears in penaeoid and sergestoid
shrimps (Dendrobranchiata). In trichobranchiate branchiae (Fig. 14.10D–G), the central axis
bears numerous fine tubular filaments. The branchiae are bilaterally symmetrical, the filaments
being aligned in transverse rows. This type is found in crayfish, lobsters, rock lobsters, her-
mit crabs, and some Dromiidea among brachyuran crabs. In phyllobranchiate branchiae (Fig.
14.10H–J), the axis is flattened and bears a series of regularly spaced, broad and leaflike lamel-
lae on each side. This type is found in most brachyuran crabs, some anomalans (Galatheidae,
Porcellanidae, Coenobitidae), and caridean shrimps.
From a functional point of view, the three types of branchiae share a basic uniform design.
A longitudinal branchial septum separates the afferent and efferent channels. If hemol-
ymph is to be channeled through the gills and the venous sinuses and into the pericardial
sinuses, the branchial septum must ultimately extend to the pericardial septum (for details
see Taylor and Taylor 1992). Decapod branchiae are also fairly uniform from a histological
point of view. A single-layered epithelium is responsible for respiration and osmoregulation.
Four main types of epithelial cells are recognized: thick cells, thin cells, attenuated cells, and
pillar (or pilaster) cells (Taylor and Taylor 1992). The apical membrane of the thick cells is
strongly folded, thus creating a subcuticular, extracellular space of substantial volume. The
basolateral membrane of these cells forms numerous villi that sometimes extend almost to
the apical membrane. In addition, thick cells contain large numbers of mitochondria that are
often unusually shaped. Cells with this structure are generally involved in osmoregulation.
The thin cells are weakly folded and contain only a few mitochondria, and the basolateral
membrane is only weakly developed. These cells are the main site of gas exchange. Decapod
epipodites probably do not contribute significantly to respiration, but they perform impor-
tant accessory roles in ventilation, gill maintenance, and, at least in crayfish, osmoregulation
(Dunel-Erb et al. 1982).
The mechanism that governs the ventilation of the branchial chamber is similar in all
aquatic decapods (following Taylor and Taylor 1992). The branchiae separate the chamber
into a hypobranchial space adjacent to the thoracic wall and an epibranchial space under the
branchiostegite (the lateral carapace fold). During ventilation, water is pumped forward from
the epibranchial space by the scaphognathite (the exopod of the maxilla), which lies within
the exhalant channels lateral to the mouthparts. Water enters from below through the inhalant
channels between the limb bases.
Within Peracarida, only Amphipoda and Lophogastrida possess a series of epipodites on the
pereopods. In other taxa, a single epipodite is present on the maxilliped (first thoracopod), but
pereopodal epipodites are absent. We exclude the oostegites from our analysis because regard-
less of whether they are homologous to epipodites, they are apparently not involved in respira-
tion (but see Oelze 1931).
In addition to one single epipodite on thoracopods 3–7 (maximum), Amphipoda exhibit flat-
tened outgrowths on the coxae of the pereopods. These “coxal plates” share their developmental
origin with the epipodites (Ungerer and Wolff 2005, Wolff and Scholtz 2008). Functionally, the
coxal plates extend the margin of the pereon ventrolaterally, shielding an inner channel through
which water flows and protecting epipodites and oostegites (Lincoln 1979). However, in
Orchestia cavimana at least, the podopericardial sinuses collects hemolymph from the endopod,
epipodite, and coxal plate, which could indicate that the coxal plate is involved in respiration or
osmoregulation (Wirkner and Richter 2007c). Kikuchi and Matsumasa (1993a) found two kinds
of epithelia in the estuarine amphipod species Grandidierella japonica and Melita setiflagella,
an ordinary respiratory epithelium close to the efferent channel and an osmoregulatory area
close to the afferent channel that exhibited many of the characteristics typical of osmoregula-
tion, including a basolateral cell membrane with frequent lamellar infoldings and many large
mitochondria.
Lophogastrida possess complex structured epipodites on thoracopods 2–8. The epipodites
on the pereopods vary among the lophogastrid taxa. In Lophogaster typicus, for example, an
A 250 μm B 25 μm
cuo
hc hc
cui
cc
C
bc
D E 500 μm
Fig. 14.11.
(A and B) Epipodites in Lophogaster typicus (Malacostraca, Lophogastrida): whole epipodite (A) and detail
(B). (C) Circulation in the carapace: horizontal semithin section through the carapace in Nabalia bipes
(abbreviations: bc, body cavity; cc, carapace cavity; cui, inner cuticle; cuo, outer circle; hc, hemolymph
channel). (D) Schematic of the respiratory carapace in Daphnia pulex. Solid arrows indicate hemolymph
currents; broken arrows indicate water flow produced by thoracopods (redrawn from Pirow et al. 1999b
with permission from the Company of Biologists, Ltd.). (E) Respiratory carapace in Vargula hilgendorfii
Ostracoda (modified from Vannier et al. 1997, with permission from Wiley).
epipodite with two branches is present whose outgrowths are very similar to phyllobranchiate
branchiae in Decapoda (Fig. 14.11A,B). Its position is proximal to the sclerotized coxa, that is,
comparable to the arthrobranchs in Decapoda (compare Haupt and Richter 2008), which might
indicate that the pereopodal exites in Lophogastrida are homologous not to the epipodites
of other malacostracans but to the decapod arthrobranchiae. That discussion, however, goes
beyond the scope of this chapter. The maxilliped (thoracopod 1) carries a well-developed plate-
like epipodite for ventilation, though the exopod of the maxilla is also involved in ventilation.
The respiratory water enters the branchial area midventrally and proceeds laterally and dorsally
through the branchiae.
Mysida, Tanaidacea, Spelaeogriphacea, and Cumacea all lack pereopodal epipodites but
retain a well-developed epipodite on the maxilliped (as is present in Lophogastrida). In most of
these taxa this epipodite is a simple lobe that is considered to be the main structure used in the
ventilation of the respiratory branchiostegite (see chapter 4 in this volume). It has been shown
for one tanaidacean, Sinelobus stanfordi, that the epipodite not only is a respiratory structure
but also is involved in osmoregulation (Kikuchi and Matsumasa 1993b). In Cumacea, the max-
illipedal epipodite can be a complex structure forming a multilobate gill (Sars 1899–1900).
Functionally, it works together with the exopodite, which forms the siphon and maintains
respiratory water flow through the branchial chamber (Oelze 1931, Siewing 1952). Epipodites
are completely absent in Mictacea (i.e., Mictocarididae) and Bochusacea (i.e., Hirsutiidae)
(Bowman and Iliffe 1985, Jaume et al. 2006). Spelaeogriphacea are remarkable in that they pos-
sess what are presumably respiratory exopods on thoracopods 5–8 (Grindley and Hessler 1971).
Isopoda also typically retain the epipodite on the maxilliped, as discussed for other taxa above,
but here it has no functional role in respiration or ventilation. Isopodan pleopods are respira-
tory and osmoregulatory (Alexander and Chen 1989, W ägele 1992). In many aquatic isopods,
the endopod epithelium displays the characteristics typical of osmoregulation, while the exo-
pod epithelium is very thin, thus permitting diffusion of respiratory gases (W ägele 1992). In
general, the same is true for terrestrial isopods, although in Porcellio scaber, for example, the
endopod also exhibits areas with a thin, possibly respiratory epithelium. The “lungs” (white
bodies) of higher Oniscidea evolved within the exopods as dorsal invaginations (Hoese 1982,
W ägele 1992, Schmidt and W ägele 2001).
Carapace
Chapter 4 in this volume provides a detailed account of the structure, development, evolution,
and function of the carapace. We refer in this chapter only to a few aspects related to the partici-
pation of the carapace in respiration, especially with regard to the hemolymph flow. The cara-
pace consists of a thin duplication of the epidermis and its cuticle. The two epidermal layers are
usually attached to each other, leaving a space in which hemolymph circulates. In many cases,
the internal layer of the carapace, that is, the one facing the body, is equipped with a delicate
cuticle only and has been suggested to play a role in respiration (Fig. 14.11C, cui). The external
side of the carapace is strongly sclerotized (Fig. 14.11C, cuo) and often calcified to enable it to
perform its protective function (Gruner and Scholtz 2004).
The inner layer of the carapace has been suggested to have a respiratory function in the
Phyllopoda, though not much detailed information is available for most taxa (Martin 1992).
Interestingly enough, Zaddach (1841) described the hemolymph flow within the carapace folds
in Notostraca as early as the mid-nineteenth century. More recent investigations by Pirow et al.
(1999a, 1999b) show that in Cladocera (exemplified in Daphnia magna) the carapace is indeed
respiratory (see Fig. 4.5A in chapter 4 this volume), with the highest hemoglobin oxygen satura-
tion near the posterior margin of the carapace and in the rostral part of the head.
The inner side of the carapace has also been proposed to be respiratory in Ostracoda (Fig.
14.11D; Fassbinder 1912, Hartmann 1967). According to Vannier et al. (1997), the surface of the
body and the inner carapace lamella suffice to supply the metabolizing organs with oxygen in
the small Podocopida, though an osmoregulatory function has also been demonstrated (Keyser
1990). The rhythmic movements of the respiratory plate (the epipodite of the maxilla) are
responsible for ventilation. Abe and Vannier (1995) also suggested that the inner lamellae of the
carapace are the main site of oxygen uptake in a larger myodocopid species, Vargula hilgendorfii,
for two reasons: afferent circulation is especially active within the posterior half of the carapace
that surrounds the best-ventilated part of the cavity, and the separation created by the inner
lamella between the hemolymph flowing into the sinuses and the seawater is thin enough to
allow rapid gas exchange.
The carapace contains a complex system of sinuses in Malacostraca as well. In Leptostraca,
sinuses in the carapace form an interconnected branching network connected to a thick, mar-
ginal channel that is best developed along the anterior margin of each carapace half. Hemolymph
enters each carapace valve anteriorly between the adductor muscles and the attachment of the
rostrum, takes up oxygen in sinuses, and returns to the pericardial cavity through the dorso-
medial channel (Vannier et al. 1997). Lauterbach (1972) mentioned that the branchiostegites
in Stomatopoda are small and more dorsally placed but still present. They form the respiratory
chamber for the five pairs of epipodites. Whether the branchiostegites are respiratory them-
selves does not seem to be known. In Euphausiacea, the inner side of the carapace possesses a
very thin cuticle and appears to be respiratory (Zimmer and Gruner 1956).
hc
e
A
os he
maf c
Si
Fig. 14.12.
(A) Corrosion cast of the carapace in Lophogaster typicus (Malacostraca, Lophogastrida). e, eye; hc, hemo-
lymph channel. (B) Schematic of the major lacunae, sinuses, and respiratory carapace in Praunus species
(Malacostraca, Mysida). Abbreviations: e, eye; he, heart; maf c, myoarterial formation c; os, ostium; si,
sinus (from Gruner 1993, with permission from Springer).
An interesting claim has been made in relation to Peracarida, with W ägele (1994) and Kobusch
(1999) suggesting that the “respiratory carapace” evolved within Peracarida to replace the per-
eopodal epipodites that are absent in peracarids apart from Lophogastrida and Amphipoda. On
the basis of this, they suggest that Mysida is more closely related to the taxa without pereopodal
epipodites than to Lophogastrida. Indeed, disunity within Mysidacea has been suggested on the
basis of other data sets, too, and although peracarid phylogeny is not the focus of this chapter
(see Wirkner and Richter 2010), the scenario described above does appear to be oversimpli-
fied. Lophogastrida have sinuses in the lateral folds of the carapace (Fig. 14.12A) that are very
similar to those in Mysida (see Delage 1883), and no carapace surface increase can be observed
in Mysida to make up for the lost epipodites (Fig. 14.12B). In addition, ultrastructural investiga-
tions in both taxa (C.S. Wirkner and S. Richter, unpublished observations) point to the carapace
having more of an osmoregulatory function, as Kikuchi and Matsumasa (1993b) also showed in
a tanaidacean, for example. Respiratory and/or osmoregulatory carapaces are also present in
other Peracarida (see Table 14.1).
In Decapoda, the carapace is fused to the entire cephalothorax. Only its lateral portions are
free, and these cover the epipodites and the branchiae. The lateral portions are generally termed
branchiostegites. Not much is known about hemolymph flow in the branchiostegites apart from
a few well-studied brachyuran crabs (see below). For the dendrobranchiate shrimp Penaeus
aztecus, Young (1959) described a large channel (probably afferent) entering the branchiostegite
anterodorsally and branching radially. A second series of parallel channels (probably efferent)
curves around the margin of the branchiostegites and intersects with the first set.
In terrestrial brachyuran crabs and terrestrial hermit crabs (Coenobitidae), the internal
integument of the branchiostegites functions as a lung (defined as the respiratory organ for air
breathing). The branchiae are retained in all taxa, and although their main function appears to
A B
ac
ac p
p ec
ec
C D
Fig. 14.13.
Branchiostegal lungs in Brachyura (Malacostraca). (A and B) Schematics of the lung vasculature in
Ocypode cordimanus (redrawn from Greenaway and Farrelly 1984): afferent (A) and efferent (B) sinuses.
(C and D) Schematics of evaginated lung (C; e.g., Ocypode sp.) and smooth lung (D; e.g., grapsids and
geocarcinids). Left, left branchiostegal lining; upper right, cross section through the carapace; lower right,
relationship between major afferent (ac) and efferent (ec) sinus systems. p, pericardial sinus (redrawn from
Farrelly and Greenaway 1993, 1994).
be osmoregulation, they continue to contribute to respiration (Farrelly and Greenaway 1994,

2005). In the branchiostegites, several circulatory patterns have been identified using corro-
sion casting techniques (Fig. 14.13A,B; Farrelly and Greenaway 1993, 2005). In Brachyura, two
general patterns appear. The simpler of the two is present in Ocypodidae and Mictyridae and
consists of an afferent system that interdigitates with an efferent system (Fig. 14.13C). The blood
passes from one to the other through a single lacunar network located close to the respiratory
surface. In Gecarcinidae, Grapsidae, and Sundathelphusidae, however, the situation is more
complex (Fig. 14.13D): the afferent system is separated from the efferent one by two interdigitat-
ing portal systems (branching networks arising and terminating in a lacunar bed), and blood
passes through three lacunar systems during transit through the lung. The lung circulation
route in both patterns runs parallel to the branchial circulation route, with each lung returning
hemolymph to the pericardium via a large pulmonary sinus (vein) that runs around the perim-
eter of the branchiostegite. Both lung types are very efficient in oxygen uptake (Farrelly and
Greenaway 1994).
The Coenobitidae possess a similar “serial lacunar system” in the branchiostegites, which
obviously evolved convergently to that in brachyurans. In Birgus latro, the only representative
of the terrestrial hermit crabs in which the adults are not shell dwelling, the branchial chambers
are extended and the lung surface is much more elaborate (Harms 1932). The blood/gas diffusion
distance is short, and oxygenated blood is returned directly to the pericardium via pulmonary
sinuses (“veins”) (Farrelly and Greenaway 2005). What is most interesting is that in Coenobita,
an extended pleonal lung is present that is formed from highly vascularized patches of the very
thin and intensely folded dorsal integument. Oxygenated blood from this respiratory surface is
returned to the pericardial sinus via the branchiae (Farrelly and Greenaway 2005). A pleonal lung
of this nature is absent in Birgus, which might have lost it in conjunction with the evolution of a
stronger pleonal cuticle to make up for the “loss” of the shell and replaced it by more extended
branchial chambers.
CONCLUSION
Crustacea display a high degree of morphological disparity, with an astonishing number of dif-
ferent body designs found throughout the different taxa. We hope we have shown, however,
that despite the variety witnessed in respiratory and/or circulatory structures, there is some
common ground.
From a circulatory point of view, all crustaceans have an open vascular system in which the
hemolymph flows not only through circumscribed vessels but also through cavities in the body
delimited only by other tissues and organs. The situation is not one of chaos and disorder, how-
ever. Because organs are found in the same regions in every specimen of a given species, these
cavities are reproducible and observable spaces, though it has been difficult until now to visual-
ize them. In the past, circulatory research has concentrated on the study of the vascular system,
but the dawn of three-dimensional reconstruction techniques in combination with virtual real-
ity methods should make it possible for future projects to capture and make visible the elusive
lacunar system in arthropods, something that is essential to our understanding of the integra-
tion of circulatory functions in an open circulatory system.
In most arthropods where the circulatory system is responsible for the transport of oxygen,
that is, where a respiratory pigment is present, the vascular system is more complex than in spe-
cies where this is not the case, displaying a higher number of more intricately branched arteries.
This, however, is a tendency, not a strict rule, as smaller arthropods tend to show reduced arte-
rial systems—perhaps as the result of a trade-off against miniaturization.
With regard to respiration, a similar trend is observable. More voluminous species tend to
possess more complex respiratory structures. As described above, decapod branchiae exhibit
various different forms of surface enlargement.
The functional morphology of crustacean circulation and respiration is an important part of
the success story of arthropods. At the center of this success story is a flexible yet in some places
extremely robust exoskeleton enclosing a liquid-filled space. This body design has proved to
be so enormously evolutionarily dynamic that it has been able to ensure survival in all sorts of
different surroundings, making possible the difficult shift from aquatic to terrestrial habitats in
a number of cases.
REFERENCES
Abe, K., and J. Vannier. 1995 . Functional morphology and significance of the circulatory system of
Ostracoda, exemplified by Vargula hilgendorfii (Myodocopida). Marine Biology 124:51–58.
Alberti, G., and U. Kils. 1983. Light- and electron microscopical studies on the anatomy and function of
the gills of krill (Euphausiacea, Crustacea). Polar Biology 1:233–242.
Alexander, D.E., and T. Chen. 1989. The respiratory roles of swimming and nonswimming pleopods in
isopod crustaceans. Comparative Biochemistry and Physiology A 94:689 –692.
Alexandrowicz , J.S. 1932. The innervation of the heart of Crustacea. I. Decapoda. Quarterly Journal of
Microscopical Science 75:182–247.
Alexandrowicz , J.S. 1934 . The innervation of the heart of Crustacea. II. Stomatopoda. Quarterly Journal
of Microscopical Science 76:511–548.
Baccetti, B., and E. Bigliardi. 1969. Studies on the fine structure of the dorsal vessel of arthropods. II. The
“heart” of a crustacean. Zeitschrift f ü r Zellforschung und mikroskopische Anatomie 99:25–36.
Balss, H. 1940 –1961. Decapoda. Der Respirationsapparat. Pages 517–561 in A. Schellenberg and H.-
E. Gruner, editors. Dr. H.G. Bronns Klassen und Ordnungen des Tierreichs. Akademische
Verlagsgesellschaft Geest and Portig , Leipzig.
Barker, D. 1962. A study of Thermosbaena mirabilis (Malacostraca, Peracarida) and its reproduction.
Quarterly Journal of Microscopical Science 103:261–286.
Barra, J.-A., A. Pequeux , and W. Humbert. 1983 A morphological study on gills of a crab acclimated to
fresh water. Tissue and Cell 15:583–596.
Bauchau, A.G. 1981. Crustaceans. Pages 386–420 in N.A. Ratcliffe and A.F. Rowley, editors. Invertebrate
blood cells, Vol. 2. New York , Academic Press.
Baumann, H. 1921. Das Gef äßsystem von Astacus fluviatilis (Potamobius L.). Zeitschrift f ü r wissen-
schaftliche Zoologie 118:246 –312.
Belman, B.W., and J.J. Childress. 1976. Circulatory adaptations to the oxygen minimum layer in the bath-
ypelagic mysid Gnathophausia ingens. Biological Bulletin 0150:15–37.
Bowman, T.E., and T.M. Iliffe. 1985 . Mictocaris halope, a new unusual peracaridan crustacean from
marine caves on Bermuda. Journal of Crustacean Biology 5:58 –73.
Boxshall, G.A., and D. Jaume. 2009. Exopodites, epipodites and gills in crustaceans. Arthropod
Systematics and Phylogeny 67:229 –254.
Brusca, R.C., and G.J. Brusca. 2003. Invertebrates. Sinauer, Sunderland, MA.
Burnett, B.R., and R.R. Hessler. 1973. Thoracic epipodites in the Stomatopoda (Crustacea): A phyloge-
netic consideration. Journal of Zoology 169:381–392.
Burrage, T.G., and R.G. Sherman. 1978. Cellular organization of the embryonic lobster heart. Cell and
Tissue Research 188:171–187.
Calman, W.T. 1909. Part VII: Appendiculata. Third fascicle: Crustacea. Pages 1–346 in R. Lancester, edi-
tor, A treatise on zoology. Adam and Charles Black , London.
Cannon, H.G. 1947. On the anatomy of the pedunculate barnacle Lithotrya . Philosophical Transactions
of the Royal Society 595:89 –136.
Cannon, H.G., and S.M. Manton. 1927. On the feeding mechanism of a mysid crustacean, Hemimysis
lamornae. Transactions of the Royal Society of Edinburgh 55:219 –253.
Chan, K.S., M.J. Cavey, and J.L. Wilkens. 2006. Microscopic anatomy of the thin-walled vessels leav-
ing the heart of the lobster Homarus americanus: Anterior lateral arteries. Invertebrate Biology
125:70 –82.
Childress, J.J. 1971. Respiratory adaptations to the oxygen minimum layer in the bathypelagic mysid
Gnathophausia ingens. Biological Bulletin 141:109 –121.
Claus, C. 1888. Ü ber den Organismus der Nebaliiden und die systematische Stellung der Leptostraken.
Arbeiten aus dem Zoologischen Institut der Universität Wien 8:1–149.
Copeland, D.E. 1967. A study of salt secreting cells in the brine shrimp (Artemia salina). Protoplasma
63:363–384.
Croghan, P.C. 1958. The osmotic and ionic regulation of Artemia salina (L.). Journal of Experimental
Biology 35:219 –233.
Dahl, E. 1977. The amphipod functional model and its bearing upon systematics and phylogeny.
Zoologica Scripta 6:221–228.
Dejours, P. 1981. Principles of comparative respiratory physiology. Elsevier, Amsterdam .
Delage, Y. 1883. Circulation et respiration chez le Crustacés Schizopodes (Mysis Latr.). Archives de
Zoologie Expérimentale et Générale 1:105–130.
Dennell, R. 1937. On the feeding mechanism of Apseudes talpa and the evolution of the peracaridan feed-
ing mechanisms. Transactions of the Royal Society of Edinburgh 59:57–78.
Dunel-Erb, S., J.C. Massabuau, and P. Laurent. 1982. Organisation fonctionnelle de la branchie
d’Écrevisse. Comptes rendus des séances de la Société de Biologie et de ses Filiales 176:248 –258.
Edgecombe, G.D. 2008. Anatomical nomenclature: Homology, standardization and datasets. Zootaxa
1950:87–95.
Farrelly, C.A., and P. Greenaway. 1993. Land crabs with smooth lungs—Grapsidae, Gecarcinidae and
Sundathelphosidae, ultrastructure and vasculature. Journal of Morphology 215:245–260.
Farrelly, C.A., and P. Greenaway. 1994 . Gas-exchange through the lungs and gills in air-breathing crabs.
Farrelly, C.A., and P. Greenaway. 2005 . The morphology and vasculature of the respiratory organs of
terrestrial hermit crabs (Coenobita and Birgus): Gills, branchiostegal lungs and abdominal lungs.
Fassbinder, K. 1912. Beiträge zur Kenntnis des Süßwasserostracoden. Zoologische Jahrbücher, Abteilung
f ü r Anatomie und Ontogenie der Tiere 32:533–576.
Foster, C.A., and H.D. Howse. 1978. A morphological study on gills of the brown shrimp, Penaeus aztecus.
Tissue and Cell 10:77–92.
Freire, C.A., H. Onken, and J.C. McNamara. 2008. A structure-function analysis of ion transport in crus-
tacean gills and excretory organs. Comparative Biochemistry and Physiology A 151:272–304.
Greenaway, P., and C.A. Farrelly. 1984 . The venous system of the terrestrial crab Ocypode cordimanus
(Desmarest, 1825) with particular reference to the vasculature of the lungs. Journal of Morphology
181:133–142.
Grindley, J.R., and R.R. Hessler. 1971. The respiratory mechanism of Spelaeogriphus and its phylogenetic
significance (Spelaeogriphacea). Crustaceana . 20:141–144.
Gruner, H.-E. 1993. Crustacea. Pages 448–1030 in H.-E. Gruner, editor. Arthropoda (ohne Insecta).
Lehrbuch der Speziellen Zoologie, Bd I, 4. Teil. Gustav Fischer, Jena.
Gruner, H.-E., and G. Scholtz. 2004 . Segmentation, tagmata and appendages. Pages 13–57 in J. Forest
, J.C. von Vaupel-Klein, and F.R. Schram, editors. Treatise on zoology—anatomy, taxonomy,
biology. The Crustacea revised and updated from the Traité de Zoologie. Brill, Leiden.
Guirguis, M.S., and J.L. Wilkens. 1995 . The role of the cardioregulatory nerves in mediating heart rate
responses to locomotion, reduced stroke volume and heurohormones in Homarus americanus.
Biological Bulletin 188:179 –185.
Harms, J.W. 1932. Die Realisation von Genen und die consekutive Adaptation. II. Birgus latro L., als
Landkrebs und seine Beziehungen zu den Coenobiten. Zeitschrift f ü r wissenschaftliche Zoologie
140:167–290.
Hartmann, G. 1967. Ostracoda. 2. Lieferung. Pages 216–408 in H.-E. Gruner, editor. Dr. H.G. Bronns
Klassen und Ordnungen des Tierreichs, Vol. 5, Abteilung 1. Akademische Verlagsgesellschaft Geest
and Portig , Leipzig.
Haupt, C., and S. Richter. 2008. Limb articulation in caridoid crustaceans revisited—new evidence from
Euphausiacea (Malacostraca). Arthropod Structure and Development 37:221–233.
Hearing , V.J., and S.H. Vernick. 1967. Fine structure of the blood cells of the lobster Homarus americanus.
Chesapeake Science 8:170 –186.
Hessler, R.R., and R. Elofsson. 1992. Cephalocarida. Pages 9–24 in F.W. Harrison and A.G. Humes,
editors. Microscopic anatomy of invertebrate. Wiley-Liss, New York.
Hessler, R.R., and R. Elofsson. 2001. The circulatory system and an enigmatic cell type of the cephalo-
carid crustacean Hutchinsoniella macracantha. Journal of Crustacean Biology 21:28 –48.
Hoese, B. 1982. Morphologie und Evolution der Lungen bei den terrestrischen Isopoden (Crustacea,
Isopoda, Oniscoidea). Zoologische Jahrbücher, Abteilung Anatomie und Ontogenie der Tiere
107:396 –422.
Holliday, C.W., D.B. Roye, and R.D. Roer. 1990. Salinity-induced changes in branchial Na+/K+-ATPase
activity and transepithelial potential differences in the brine shrimp Artemia salina. Journal for
Hong , S.Y. 1988. Development of epipods and gills in some pagurids and brachyurans. Journal of Natural
History 22:1005–1040.
Hose, J.E., and G.G. Martin. 1989. Defense function of granulocytes in the ridgeback prawn Sicyonia
ingentis Burkenroad 1938. Journal of Invertebrate Pathology 53:335–346.
Hose, J.E., G.G. Martin, and A.S. Gerard. 1990. A decapod hemocyte classification scheme integrating
morphology, cytochemistry, and function. Biological Bulletin 178:33–45.
Howse, H.D., V.J. Ferrans, and R.G. Hibbs. 1971. A light and electron microscopic study of the heart of a
crayfish, Procambarus clarkii (Giraud). II. Fine structure. Journal of Morphology 133:353–374.
Huber, B.A. 1992. Frontal heart and arterial system in the head of Isopoda. Crustaceana 63:57–69.
Huckstorf, K., and C.S. Wirkner, 2011. Comparative morphology of the hemolymph vascular system in
Krill (Euphausiacea; Crustacea). Arthropod Structure and Development 40:39 –53.
Jaume, D., G.A. Boxshall, and R.N. Bamber. 2006. A new genus from the continental slope of Brazil and
the discovery of the first males in the Hirsutiidae (Crustacea: Peracarida: Bochusacea). Zoological
Journal of the Linnean Society 148:169 –208.
Johnson, P.T. 1980. Histology of the blue crab Callinectes sapidus: A model for the Decapoda. Praeger,
New York.
Keyser, D. 1990. Morphological changes and function of the inner lamella layer of podocopid Ostracoda.
Pages 401–410 in R. Whatley and C. Maybury, editors. Ostracoda and global events. Chapman and
Hall, London.
Kihara, A., and K. Kuwasawa. 1984 . A neuroanatomical and electrophysiological analysis of nervous
regulation in the heart of an isopod crustacean, Bathynomus doederleini: Excitatory and inhibitory
junction potentials. Journal of Comparative Physiology 154:883–894.
Kikuchi, S., and M. Matsumasa. 1993a . The osmoregulatory tissue around the afferent blood vessels of
the coxal gills in the estuarine amphipods, Grandidierella japonica and Melita setiflagella. Tissue and
Cell 25:627–638.
Kikuchi, S., and M. Matsumasa. 1993b. Two ultrastructurally distinct types of transporting tissues,
the branchiostegal and the gill epithelia, in an estuarine tanaid, Sinelobus stanfordi (Crustacea,
Peracarida). Zoomorphology 113:253–260.
Kikuchi, S., and K. Shiraishi. 1997. Ultrastructure and ion permeability of the two types of epithelial cell
arranged alternately in the gill of the fresh water branchipod Caenestheriella gifuensis (Crustacea).
Kobusch, W. 1999. The phylogeny of Peracarida (Crustacea, Malacostraca). Morphological investiga-
tions of the peracaridan foreguts, their phylogenetic implications, and an analysis of peracaridan
characters. Cuvillier, Göttingen.
Kuramoto, T., and A. Ebara. 1984 . Neurohormonal modulation of the cardiac outflow flow through the
cardioarterial valve in the lobster Homarus americanus. Journal of Experimental Biology 111:123–130.
Lauterbach, K.-E. 1970. Der Cephalothorax von Tanais cavolinii Milne Edwards
(Crustacea-Malacostraca). Zoologische Jahrbücher, Abteilung Anatomie und Ontogenie der Tiere
87:94–204.
Lauterbach, K.-E. 1972. Zur Kenntnis von Carapax und Thorax der Stomatopoda (Crustacea).
Zoologischer Anzeiger 188:75–88.
Lauterbach, K.-E. 1979. Ü ber die mutma ßliche Herkunft der Epipodite der Crustacea. Zoologischer
Anzeiger 202:33–50.
Lincoln, R.H. 1979. British marine Amphipoda: Gammaridea. British Museum (Natural History),
London.
Lochhead, J.H., and M.S. Lochhead. 1941. Studies on the blood and related tissues in Artemia (Crustacea,
Anostraca). Journal of Morphology 68:593–632.
Lowe, E. 1935 . On the anatomy of a marine copepod, Calanus finmarchicus (Gunner). Transactions of the
Royal Society of Edinburgh 58:561–603.
Maas, A., C. Haug , J.T. Haug, J. Olesen, X. Zhang , and D. Waloszek. 2009. Early crustacean evolution and
Madaras, F., J.D. Parkin, and P.A. Castaldi. 1979. Coagulation in the sand crab (Ovalipes bipustulatus).
Thrombosis and Haemostasis 42:734–742.
Maitland, D.P. 1986. Crabs that breath air with their legs— Scopimera and Dotilla. Nature 319:493–495.
Martin, G.G., and J.E. Hose. 1992. Vascular elements and blood (hemolymph). Pages 117–146 in F.W.
Harrison, and A.G. Humes, editors. Microscopic anatomy of invertebrates, Vol. 10, Crustacea,
Decapoda. Wiley-Liss, New York.
Martin, J.W. 1992. Branchiopoda. Pages 25–224 in F.W. Harrison and A.G. Humes, editors. Microscopic
anatomy of invertebrates. Vol. 9, Crustacea. Wiley-Liss, New York.
Mauchline, J. 1958. The circulatory system of the crustacean euphausid, Meganyctiphanes norvegica
(M. Sars). Proceedings of the Royal Society of Edinburgh 67:32–42.
Maynard, D.M. 1960. Circulation and heart function. Pages 161–226 in T.H. Waterman, editor. The physi-
ology of Crustacea. Academic Press, New York.
Mayrat, A., B.R. McMahon, and K. Tanaka. 2006. The circulatory system. Pages 3–84 in J. Forest , J.C.
von Vaupel Klein, and F.R. Schram, editors. Treatise on zoology—anatomy, taxonomy, biology.
The Crustacea revised and updated from the Traité de Zoologie, 2. Brill, Leiden.
McConnell, F.M. 1987. Morphometry of transport tissues in a freshwater crustacean. Tissue and Cell
19:319 –349.
McMahon, B.R. 1999. Heart rate: Is it a useful measure of cardiac performance in crustaceans? Pages 807–822
in F.R. Schram and J.C. von Vaupel Klein, editors. Crustaceans and the biodiversity crisis. Brill, Leiden.
McMahon, B.R. 2001. Control of cardiovascular function and its evolution in Crustacea. Journal of
McMahon, B.R., and L.E. Burnett. 1990. The crustacean open circulatory system: A reexamination.
Physiological Zoology 63:35–71.
McMahon, B.R., and J.L. Wilkens. 1983. Ventilation, perfusion and oxygen uptake. Pages 290–372 in D.E.
Bliss and L.H. Mantel, editor. The biology of Crustacea, Vol. 5, Internal anatomy and physiological
regulation. Academic Press, New York.
McMahon, B.R., J.L. Wilkens, and P.J.S. Smith. 1997. Invertebrate circulatory systems. Pages 931–1008
in W.H. Dantzler, editor. Handbook of physiology, Section 13, Comparative Physiology, Vol. 2.
American Physiological Society, Bethesda, NY.
Nylund, A., and A.Tjønneland . 1989. Crustacean heart ultrastructure and its phylogenetic implica-
tions, with special reference to the position of the isopods within the eumalacostracan phylogeny.
Monitore Zoologico Italiano 4:29 –42.
Oelze, A. 1931. Beiträge zur Anatomie von Diastylis rathkei Kr. Zoologische Jahrbücher, Abteilung
Økland, S., A. Tjønneland, L.N. Larsen, and A. Nylund. 1982. Heart ultrastructure in Branchinecta
paludosa, Artemia salina, Branchipus schaefferi, and Streptocephalus sp. (Crustacea, Anostraca).
Paterson, N.F. 1968. The anatomy of the Cape rock lobster, Jasus lalandii (H. Milne Edwards). Annals of
the South African Museum 51:1–232.
Paul, R., S. Zahler, R. Werner, and J. Markl. 1991. Adaptation of an open circulatory system to the oxida-
tive capacity of different muscle cell types. Naturwissenschaften 78:134–135.
Pequeux , A.J.R., R. Gilles, and W.S. Marshall. 1988. NaCl transport in gills and related structures.
Pages 1–73 in R. Greger, editor. Advances in comparative and environmental physiology, Part I,
Invertebrates. Springer, Berlin.
Pirow, R., F. Wollinger, and R.J. Paul. 1999a . The importance of the feeding current for oxygen uptake in
the water flea Daphnia magna. Journal of Experimental Biology 202:553–562.
Pirow, R., F. Wollinger, and R.J. Paul. 1999b. The sites of respiratory gas exchange in the planktonic
crustacean Daphnia magna: An in vivo study employing blood haemoglobin as an internal oxygen
probe. Journal of Experimental Biology 202:3089 –3099.
Ravindranath, M.H. 1980. Hemocytes in haemolymph coagulation in arthropods. Biological Reviews
55:139 –170.
Rogers, P.A.W. 1982. Vascular and microvascular anatomy of the gill of the southern rock lobster, Jasus
novaehollandiae Holthius. Australian Journal of Marine and Freshwater Research 33:1017–1028.
Saalfeld, E. 1936. Untersuchungen über den Blutkreislauf bei Leptodora hyalina . Zeitschrift f ü r ver-
gleichende Physiologie 24:58 –70.
Sars, G.O. 1896. Fauna Norvegiae, Vol.1, Descriptions of the Norwegian species at present known belong-
ing to the suborders Phyllocarida and Phyllopoda. Joint-Stock, Christiania, Norway.
Sars, G.O. 1899 –1900. An account of the Crustacea of Norway: With short descriptions and figures of all
the species, Vol. 3, Cumacea. Cammermeyers, Christiania, Norway.
Schmidt, C., and J.W. W ägele. 2001. Morphology and evolution of respiratory structures in the pleopod
exopodites of terrestrial Isopoda (Crustacea, Isopoda, Oniscidea). Acta Zoologica 82:315–330.
Schmitz , E.H. 1992. Amphipoda. Pages 443–528 in F.W. Harrison and A.G. Humes, editors. Microscopic
anatomy of invertebrates, Vol. 9. Wiley-Liss, New York.
Schwartzkopff, J. 1955 . Vergleichende Untersuchung der Herzfrequenz bei Krebsen. Biologisches
Zentralblatt 74:480 –497.
Siewing , R. 1952. Morphologische Untersuchungen an Cumaceen (Cumopsis goodsiri v. Beneden).
Zoologische Jahrbücher, Abteilung Anatomie und Ontogenie der Tiere 72:522–559.
Siewing , R. 1954 . Ü ber die Verwandtschaftsbeziehungen der Anaspidaceen. Verhandlungen der
Deutschen Zoologischen Gesellschaft 16:210–252.
Siewing , R. 1956. Untersuchungen zur Morphologie der Malacostraca (Crustacea). Zoologische
Jahrbücher, Abteilung Anatomie und Ontogenie der Tiere 75:39 –176.
Siewing , R. 1958. Anatomie und Histologie von Thermosbaena mirabilis: ein Beitrag zur Phylogenie der
Reihe Pancarida (Thermosbenacea). Abhandlungen der Mathematisch Naturwissenschaftlichen
Klasse/Akademie der Wissenschaften und der Literatur in Mainz 7:195–270.
Siewing , R. 1959. Syncarida. Pages 1–121 in H.-E. Gruner, editor. Dr. H.G. Bronns Klassen und Ordnungen
des Tierreichs, Vol. 5, Abteilung 1. Akademische Verlagsgesellschaft Geest and Portig , Leipzig.
Silen, L. 1954 . On the circulatory system of the Isopoda Oniscoidea. Acta Zoologica 35:11–70.
Söderhä ll, K., and V.J. Smith. 1983. Separation of the haemocyte populations of Carcinus maenas and
other marine decapods, and prophenoloxidase distribution. Developmental and Comparative
Immunology 7:229 –239.
Söderhä ll, K., V.J. Smith, and M.W. Johansson. 1986. Exocytosis and uptake of bacteria by isolated
haemocyte populations of two crustaceans: Evidence for cellular co-operation in the defense reac-
tions of arthropods. Cell and Tissue Research 245:43–49.
Steel, D.H., and V.J. Steel. 1991. The structure and organization of the gills of the gammaridean
Amphipoda. Journal of Natural History 25:1247–1258.
Stillman, J.H. 2000. Evolutionary history and adaptive significance of respiratory structures on the legs
of intertidal porcelain crabs, genus Petrolisthes. Physiological and Biochemical Zoology 73:86 –96.
Taube, E. 1914 . Beiträge zur Entwicklungsgeschichte der Euphausiden. Zeitschrift f ü r wissenschaftliche
Zoologie 114:577–656.
Taylor, H.H., and E.W. Taylor. 1992. Gills and lungs: The exchange of gases and ions. Pages 203–293 in
F.W. Harrison and A.G. Humes, editors. Microscopic anatomy of invertebrates, Vol. 10, Crustacea,
Decapoda. Wiley-Liss, New York.
Terwilliger, N.B., and M. Ryan. 2001. Ontogeny of crustacean respiratory proteins. American Zoologist
41:1057–1067.
Tjønneland, A., S. Økland, and A. Nylund. 1987. Evolutionary aspects of the arthropod heart. Zoologica
Scripta 16:157–175.
Toney, M.E. 1958. Morphology of the blood cells of some Crustacea. Growth 22:35–50.
Ungerer, P., and C. Wolff. 2005 . External morphology of limb development in the amphipod Orchestia
cavimana (Crustacea, Malacostraca, Peracarida). Zoomorphology 124:89 –99.
Vannier, J., M. Williams, and D.J. Siveter. 1997. The Cambrian origin of the circulatory system of crusta-
ceans. Lethaia 30:169 –184.
Vogt, G., C.S. Wirkner, and S. Richter. 2009. Symmetry variation in the heart-descending artery system
of the parthenogenetic marbled crayfish. Journal of Morphology 207:221–226.
Vogt, L. 2008. Learning from Linnaeus: Towards developing the foundations for a general structure
concept for morphology. Zootaxa 1950:123–152.
W ägele, J.-W. 1989. Evolution und phylogenetisches System der Isopoda—Stand der Forschung und neue
Erkentnisse. Zoologica 140:1–262.
W ägele, J.-W. 1992. Isopoda. Pages 529–617 in F.W. Harrison and A.G. Humes, editors. Microscopic
anatomy of invertebrates, Vol. 9, Crustacea. Wiley-Liss, New York.
W ägele, J.-W. 1994 . Review of methodological problems of “computer cladistics” exemplified with a
case study on isopod phylogeny (Crustacea: Isopoda). Journal of Zoological Systematics and
Evolutionary Research 32:81–107.
Wilkens, J.L., M.J. Cavey, I. Shovkivska, M.L. Zhang , and H.E.D.J. ter Keurs. 2008. Elasticity, unex-
pected contractility and the identification of actin and myosin in lobster arteries. Journal of
Wilkens, J.L., and R.L. Walker. 1992. Nervous control of crayfish cardiac hemodynamics. Molecular
Comparative Physiology 11:115–122.
Wilkens, J.L., T. Yazawa, and M.J. Cavey. 1997. Evolutionary derivation of the American lobster cardio-
vascular system: A hypothesis based on morphological and physiological evidence. Invertebrate
Biology 116:30 –38.
Wirkner, C.S., and S. Richter. 2003. The circulatory system in Phreatoicidea: Implication for the isopod
ground pattern and peracarid phylogeny. Arthropod Structure and Development 32:337–347.
Wirkner, C.S., and S. Richter. 2004 . Improvement of microanatomical research by combining corrosion
casts with MicroCT and 3D reconstruction, exemplified in the circulatory organs of the woodlouse.
Microscopy Research and Technique 64:50 –54.
Wirkner, C.S., and S. Richter. 2007a . The circulatory system in Mysidacea—implications for the phylo-
genetic position of Lophogastrida and Mysida (Malacostraca, Crustacea). Journal of Morphology
268:311–328.
Wirkner, C.S., and S. Richter. 2007b. The circulatory system and its spatial relations to other major organ
systems in Spelaeogriphacea and Mictacea (Malacostraca, Crustacea)—a three-dimensional analy-
sis. Zoological Journal of the Linnean Society 149:629 –642.
Wirkner, C.S., and S. Richter. 2007c . Comparative analysis of the circulatory system in Amphipoda
(Malacostraca, Crustacea). Acta Zoologica 88:159 –171.
Wirkner, C.S., and S. Richter. 2008. Morphology of the haemolymph vascular system in Tanaidacea and
Cumacea: Implications for the relationships of “core group” Peracarida (Malacostraca; Crustacea).
Wirkner, C.S., and S. Richter. 2009. The hemolymph vascular system in Tethysbaena argentarii
(Thermosbaenacea, Monodellidae) as revealed by 3D reconstruction of semi-thin sections. Journal
Wirkner, C.S., and S. Richter. 2010. Evolutionary morphology of the circulatory system in Peracarida
(Malacostraca; Crustacea). Cladistics 26:143–167.
Wolff, C., and G. Scholtz. 2008. The clonal composition of biramous and uniramous arthropod limbs.
Wood, P.J., J. Podlewski, and T.E. Shenk. 1971. Cytochemical observations of the hemolymph cells during
coagulation in the crayfish Orconectes virilis. Journal of Morphology 134:479 –488.
Young , J.H. 1959. Morphology of the white shrimp, Penaeus setiferus (Linnaeus 1758). Fishery Bulletin of
the Fish and Wildlife Service 59:1–168.
Zaddach, E.G. 1841. De Apodis cancriformis Schaeff. Anatome et historia evolutionis, Dissertatio inau-
guralis zootomica. Kessinger, Bonnae, Germany.
Zimmer, C., and H.-E. Gruner. 1956. Euphausiacea. Pages 1–286 in H.-E. Gruner . Dr. H.G. Bronns
Klassen und Ordnungen des Tierreiches, Vol. 5, Abteilung 1. Akademische Verlagsgesellschaft
Geest and Portig, Leipzig , Germany.
15
FUNCTIONAL ANATOMY OF THE REPRODUCTIVE SYSTEM
Laura S. L ópez Greco
Abstract
This chapter brief ly describes the diversity in the functional morphology of the crustacean
reproductive organs from both macroscopic and microscopic approaches. The anatomical
design of the female reproductive system involving the different positions of germaria and
growing oocytes and types of accessory cells is compared within crustaceans and partially
with other Arthropoda. Male reproductive systems also show diversity in testes design and
in the proposed roles of Sertoli-like cells. The genital ducts in both females and males show
large morphological variability related to their functions in gamete transport, sperm matura-
tion, sperm storage, and spermatozoa packaging. This anatomical diversity is proposed to be
partially driven by the environment since some similar morphofunctional patterns are found
in similar habitats. Specially, different patterns of sperm storage are discussed within the
framework of sperm competition. Reproductive morphology in hermaphroditic and intersex
species is also included and compared, highlighting the significance of these reproductive
models to understand sexual differentiation mechanisms in crustaceans. Finally, morpho-
logical comparative studies are proposed to address questions related to the evolution of gen-
eral and particular designs and primitive and advanced patterns, as well as the study of the
embryological development of the reproductive system as a key to understand the differences
between and within taxa and neurohormonal pathways of sexual differentiation and endo-
crine disruption.
INTRODUCTION
The enormous diversity in external morphology among the various crustacean taxa is
accompanied by significant diversity in the major organ systems, including the reproductive
organs. The relationship between the anatomy of the male reproductive system and that of
413
the female, including the size, form, and mechanisms of spermatozoa/spermatophore main-
tenance, has rarely been studied in crustaceans, although in many other taxa the close coev-
olution between male and female systems has been demonstrated (see Miller and Pitnick
2002 for review). Studying the reproductive systems in a phylogenetic context can show how
internal organs, external structures, mating behaviors, and fertilization mechanisms have
coevolved.
In his review on the role of the ovary and vitellogenesis mechanisms in the evolution of
invertebrate life-history patterns, Eckelbarger (1994, 194) stated that “life-history traits are
constrained by ovarian structure and species-specific vitellogenic mechanisms determining
quantity, quality and rate of energy incorporation. The rate of egg production, frequency of
breeding, size and energy content of the egg, and the resultant consequences to the larval
ecology are strongly influenced by the ovary.” In this context, the study of ovarian form and
function can provide important hints to understanding the evolution of life-history patterns
in crustaceans.
Similarly, sperm competition is one of the main forces involved in the evolution of very
complex social behaviors, and it is strongly dependent on structures for sperm storage in the
female reproductive tract. Crustaceans exhibit a great morphological diversity in sperm stor-
age chambers. Many species do not have these chambers and need to mate at each spawning,
involving different mating behaviors and female guarding strategies. Female sperm storage,
when present, is an integral part of the female’s mating strategy that can modify her mating
frequency and favor the control/manipulation of male gametes (Neubaum and Wolfner 1999).
Within this framework, there is no doubt that the comparative analysis of reproductive struc-
tures can help us understand the diversity of sexual and mating systems that has evolved in
crustaceans.
SEXUAL DIFFERENTIATION
The mechanisms involved in crustacean sex determination/differentiation are not clearly under-
stood. Although determination and differentiation are mainly determined genetically, extrinsic
factors such as seasonal variations in the length of the photoperiod, environmental tempera-
ture, and factors related to the “social structure” of the population act as modulators or even
sex determinants in crustaceans (Ginsburger-Vogel and Charniaux-Cotton 1982, Bergström
1997, McCabe and Dunn 1997, Johnson et al. 2001). In the amphipods Orchestia gammarella and
Gammarus duebeni (Legrand et al. 1987), as in many isopods (Rigaud et al. 1997), parasites play
a role in sex determination. Microbial parasites live in the ovarian tissue and are transmitted
from mother to offspring, with infected females producing only daughters (see Johnson et al.
2001 for review).
With respect to sexual differentiation, the androgenic gland (AG) is the only endocrine gland
in crustaceans specifically related to the male sexual function. Hormones produced by the AG
regulate the differentiation of the primary and secondary sexual characters, including repro-
ductive behavior (Charniaux-Cotton and Payen 1988, Sagi et al. 1997, Sagi and Khalaila 2001,
Barki et al. 2003). These hormones have striking effects on both somatic growth and inhibition
of vitellogenesis (Sagi et al. 2002, Barki et al. 2003, Manor et al. 2004). In the absence of the AG,
a sexually undifferentiated gonad will develop into an ovary. Charniaux-Cotton (1954) was the
first to suggest a regulatory role for the AG. She demonstrated that the bilateral ablation of the
AG blocked the differentiation of secondary male characteristics and suppressed spermatogen-
esis in Orchestia gammarella. Posterior studies that involved removal of the AG from males and/
or transplantation of the gland into females have demonstrated similar effects in amphipods,
isopods, crayfish, and crabs (for review, see Martin et al. 1996, Johnson et al. 2001, Cui et al.
Functional Anatomy of the Reproductive System 415
2005, Aflalo et al. 2006), but it has not been studied in nonmalacostracans. AG is the exclusive
source of the androgenic gland hormone (AGH), whose effects are considered similar to those
of androgens in mammals (Sagi and Khalaila 2001, Manor et al. 2004). The biochemical nature
of AGH is not clearly understood (for review, see Johnson et al. 2001, Manor et al. 2004). The
recent discovery of an AG-specific gene expressed in males, structurally similar to insulin or
insulin-like growth factor, supports the hypothesis that insulin participates in sexual differen-
tiation in crustaceans (Manor et al. 2007). The role of the AG secreting the AGHs seems to be
decisive for the development and maintenance of the male function in intersex individuals or in
protandric hermaphroditic species (Hasegawa et al. 1993, Sagi et al. 1997, Suzuki and Yamasaki
1998, Barki et al. 2003, Manor et al. 2004, Okumura et al. 2005). At present, it is unknown how
the male function is regulated by the AG when species are functional simultaneous hermaphro-
dites, as in many caridean species (for review, see Bauer 2000, Baeza 2008, Laubenheimer and
Rhyne 2008). How the AG induces male function and inhibits female function is an unresolved
question that might involve different regulatory pathways of neurohormonal control of sperma-
togenesis and oogenesis in those species.
Although hermaphrodites are found in a few taxa, most crustaceans are gonochoric. The fact
that the sexes are separate opens the door for sexual conflicts, which has implications for the
evolution of not only their mating behaviors but also the reproductive organs. Below I describe
separately the detailed anatomy and function of the female and male reproductive systems
before comparing them in the context of female/male coevolution.
FEMALE REPRODUCTIVE SYSTEM
In crustaceans, the female reproductive system is dorsally or dorsolaterally positioned with

respect to the hepatopancreas (Fig. 15.1). The female reproductive system consists of paired or
unpaired ovaries leading through the genital ducts into a pair of gonopores, or in some cases a
single gonopore. In many taxa, structures for sperm or spermatophore retention (derived or not
from the genital ducts) are present (Table 15.1). While in all malacostracans the female gonop-
ores open on the sternite or coxae of the sixth thoracic somite, in nonmalacostracan crustaceans
the position is quite variable (McLaughlin 1983).
Ovary Architecture
Macroscopic Features
The ovaries are usually characterized according to their form. Rounded or elongated ovaries
with or without lateral lobules with some degree of medial fusion are found in many crusta-
ceans (Adiyodi and Subramoniam 1983, McLaughlin 1983, Johnson et al. 2001). In Ostracoda,
paired ovaries are housed in the posterodorsal and posterior regions of the body and may
extend between valve lamellae (Cohen and Morin 1990, Maddocks 1992). In Branchiura, the
ovary is a single bilobed organ (Overstreet et al. 1992). In Cirripedia, in balanomorphs paired
ovaries lie in the mantle tissue overlaying the basis, or they can extend into the spaces within
the wall plates, while in lepadomorphs the ovaries tend to lie in the distal half of the peduncle
(see Walker 1992 for review). In Copepoda, paired ovaries are retained in only a few taxa, such
as the misophrioids and siphonostomatoids, while females of most species have a modified
system with a single median ovary, as found in calanoids and harpacticoids (Boxshall 1992).
Elongated and paired ovaries are the general condition among the Malacostraca, and within
the Decapoda some degree of fusion is common. In penaeid shrimps, the ovary is partially
fused in the cephalothoracic region and consists of a pair of anterolateral horns and lateral
Fig. 15.1.
Schematic drawings showing the relative position of the reproductive systems in crustaceans. Black
shading indicates the reproductive system; gray shading, the digestive system. (A) Anostraca (female).
(B) Ostracoda (male). (C) Cladocera (female). (D) Cirripedia (hermaphrodite). (E) Copepoda (male).
(F) Leptostraca (female). (G) Stomatopoda (male). (H) Isopoda (male). (I) Decapoda: Anomura (male).
(J) Decapoda: Astacida (female). (K) Decapoda: Brachyura (male). Adapted from McLaughlin (1983).
Table 15.1. General features of the reproductive systems in crustaceans.
Taxa Ovary type Testes Sexuality
Class
Subclass
H-shaped
Superorder
Type I or II
Subphylum
Paired lobes
Paired testes
Partially fused
Partially fused
Follicular cells
Unpaired ovary
Unpaired testes
Spermatophore
attachmentc
Hermaphrodites
or intersex species
Seminal receptacle
Gonochoric species
Paired or unpaired
seminal receptaclesa
Sertoli-like cells or
accessory cells
Spermatophore typeb
Nurse or accessory cells

Crustacea
Remipedia X X I X
Cephalocarida X X X X X
Branchiopoda X X I X X U X X X 0/I I X X
Maxillopoda
Thecostraca
Cirripedia X I X P X X 0 I X
Copepoda X X I X X P X X X II E X
Branchiura X II X X P X I/0 E X
Ostracoda X X I, II X X P X X X I/0 X
Malacostraca
Phyllocarida I X I X
Eumalacostraca
Hoplocarida X X I X X U X X I E X
Syncarida I X X X I E X
Eucarida X X X X I X X P/U X X X I, II I, E X X
Peracarida X X I X X P X X I I, E X X
a
Seminal receptacles: P, paired; U, unpaired.
b
Spermatophore type: 0, no spermatophore; I, simple spermatophore; II, complex spermatophore.
c
Spermatophore/spermatozoa attachment: I, internal; E, external.
lobes, while in anomurans, marine lobsters, and brachyuran crabs, an H-shaped ovary with
anterior and posterior lobes is found (see Krol et al. 1992 for review). Recent anatomical stud-
ies have shown two different anatomical patterns in freshwater crayfish, one with a Y-shaped
ovary (mainly in Cambaridae), and the other with an H-shaped ovary or parallel strands, found
in Parastacidae (Vogt 2002, Vazquez et al. 2008). In the Peracarida, the paired tubes that dif-
ferentiate into ovaries are often spindle shaped and prolonged at each end in a suspensory liga-
ment (see Johnson et al. 2001 for review), while H-shaped ovaries are found in sphaeromatid
isopods (Shuster 1991). The ovaries of parasitic bopyrids often grow into very different forms
with segmentally arranged diverticula (see W ägele 1992 for review).
Mature ovaries are usually characterized according to their color, and specific developmental
categories are commonly used to identify the reproductive status of the individuals in ecological
studies. Since determining the color of the ovary can be very subjective, the use of a chromatic
scale catalog (e.g., Pantone Matching System) has been recently introduced (see Peixoto et al.
2005 for review).
Microscopic Features
Ovarian Wall
The connective tissue surrounding the ovary is referred to as the ovarian wall and in most
studied species it is a thin layer of connective tissue that leads into the outer layer of the ovi-
duct (Adiyodi and Subramoniam 1983, Krol et al. 1992, Ikuta and Makioka 1997, Johnson et al.
2001). In the marine lobsters Homarus americanus (Talbot 1981) and Jasus frontalis (Elorza and
Dupré 1999), the presence of a thick, multilayered muscular tunic composed of three or four
layers of muscular cells and blood vessels has been reported. This layer forms a highly devel-
oped muscular net resembling “guy wires” (sensu Talbot 1981) around the follicles (Talbot 1981,
Elorza and Dupré 1999). The muscular components in the ovarian wall have been proposed to
play an important role during ovulation (Talbot 1981, Elorza and Dupré 1999). In other species
(nonmalacostracans, amphipods, isopods, caridean shrimps, crabs), the ovarian wall has no
differentiated muscular layer, and so the contraction of body muscles during prespawning and
spawning behavior is partially involved in releasing the oocytes from the ovary. In the crayfish
Astacus leptodactylus, the presence of myotropic neuropeptides stimulating the muscular sheath
of the oviduct has been demonstrated (Torfs et al. 2002). Prostaglandins are thought to stimu-
late the contraction of ovarian tissue in crayfish and prawns (for review, see Spaziani et al. 1995,
Silkovsky et al. 1998).
Germinal Zone and the Growing Oocytes

The germinal zone is continually active throughout the reproductive life of the females, and
because of the size of the mature oocytes, it is seen more easily in juveniles (Fig. 15.2) and
recently postspawned females (Adiyodi and Subramoniam 1983). In the ostracod Argulus japon-
icus, the germarium lies along the dorsomedial side of the ovary, and the growing oocytes are
arranged in order of size with the larger oocytes farther from the germarium in a more ventral
position (Ikuta and Makioka 1997). In Remipedia, the oocytes are positioned along the ovary
with the smallest (youngest) oocytes anteriorly and the largest (mature) oocytes proceed-
ing posteriorly (Yager 1991), as has also been observed in the ostracod Cyprinotus uenoi (Ikuta
et al. 2007). In Cladocera, the position of the germarium varies (between the anterior and the
posterior end of the ovary), depending on the mode of reproduction and types of resting eggs
(for review, see Rossi 1980, Martin 1992). In Vargula hilgendorfii (Ostracoda), the laterally flat-
tened and saclike ovaries on both sides of the alimentary canal show another inner regionaliza-
tion: the lateral side of the ovary wall, which is facing the alimentary canal, is thick, while the
Fig. 15.2.
Crustacean ovaries. (A and B) Schematic drawing of the mandibulate (A) and chelicerate (B) type of
ovary. Abbreviations: GE, germarium; GO, growing oocytes; MO, mature oocytes; OL, ovarian lumen
(redrawn and modified after Ikuta and Makioka 1999a and Ikuta and Makioka 2004, respectively). (C)
Detail of the germarium (GE) and early growing oocytes (GO) surrounded by the follicular cells (FC)
in Leurocyclus tuberculosus (Brachyura) (courtesy of X. Gonzalez Pisani). (D) Detail of a growing oocyte
(GO) surrounded by follicular cells (FC) in Cherax quadricarinatus (Astacida).
side facing the body wall is thin; growing oocytes are found only in the thin wall (Ikuta and
Makioka 1999a). Based on the internal design of the ovary (a common cause of confusion), in
balanomorphs (Cirripedia) the branched tubules of the ovaries have been named “ovarioles,”
the common name of the ovarian unit of insects (for review, see McLaughlin 1983, Chapman
1998). In Labidocera aestiva (Copepoda), the oogonia proliferate at the posterior end of the ovary
and then move anteriorly as they undergo differentiation (see Boxshall 1992 for review). In the
Malacostraca, the growing oocytes surround the germarium, and there is no clear regionaliza-
tion along the anterior-posterior axis of the ovary, except in some Peracarida. Single or double
rows of oocytes along the anterior-posterior axis are found in cumaceans, tanaids, and amphi-
pods (see Johnson et al. 2001 for review).
Depending on the position of the growing oocytes with respect to the ovarian lumen, two
morphological types of ovaries are recognized in crustaceans: the mandibulate type (type I)
and the chelicerate type (type II; according to Makioka 1988, Ikuta and Makioka 1999a) (Fig.
15.2A,B). In type I ovaries, the developing oocytes that leave the germarium grow in the inner
surface of the ovarian wall facing the ovary lumen (Fig. 15.2A). This mode of oogenesis is seen
in many malacostracan species (Adiyodi and Subramoniam 1983, Krol et al. 1992, Ando and
Makioka 1998, Kronenberger et al. 2004), in the freshwater ostracod Cyprinotus uenoi (Ikuta
et al. 2007), and in other mandibulate arthropods (Makioka 1988). Since the developing oocytes
move toward the lumen, a usual feature in this ovary type is that the mature ovary filled with
the largest oocytes seems to be a “compact” organ from a histological point of view. In type II
ovaries, the developing oocytes of various sizes are attached to the outer surface of the ovary
according to their sizes, with the larger oocytes being farther from the germarium (Fig. 15.2B).
The ovarian lumen includes no growing oocytes, and the secondary oocytes are ovulated from
the outer surface of the ovarian wall into the ovarian lumen through the gaps between the elon-
gated ovarian epithelial cells forming “stalks” that support them. Once ovulated toward the
ovarian lumen, oocytes are transported into the oviduct as in type I (Ikuta and Makioka 2004).
This type has been described in myodocopids (Ikuta and Makioka 1999a, 1999b), branchiurans
(Ikuta and Makioka 1997), pentastomids (Nørrevang 1983), and chelicerates (Makioka 1988,
Soranzo et al. 2000). While this distinction is very useful and supported by numerous studies,
unfortunately it did not find its way into the general literature, mainly due to the lack of com-
parative studies on the ovarian anatomy, especially in nonmalacostracans.
When comparing both types, the female germ cells are positioned in “reversed” directions
in the germaria, and consequently, the oocytes grow in different position with respect to the
ovarian lumen (Ikuta and Makioka 1999a). No explanation has been given for the embryologi-
cal origin of these two types of ovary, but possibly they are a reflection of two ancient modes of
oogenesis.
Within type II, two different relative positions of the germarium have been reported: the
germarium facing into the ovarian lumen, as seen in Argulus japonicus (Ikuta and Makioka 1997),
or facing to the body cavity, as found in the ostracod Conchoecia imbricata (Ikuta and Makioka
2004) (Fig. 15.2B).
Besides the oogonia and oocytes, other cell types are usually found in the ovary: follicular
cells, accessory cells, nurse cells, or mesodermal stroma (Adiyodi and Subramoniam 1983, Krol
et al. 1992, Johnson et al. 2001). These cells are commonly assumed to play a trophic role in
invertebrates. Although the topographic, structural, and functional relationships between germ
cells and these other cell types are poorly understood in most invertebrate species, many exam-
ples demonstrate that some accessory cells enable the organism to accelerate egg production
through trophic support of the growing oocytes (see Eckelbarger 1994 for review). Although
various names have been extensively used for these cell types in crustaceans (see Krol et al. 1992
for review), at least two types can be identified according to their embryological origin: follicu-
lar cells and nurse cells.
Follicular cells are nongerminative accessory somatic cells in the crustacean ovary (Adiyodi
and Subramoniam 1983, Johnson et al. 2001). These mesodermal cells are present in the gonad
from the early developmental stage on and are very common within the germarium. The fol-
licular cells are usually round or oval when in aggregation and become flattened on attachment
to the oocyte surface defining the “ovarian follicle” (Adiyodi and Subramoniam 1983) (Fig.
15.2C,D). This description is mainly based on the malacostracan design, and this “folliculogen-
esis” process (sensu Adiyodi and Subramoniam 1983) is related to the proposed role of the follic-
ular cells during vitellogenesis (see Legrand and Juchault 1994 for review). These cells are also
involved, at least partially, in the formation of oocyte/egg envelopes (Talbot 1981, Adiyodi and
Subramoniam 1983, Krol et al. 1992, Rosati 1995), and they remain within the ovary after ovula-
tion, playing an important role in the oosorption process (Adiyodi and Subramoniam 1983, Krol
et al. 1992). Important variations are seen among the Peracarida. While in amphipods follicle
cells are recycled after ovulation to join other new oocytes that are entering vitellogenesis, it is
believed that in isopods the follicular cells degenerate after completion of oogenesis (Johnson
et al. 2001).
Nurse cells are germinal in origin, being formed by incomplete cytokinesis of oogonial divi-
sions in the germarium and accompanying the growing oocytes in ovaries in some arthropod
groups, such as insects (see Ikuta et al. 2007 for review). In crustaceans, they have been charac-
terized in some branchiopods (Criel 1991, Martin 1992) and in the freshwater ostracod Cyprinotus
uenoi (Ikuta et al. 2007). In branchiopods, the ovarian cells begin as a cluster of four cells, three
of which become “alimentary” or “nurse” cells, aiding in the development of the fourth cell, the
true oocyte (for review, see Criel 1991, Martin 1992). In C. uenoi, the nurse cells originate from
one of the two adjoining germ cells connected by a cytoplasmic bridge in the germarium, and
according to this, these nutritive cells would be similar to those of branchiopod crustaceans and
insects with meroistic ovarioles (Ikuta et al. 2007). These nurse cells thus have the same func-
tion as the trophocytes in insects (Chapman 1998).
There are at least two other kinds of supportive and nutritional cell types in the ovary of
crustaceans that from a functional point of view have “nurse function” for the growing oocyte
but a different origin. Some authors use the term interstitial cells to refer to somatic cells arranged
in a layer along the germarian periphery (Ikuta and Makioka 1997, 2004). According to the
name somatic cells, they can be considered homologous to the follicular cells. In Cephalocarida,
besides the oocytes, epithelial cells that send projections to interdigitate with the germ cells are
found within the ovary, but they are not considered follicle or nurse cells (Hessler et al. 1995).
Finally, an unusual feature of the ovarian morphology has been recently studied in the fresh-
water crayfish Cherax quadricarinatus (Vazquez et al. 2008): the presence of nongerminal areas
functioning as evacuating ducts within the ovary that support the transport of mature oocytes
from the more anterior part of the ovary. This has not been previously reported for any malacos-
tracan species and could be functionally compared with the follicular ducts of the notostracan
Triops cancriformis (Trentini and Sabelli Scanabissi 1982) and possibly with the pedicels or stalks
of the ovarioles in insects (Chapman 1998).
Ovary Function: Growing Oocytes and Cortical Specializations
Oogenesis is an energetically expensive process. Two types of oogenesis have evolved in inver-
tebrates: extraovarian oogenesis and the more common pattern, the intraovarian oogenesis that
involves the retention of oocytes in the ovary until late in development or just prior to spawn-
ing (e.g., echinoderms, mollusks) (Eckelbarger 1994). The latter type of oogenesis is found in
crustaceans, with one single exception. Cephalocarida are unique among crustaceans in that
vitellogenesis does begin not in the ovary but in the middle portion of the oviduct (Hessler
et al. 1995). This type of oogenesis, which corresponds to the extraovarian oogenesis, involves
the release of oocytes from the ovary early during development (before vitellogenesis begins),
and it is found, for example, in polychaetes, where vitellogenesis occurs in the coelomic space
(Eckelbarger 1994).
Two major phases are recognized during oogenesis: the proliferative phase, representing
the mitotic activity of the oogonia, and the growing phase, involving the growth of the oocyte.
The growing phase involves the synthesis mainly of proteins by the oocyte in addition to trans-
fer of components from the follicular/nurse cells and from storage organs (e.g., from the liver
in vertebrates, the hepatopancreas in crustaceans, or the digestive glands in molluscans). The
growing phase involves the previtellogenesis, which is characterized by an increase in activ-
ity of various cytoplasmic organelles mainly involved in protein synthesis; this is usually an
extended and gradual process initiated in maturing females. Then, periods characterized by the
accumulation of yolk proteins and by a significant increase in oocyte diameter are referred to
as primary and secondary vitellogenesis. Some yolk proteins are synthesized within the oocytes
while vitellogenin is transported from the hepatopancreas through the hemolymph to the
developing oocytes, sequestered by the growing oocytes, and modified by addition of polysac-
charides and lipids. This process results in the most common form of yolk, named vitellin or
lipovitellin, which provides materials and energy for the embryos until they begin to feed (for
review, see Meusy and Charniaux-Cotton 1984, Tsukimura 2001). Although the main constitu-
ents of vitellin besides water are proteins and lipids, the total amount and the relative quantity
of each component are modulated by the type of development (e.g., direct vs. indirect devel-
opment, planktotrophy vs. lecithotrophy). Furthermore, the embryonic metabolism of these
components is strongly modulated by abiotic factors such as temperature or salinity. Besides
the glycolipoprotein components of the yolk, carotenoids are tetraterpenoids fundamental for
the development of the embryos. They are widespread among different animal taxa, a source of
pro-vitamin A, and involved in antioxidant functions, cellular protection from photodynamic
damage, enhancement of growth, and embryo development (see Li ñá n-Cabello et al. 2002 for
review).
The growing phase of the vitellogenesis is usually studied by the histological analysis of the
ovary and mainly involves the characterization of oocyte size, presence of one or more nucleoli,
and the consistency of the cytoplasm, which is determined by the presence of yolk droplets or
yolk globules (see, e.g., Zerbib 1980, Adiyodi and Subramoniam 1983, Krol et al. 1992, Legrand
and Juchault 1994, Johnson et al. 2001, Kronenberger et al. 2004, Vazquez et al. 2008) (Fig.
15.3A–C).
Cortical differentiation. During oogenesis, the cortical differentiation occurs in the
developing oocytes, resulting in the differentiation of cytoplasmic organelles known as cortical
granules. The cortical granules are membrane-bound structures that accumulate in the cortex
of the oocytes of most animals. They are extruded after fertilization or spawning to form an
envelope or to modify the composition of the vitelline envelope to prevent polyspermy as part
of the cortical reaction and/or to provide a suitable microhabitat for the developing embryo
(Guraya 1982, Hinsch 1990, Rosati 1995). A recent study proposes that, within arthropods, the
presence of these electron-dense bodies/cortical granules represents a plesiomorphic charac-
ter inherited from the arthropod ancestor (Bili ński et al. 2008). This character was retained
in crustaceans, entognathous hexapods, archaeognathans, pycnogonids, and chelicerates and
secondarily lost in pterygote insects and myriapods (Bili ński et al. 2008). In crustaceans, corti-
cal granules have been identified by ultrastructural studies in crabs (Goudeau 1984), marine
lobsters (see Talbot 1991 for review), amphipods (Zerbib 1980), copepods (Blades-Eckelbarger
and Marcus 1992, Santella and Ianora 1992), and penaeid shrimps (Rankin and Davis 1990).
In addition to cortical granules, another cortical specialization named cortical rods is
found in mature oocytes of many penaeid species (for review, see Anderson et al. 1984, Clark
et al. 1990, Rankin and Davis 1990, Khayat et al. 2001). Large jellylike inclusions develop in the
cytoplasm and become externalized in deep cortical crypts around the periphery of the oocyte;
they may constitute up to 10% of the oocyte volume (Fig. 15.3D). The direct contact of the
oocytes with seawater at spawning leads to the expulsion of the cortical rods. The content of the
cortical rods form a “crown” composed of a flocculent matrix around the egg usually named
the jelly coat or the jelly layer. Recent studies have demonstrated that a protein component of
the cortical rods is homologous to insect intestinal peritrophins (Khayat et al. 2001). Because
of the antipathogen activity of this protein, a significant role in the protection of the spawned
eggs against pathogens is proposed (Loongyai et al. 2007). The presence of a jelly coat or the
jelly layer is unusual within arthropods, but it is found in eggs of echinoderms and mollusks
(Rosati 1995).
Oocyte and egg envelopes. In addition to the cytoplasmatic changes during vitellogenesis, all
mature oocytes are surrounded by a fibrous glycoprotein coat that adheres to the plasma mem-
brane; in most cases, it is synthesized almost exclusively by the oocyte. This membrane plays a
key role in the sperm-oocyte interaction, and it is usually named vitelline envelope, vitelline coat,
or fertilization membrane. It is a fibrous network composed of proteins and carbohydrates whose
supramolecular organization and thickness vary slightly from species to species, from a homo-
geneous single layer up to two or three layers (Rosati 1995). The knowledge of vitelline envelope
Fig. 15.3.
(A) Histological section of the ovary showing a primary (PO) and secondary (SO) oocyte in Cherax quadri-
carinatus (Astacida). Y, yolk platelets. (B) Detail of primary oocytes (PO) showing the homogeneous cyto-
plasm and the presence of follicular cells (FC) surrounding them in C. quadricarinatus. SO, secondary oocyte;
Y, yolk platelets. (C) Detail of an advanced primary oocyte (PO) showing the first yolk platelets (Y) within the
cytoplasm. FC, follicular cells. (D) Histological section of the mature ovary of Pleoticus muelleri (Penaeoidea)
showing primary (PO) and secondary (SO) oocytes with the cortical rods (CR) (courtesy of K. Fischbach
and P. Moriondo). (E and F) Transversal section of the oviduct (E) and detail of the wall of the oviduct (F) in
C. quadricarinatus. ME, mesodermic epithelium; SE, secretion from the mesodermic epithelium.
composition, synthesis during the vitellogenesis, and postfertilization modifications in crusta-

ceans is fragmentary. The vitelline envelope has been identified in ostracods (Ikuta and Makioka
1999b, Ikuta et al. 2007), branchiurans (Overstreet et al. 1992), copepods (Blades-Eckelbarger
and Youngbluth 1984), peracarids (Zerbib 1980, W ägele 1992), and decapods (Talbot 1981, Krol
et al. 1992, Rosati 1995, Glas et al. 1997).
Other embryonic coats or egg envelopes surrounding the vitelline envelope have been
reported in many taxa, including crustaceans (Talbot 1991, Hirose et al. 1992, Rosati 1995, Glas
et al. 1997). Secretions of the follicular cells and/or the oviduct epithelium appears to be produc-
ing these coats, whose homologies between taxa are not clearly understood because of differ-
ent nomenclature for each component (Hinsch 1990, Talbot 1991, Hirose et al. 1992, Glas et al.
1997, Saigusa et al. 2002). From a functional point of view, these secondary coats are involved
in embryo protection from microbial, physical, and chemical conditions of the ambient water
while allowing passage of gases (Glas et al. 1997) and providing osmotic protection for embryos
(see Charmantier and Charmantier-Daures 2001 for review). Their structure and permeabil-
ity change during the embryonic period, ensuring not only the protection of the embryo but
also the hatching of the larvae/juvenile (Glas et al. 1997). Branchiopods, most of which produce
some form of resting eggs or cysts, have a very thick external shell to reduce the risk of desicca-
tion. This structurally complex shell is produced by shell glands, cells of the follicular ducts, or
exocytosis of the oocyte. The dormant resting egg usually consists of a thick outer shell and one
or two inner chitin embryonic cuticles (see Martin 1992 and references therein). In species that
incubate their embryos on pleopods, the outer investment coat would also be involved in the
attachment (Saigusa et al. 2002). At least in some decapod species, some pleopodal tegumental
glands or cement glands are suggested to fulfill this function (Fisher and Clark 1983, Talbot
1991). Recently, phylogenetic relationships within Arthropoda have been analyzed based on the
structure of embryonic envelopes, suggesting significant similarities between Myriapoda and
Crustacea (Machida 2006).
Oogenesis in crustaceans has been extensively studied via anatomical and physiological-
endocrinological approaches with the objective of understanding the regulation pathways (see
Fingerman 1997, Tsukimura 2001, Wilder et al. 2002, García et al. 2006, Walker et al. 2006 and
references therein). More recently, evolutionary studies have compared the vitellogenin and
vitellogenin-related proteins of crustaceans with those of other taxa (Zmora et al. 2007, Tiu et al.
2009). Most of these studies have been conducted in Malacostraca, so there is a significant gap in
the knowledge of vitellogenesis in the other crustacean taxa and the regulating role of the nurse
cells/follicular cells during this process. An important aspect in the context of the relationship
to crustacean mating systems is the fact that mating is linked to female molting in some species
(vitellogenesis occurring during the premolt period) but not in others (vitellogenesis occurring
during the intermolt period). The resulting differences in the coordination between molting
and reproduction by the interactive effects of neuropeptides, neurotransmitters, and trophic
hormones make the female function, oogenesis, a more complex process to be analyzed.
Genital Ducts and Seminal Receptacles
The genital ducts are paired or unpaired tubular structures extending from the ovary to the
gonopores. They are also usually named oviducts, but since some authors use this term for the
entire genital duct and others use it for the portion of the genital duct that connects the ovary
with the seminal receptacles (e.g., Hartnoll 1968 for eubrachyuran crabs) or for the portion that
connects the ovary with the brood pouch, ovisac, or “uterus” (e.g., see Martin 1992 for review in
Branchiopoda), here I use the term genital ducts to refer to their function. In this context, genital
ducts transport oocytes from the ovaries to the gonopores, and if fertilization occurs within the
genital duct, they transport oocytes from the ovary to the fertilization place and eggs from the
fertilization place to the gonopores.
According to their origin, the female genital ducts in crustaceans are mesodermic or meso-
ectodermic structures. When they have mesoectodermic origin, the proximal (in relation to the
ovary) part is mesodermic, with the inner epithelium lined to the ovarian epithelium, and the
more distal part is formed by an invagination of the integument, that is, of ectodermic origin.
Although scarcely studied in crustaceans, the mesodermic genital duct or the mesodermic part
of a mixed genital duct usually has secretory function and a muscularized sheath involved in
ovulation (Fig. 15.3E,F) (Adiyodi and Subramoniam 1983, Krol et al. 1992, Martin 1992, Walker
1992, Johnson et al. 2001, Kronenberger et al. 2004, Vazquez et al. 2008), except in Speleonectes
benjamini (Remipedia), where histological differences between ovary and genital duct are not
apparent (Yager 1991). While in Asellus aquaticus (Isopoda) no secretory function is proposed
for the mesodermic genital duct (Erkan 1998), in the caridean shrimp Macrobrachium nippon-
ense the wall of the genital duct seems to be involved in the spawning process, showing a com-
plex dynamism in their cells (Lu et al. 2006). Although the genital ducts are paired in most
crustaceans, a single duct is found in some copepods (Boxshall 1992), and paired (but only one
functional) ducts in branchiurans (Overstreet et al. 1992). In cumaceans, the oviducts of some
species appear for the first time during the parturial molt and disappear between egg deposi-
tions (see Johnson et al. 2001 for review).
Many invertebrates present morphological structures to store spermatozoa or spermat-
ophores, including mollusks, annelids, chelicerates, and insects. In crustaceans, the mor-
phological structures to store spermatozoa/spermatophores are highly diverse, and their
homologies in many cases are not clear, especially within the nonmalacostracans. Paired
or unpaired sperm/spermatophore storage chambers are found in Anostraca (Martin 1992),
Cirripedia (Walker 1992), Copepoda (Boxshall 1992, Corni et al. 2000, Titelman et al. 2007),
Branchiura (Overstreet et al. 1992), Ostracoda (Cohen and Morin 1990, Matzke-Karasz et al.
2009), Isopoda (Wilson 1991, Johnson et al. 2001, Zimmer 2001, Suzuki and Ziegler 2005,
Ziegler and Suzuki 2011), Euphausida (Guglielmo and Costanzo 1983), and Decapoda (Table
15.1) (for review, see Adiyodi and Subramoniam 1983, Bauer 1986, 1991, Wortham-Neal 2002,
Sainte-Marie 2007). In many cases, the sperm/spermatophore storage chambers are differen-
tiated regions of the genital duct, and in other cases they are morphologically separated from
the genital duct. In this context, I use the name seminal receptacles for all structures involved
in sperm/spermatophore storage, regardless of their position, embryonic origin, or relation
with the genital duct.
In an attempt to address the diversity in morphology of the genital ducts and the seminal
receptacles related to sperm transfer, at least four patterns can be recognized in crustaceans:
type I to type IV, representing a range from an “ephemeral” storage mode (sensu Sainte-Marie
2007) to long-term storage.
Type I. This type refers to genital ducts of mesodermic origin and no differentiated seminal
receptacles. Spermatophores are attached to the ventral surface of the female, which is little
modi fied from that of males or juveniles (Fig. 15.4A–C). The female lacks internalized sperm
storage structures, reflecting an ephemeral storage (Sainte-Marie 2007). This type is found in
amphipods (Borowsky 1991), Epicaridea (isopod), anomurans, freshwater crayfish (Astacidae
and Parastacidae), caridean shrimps (Bauer 1986), and stenopodidean shrimps (for review, see
Bauer 1986, Wortham-Neal 2002, Gregati 2009).
Type II. This type indicates genital ducts of mesodermic origin and paired or unpaired ven-
tral invagination(s) of the ventral surface of females forming some kind of ectodermic “pocket”
where spermatophores are deposited (Fig. 15.4A,D–F). The genital ducts open in the gonopores,
and the seminal receptacles open separately. This kind of seminal receptacle has received dif-
ferent names in the different taxa: thelycum (open or closed) in penaeid shrimps, annulus ven-
tralis in Cambaridae, seminal receptacles or spermathecae in marine lobsters and stomatopods,
and spermathecae or thelyca in primitive crabs (for review, see Bauer 1986, 1991, Wortham-Neal
2002, Guinot and Quenette 2005). In decapods, the comparative features of the seminal recep-
tacles, structure of the spermatophore, and morphology of male pleopods have been extensively
Fig. 15.4.
(A) Schematic drawings of type I (right) and type II (left) relationship between seminal receptacles
(SR) and genital duct (GD). Abbreviations: GO, gonopore; OV, ovary; SPF, spermatophore; SR, seminal
receptacle. (B) Sternum without any differentiation, showing where the spermatophore will attach. SR,
seminal receptacle. (C) Sternum in the freshwater crayfish Cherax quadricarinatus (Astacida). GO, gonop-
ore. (D and E) Seminal receptacle (SR) where the spermatophore (SPF) is stored in the marine lobster
Thymops birsteini. GO, gonopore. (F) Seminal receptacle (SR) in the marine shrimp Xiphopenaeus kroyeri
(Penaeoidea) (courtesy of V. Fransozo).
analyzed by Bauer (1986; see chapter 13 in this volume). Two different patterns have been
described. In one form, the genital duct and the seminal receptacle are connected by a thin
bridge, as proposed for the branchiurans Dolops ranarum and Argulus species (Overstreet et al.
1992) and some copepods (Boxshall 1992). In the other form, the genital duct and the seminal
receptacle are not connected, as in ostracods (Maddocks 1992), branchiurans (Overstreet et al.
1992), euphausiids (Guglielmo and Costanzo 1983), penaeid shrimps, marine lobsters (Bauer
1986, 1991), and primitive crabs (see Guinot and Quenette 2005 for review). This anatomical dif-
ference results in different fertilization patterns (internal in the first case and external in the sec-
ond case) (Fig. 15.4A). In copepods, the spermatophore(s) is attached to the female’s urosome,
and the spermatophoric contents empty into the chitin-lined seminal receptacle (Boxshall 1992,
Corni et al. 2000).
Type III. This type represents genital ducts of mesodermic origin with a more or less
expanded mesodermic chamber, the seminal receptacle, where the spermatozoa/spermato-
phores are deposited and fertilization takes place internally (within mesodermic seminal
receptacles) (Fig. 15.5A). According to the schematic drawings of the isopod female genital
anatomy (Wilson 1991), some species could present this pattern as well, while others appear
to have type II. In the sphaeromatid isopod Paracerceis sculpta, the presence of sperm tails in
the spent ovary (Shuster 1989) or within the oviduct (Shuster 1991, Ziegler and Suzuki 2011)
indicates the occurrence of internal fertilization. Since most female sphaeromatids lack sperm
storage organs of ectodermic origin, the presence of sperm within the ovary or the oviduct
would indicate ephemeral sperm storage within the oviduct and in this way type III seminal
receptacle.
Type IV. This type refers to genital ducts of mixed origin and expanded mesoectoder-
mic chambers where spermatophores are deposited and fertilization takes place (internal
fertilization with mesoectodermic seminal receptacles) (Fig. 15.5B). This type is observed
in Cirripedia (Walker 1992), eubrachyuran crabs (for review, see Hartnoll 1968, Guinot and
Quenette 2005, McLay and L ópez Greco 2011), possibly in Anostraca (Martin 1992) (Fig. 15.5C–
F), and in some deep-sea and terrestrial isopods (Wilson 1991, Johnson et al. 2001, Suzuki and
Ziegler 2005).
While most crustacean taxa feature one or maximally two different types of seminal recep-
tacles, all four “designs” can be found among the Isopoda. The morphological diversity of the
reproductive tract and its impact on mating strategies have been related to the aquatic or ter-
restrial habitat of the diverse taxa of isopods (Zimmer 2001). Thus, isopods appear an excellent
model to study phylogenetic trends in sperm storage and the influence of the habitat on the
coevolution of form-function and reproductive behavior.
The anatomical diversity of the seminal receptacles has a profound impact on the evolution
of mating strategies that the species adopt to minimize or avoid the risk of sperm competition
(Wortham-Neal 2002). As stated by Parker (1970) for insects and then later for other taxa (see
Birkhead and Møller 1998 for review), including crustaceans (for review, see Diesel 1991, Wilson
1991, Röder and Linsenmair 1999, Moreau et al. 2002, Wortham-Neal 2002, Suzuki and Ziegler
2005, Sainte-Marie 2007, Sato and Goshima 2007, Titelman et al. 2007), sperm competition can
be defined as the competition between sperm of at least two males for fertilization of the female
oocytes. There is a great potential for sperm competition in species where female store viable
sperm for extended periods in specialized organs and mate with more than one male before
oocytes are fertilized (Parker 1970, Diesel 1991, Wortham-Neal 2002). Sperm priority is often
determined by the morphology of the seminal receptacle (for review, see Parker 1984, Diesel
1991, Röder and Linsenmair 1999), giving an advantage to the “first” male or the “last” male at
mating (Johnson 1982, Shuster 1989, Diesel 1991, Urbani et al. 1998, Gosselin et al. 2005, McLay
and L ópez Greco 2011). Since sperm can compete during an extended time, components of
the seminal receptacles, the transferred spermatophore, and/or the seminal plasma could be
involved in maintenance of sperm viability, maturation, and capacitation (Subramoniam 1995).
The potential for long-term sperm storage has been analyzed mainly in decapods and iso-
pods (for review, see Johnson 1982, Neubaum and Wolfner 1999, Suzuki and Ziegler 2005, Sainte-
Marie 2007). In eubrachyuran crabs, the seminal receptacles contain substantial amounts of
Fig. 15.5.
Crustacean seminal receptacles. (A) Schematic drawings of type III (right) and type IV (left) relation-
ship between seminal receptacles (SR) and genital duct (GD). Abbreviations: GO, gonopore; OV, ovary;
SPF, spermatophore; SR, seminal receptacle. (B and C) General view (B) and detail (C) of the H-shaped
ovaries (OV) and their connection with the seminal receptacles (SR) in Cancer setosus (Brachyura).
GO, gonopore. (D) Histological section showing the connection of the genital duct (or oviduct in
Eubrachyura) to the mesodermic part of the seminal receptacle in Leurocyclus tuberculosus (Brachyura).
The point of connection is indicated with an arrow. ME, mesodermic epithelium of the seminal recep-
tacle (courtesy of X. Gonzalez Pisani). (E) Histological detail of the mesodermic part of the seminal
receptacle showing the secretory epithelium (ME) and the free spermatozoa (SPZ) within the lumen in
Ocypode quadrata (Brachyura). (F) Cuticular layer (CL) of the ectodermic part of the seminal receptacle
stained with toluidine blue after fresh tissue was removed in Leurocyclus tuberculosus (Brachyura) (cour-
tesy of X. Gonzalez Pisani).
proteins and lipids (mainly phospholipids). It has been proposed that these proteins are involved
in sperm nutrition (for review, see Diesel 1991, Anilkumar et al. 1996), sperm stabilization, and
bacterial control (see Sainte-Marie 2007 for review). In the grapsid crab Metopograpsus messor,
the spermathecal fluid may have the function of digesting the spermatophore wall (Anilkumar
et al. 1999). In accordance with the enzymatic profile, aerobic respiration is suggested for the
sperm stored in the seminal receptacles in eubrachyuran crabs (Anilkumar et al. 1996). The bio-
chemical pathways within the seminal receptacles of majoid species maintain the spermatozoa
viable for at least four to six years (see Sainte-Marie 2007 for review). Similarly, in the terrestrial
isopod Armadillidium vulgare, sperm can be stored for more than 15 months, producing viable
embryos without further mating (see Suzuki and Ziegler 2005 for review). In the terrestrial iso-
pod Cubaris murina, up to five broods can be produced from a single mating without a reduction
in brood size (Niemeyer et al. 2009). Further research is needed to better understand the general
metabolic pathways within seminal receptacles in crustaceans.
MALE REPRODUCTIVE SYSTEM
In crustaceans, the male reproductive system is dorsally or dorsolaterally positioned with respect
to the hepatopancreas (Fig. 15.1). The male reproductive system consists of paired testes, which
might be fused or partially joined, and paired genital ducts leading to the gonopores (McLaughlin
1983). Each genital duct consists of a collecting tubule, a vas deferens, and an ejaculatory duct, and
in many species when it is expanded and sperm/spermatophore accumulation occurs, it is usually
named seminal vesicle (not to be confused with the seminal receptacle) or terminal ampoule (Krol
et al. 1992). The male genital system opens to the exterior through simple gonopores, elevated
papillae, or elaborate copulatory structures that are quite variable and therefore are considered
a useful taxonomic character (see also chapter 13). Furthermore, they are an important tool to
understand phylogenetic trends in sperm transfer mainly studied in Decapoda (Bauer 1986, 1991)
and Peracarida (Wilson 2009). As in females, the relative position of the male reproductive system
depends on the body plan (Adiyodi and Subramoniam 1983, McLaughlin 1983). The general con-
dition is a paired reproductive system (Adiyodi and Subramoniam 1983, McLaughlin 1983, Krol
et al. 1992, Johnson et al. 2001). Compared to the females, the morphology of the male reproduc-
tive system is less studied, and the roles of neuropeptides, neurotransmitters, and trophic hor-
mones on spermatogenesis are nearly unknown.
Testes Architecture
Macroscopic Features
Testes are usually characterized according to their form. The most common forms are oval or
elongated (Adiyodi and Subramoniam 1983, McLaughlin 1983, Johnson et al. 2001). In most
crustaceans, they are paired structures, although an unpaired testis (and genital duct) is found
in the Copepoda (Boxshall 1992), some Branchiopoda (Martin 1992), and Ostracoda (Cohen
and Morin 1990) (Table 15.1). In Branchiura, the paired testes are elongated or oval, except in
Dolops, where three lobed testes are found (Overstreet et al. 1992). In the Cirripedia, the paired
testes are diffuse organs scattered throughout the connective tissue of the prosoma (Walker
1992), while in the other taxa, they are compact and clearly “defined” structures. Relative to
their size, the Ostracoda exhibit the largest male reproductive system, achieving one-third of
the body volume (Cohen and Morin 1990). In the Malacostraca, elongated testes are most com-
mon, but some degree of medial fusion is found in decapods, and the presence of testicular lobes
is observed in penaeid shrimps and many crabs (see Krol et al. 1992 for review). The testes of the
Decapoda are generally V-shaped or H-shaped (for review, see Krol et al. 1992, Kronenberger
et al. 2004). More recently, anatomical studies have shown two different patterns in fresh-
water crayfishes: the H-shaped testes of Parastacoidea and the Y-shaped testes of Astacoidea
(Astacidae and Cambaridae) (Hobbs et al. 2007). In the Peracarida, the male reproductive sys-
tem varies among the different orders and sometimes from species to species (see Johnson et al.
2001 for review). Generally, it originates from paired tubes with the sperm-producing tissue or
testes in the anteriormost region. The tubes are unbranched in amphipods, tanaids, and some
isopods, while in other isopods and cumaceans, the testes consist of lobes extending from each
tube (Johnson et al. 2001).
Microscopic Features
Spermatogenesis occurs within the testes, and various names, without a clear definition, are
used to define the morphophysiological unit. Spermatogenesis occurring in clusters has been
reported in the remipede Speleonectes benjamini (Yager (1991), Cephalocarida (Hessler and
Elofsson 1992, Hessler et al. 1995), and Branchiopoda (Martin 1992). Diffuse testes are found in
Cirripedia (Walker 1992). In Rhizocephala, the testis design is the spermatogenic island derived
from the inner and outer mantle epithelia (Høeg 1991), while Grygier (1981) described the testis of
Dendrogaster (Ascothoracida) as consisting of an anastomosing network of tubules. In Isopoda,
each gonad consists of testes follicles (W ägele 1992), while in mysids, spermatocytic sacs arise as
outpocketings of the testicular cords (McLaughlin 1983). In the Decapoda, various expressions
(testicular lobe, testicular lobule, testicular acinii, testicular cysts, and seminiferous tubules)
are used to refer to the anatomical units of spermatogenesis (for review, see Hinsch 1988, Krol
et al. 1992, Moriyasu et al. 2002, Hobbs et al. 2007, Silva-Castiglioni et al. 2008, Erkan et al.
2009); the term testicular lobes is also used in cumaceans and isopods (Johnson et al. 2001).
Within the variety of testes architecture, it is difficult to trace general features, primitive
and derived designs within crustaceans, or homologies between taxa. Nevertheless, two major
designs (seminiferous tubules and testicular lobules) can be recognized in Decapoda based on
the microscopic architecture of the testes (these designs cannot be compared to other crus-
taceans due to lack of information in other taxa). The seminiferous tubule involves a tubular
structure in which, if cut in a transverse plane, the lumen might be seen depending on the game-
togenic stage. From the outer region of the tubule toward the interior lumen, one or two stages of
spermatogenesis can be seen (more immature stages, near the base and more advanced near the
center). This would be similar to the spermatogenesis in Amniota, in which a centripetal gradi-
ent of maturity can be recognized and sperm release occurs toward the lumen of the seminifer-
ous tubule. While spermatozoa are seen in the lumen, spermatogonia and/or spermatocytes are
seen in the outer region of the tubule. The lumen of the seminiferous tubule leads into the vas
deferens. Usually, the developmental stages are synchronized within a particular region of the
testes (see Krol et al. 1992 for review), and thus in a histological slide, many sections of similar
spermatogenic development are found. This is also named restricted testes by Grier (1993) and is
observed in some penaeid and caridean shrimps and in brachyuran crabs (Boddeke et al. 1991,
Krol et al. 1992, García and Silva 2006, Simeó et al 2009) (Fig. 15.6). In other taxa, the testicular
lobules or testicular acinii design involves rounded “pockets” where spermatogenesis occurs,
with each lobule being connected to the collecting tube or testicular lumen. Each testicular unit
contains cells in a single stage of spermatogenesis, and sperm release occurs toward the collect-
ing tube of the testes, which connects to the lumen of the vas deferens. Usually, each lobule or
acinus shows one stage of spermatogenesis regardless of the different stages occurring in the
adjacent lobes. Accordingly, this is termed unrestricted testes (Grier 1993). This pattern is found
Fig. 15.6.
Seminiferous tubules. (A and B) Histological section of the testes in Xiphopenaeus kroyeri (Penaeoidea)
(courtesy of V. Fransozo), showing general view of testes (A) and detail of the seminiferous tubule (ST)
(B). SPC, spermatocytes; SPZ, spermatozoa. (C) Seminiferous tubule (ST) in Rhynchocinetes typus
(Caridea). L, lumen; SPZ, spermatozoa. (D) Seminiferous tubule (ST) with spermatids (SPT) showing
the presence of many Sertoli cells (SC) in the basis of the tubule in Zilchiopsis collastinensis (Brachyura).
in Astacida (Hobbs et al. 2007, L ópez Greco et al. 2007, Silva-Castiglioni et al. 2008 for review),
except in Astacus leptodactylus (Erkan et al. 2009) and in Aegla species (Anomura) (Sokolowicz
et al. 2007) (Fig. 15.7). This design is similar to that in mysids, where “spermatocytic sacs arise as
outpocketings of the testicular cords” (McLaughlin 1983, 37).
Besides the germ cells, other cell types are usually found in the testes: accessory, nurse,
Sertoli, Sertoli-like, follicular, intercalary, epithelial, or sustentacular cells (see Hinsch 1993
for review). However, knowledge about their embryological origin, differentiation, and regula-
tion is scarce. These cells are found in Branchiopoda, Copepoda, Cirripedia, Peracarida, and
Decapoda, where they are involved in various processes. They seem to regulate sperm numbers
in the testis by phagocytizing excess spermatids, producing flocculent material that surrounds
the sperm in the spermatophore and eliminating excess cytoplasm during spermatogenesis (see
Hinsch 1993 for review). Furthermore, these cells are also proposed to be involved in the syn-
thesis of microtubules rather than in nutrition in Peracarida (see Johnson et al. 2001 for review).
In Hutchinsoniella macracantha (Cephalocarida), epithelial cells extend centripetally to form
thin septae between clusters of sperm cells, but they are not considered accessory cells (Hessler
et al. 1995).
Spermatogenesis in crustaceans follows the general trend found in other taxa but is quite vari-
able, as reflected in the great diversity of spermatozoa morphology and motility (Pochon-Masson
Fig. 15.7.
Testicular lobules. (A and B) Histological section of the testes in a longitudinal plane of a young male of
Cherax quadricarinatus (Astacida) showing the connection of the testicular lobules (TL) to the testicular
lumen (L) as rounded pockets (A) and detail of a lobule with spermatozoa (SPZ) connected to the testicu-
lar lumen (B). SPC, spermatocytes. (C) Histological section of the testes in a longitudinal plane of a big
male of C. quadricarinatus where the connection of the testicular lobule (TL) to the testicular lumen is not
evident. SPZ, spermatozoa. (D) Histological section of the testes in a transversal plane of Aegla uruguayen-
sis (Anomura). L, testicular lumen; TL, testicular lobule.
1994). For example, in the Ostracoda alone, eight different sperm types have been characterized
(Cohen and Morin 1990), and two types in Copepoda (Boxshall 1992). Another particularity
found in Ostracoda is the presence of “giant” sperm (Cohen and Morin 1990, Matzke-Karasz et al.
2009). This is an ancient feature in Ostracoda, according to the fossil record (Matzke-Karasz
et al. 2009). Giant sperm occur in many groups scattered throughout the animal kingdom, and
this feature is considered a sexual selection mechanism in species without postmating parental
investment (Miller and Pitnick 2002, Bjork and Pitnick 2006, Matzke-Karasz et al. 2009). Large
sperm are also found in the sphaeromatid isopod Paracerceis sculpta; in this species, males no
larger than 7 mm transfer several hundred 1-mm-long sperm within 30 s (Shuster 1989). As in other
taxa, the spermatozoan diversity is considered a useful tool to analyze phylogenetic relationships
(for review, see Jamieson 1991, Buckland-Nicks and Scheltema 1995, Tudge 1995, Jamieson and
Tudge 2000, Tudge 2009, Wilson 2009), but knowledge of the possible relationships between
spermatozoon morphology and mechanisms of gamete recognition at penetration of oocyte

envelopes or fertilization is scarce.
Genital Ducts and Accessory Glands
The genital ducts and male accessory glands exhibit a great variety of design within crusta-
ceans; the vas deferens or the seminal vesicle is usually the most developed region in decapods
(Krol et al. 1992) and peracarids (Johnson et al. 2001), respectively. Secretions from the vas
deferens are involved in formation of the spermatophore(s) layer(s) and production of semi-
nal plasma, in sperm maturation (Subramoniam 1995), and as lubricating agents (Hessler et al.
1995). Mainly in the Cirripedia and Brachyura, the amount of seminal plasma is conspicuous
in the same way as in advanced insect species. While the brachyuran seminal plasma aids in
the transfer of spermatophores, in cirripedes free spermatozoa are found in the seminal plasma
(Subramoniam 1993, 1995). High proteolytic and antibacterial activities have been detected in
the seminal plasma of Scylla serrata, and different functions have been suggested: degradation
of the sperm plug, protecting the male reproductive tract against microorganisms, and possibly
antibacterial functions during the prolonged storage of spermatozoa in the seminal receptacles
(Jayasankar and Subramoniam 1997, 1999). The seminal plasma is also thought to be involved
in the nutrition of spermatozoa both within the male and female tracts, being a heterogeneous
matrix mainly composed of proteins, carbohydrates, and lipids (Subramoniam 1993).
The histological differentiation of the epithelium of the vas deferens and the seminal vesicle
has been studied in many species (Krol et al. 1992, Subramoniam 1995, Johnson et al. 2001). The
epithelial cells mainly secrete mucoprotein or mucopolysaccharides (Subramoniam 1993, 1995
and references cited therein, Johnson et al. 2001) (Fig. 15.8). Based on its complexity and its role
in spermatophore formation, the vas deferens can be divided into 3–10 distinct regions that usu-
ally involve macroscopic differences related to size or degree of folding of the different parts
(Krol et al. 1992). However, in some species, such as in Artemia, no differences are seen in the
structural components along the vas deferens, with the exception of a varying diameter, depend-
ing on the amount of sperm (Martin 1992). In Hutchinsoniella macracantha (Cephalocarida), the
vas deferens is a simple tube of uniform appearance lacking muscles, widened portions, or glands
over its entire length (Hessler et al. 1995). While the proximal zone of the vas deferens is usu-
ally highly secretory, the more distal zone usually presents a more muscularized tunica involved
in spermatozoa/spermatophore release during mating (Krol et al. 1992, Avenant-Oldewage and
Swanepoel 2005).
The accumulation of spermatophores or spermatozoa occurs in an expanded area of the
distal part of the genital duct named seminal vesicle or terminal ampoule found in peracarids
(see Johnson et al. 2001 for review), ostracods (Cohen and Morin 1990, Maddocks 1992),
branchiurans (Overstreet et al. 1992), and many decapods (Krol et al. 1992), where it is specially
developed in penaeid shrimps (Bauer 1986, 1991, Bauer and Cash 1991). According to W ägele
(1992) and Johnson et al. (2001), the seminal vesicle in isopods is located in the anterior part of
the vas deferens. In anostracans, accessory glands, each consisting of nearly 20 cell pairs located
anterolateral to the tip of the penis, have been reported (reviewed by Martin 1992). A suggested
function for the neutral mucoprotein secretion is lubrication and sperm plug activator for fertili-
zation (Martin 1992). The anatomical position of these glands is similar to the accessory glands
in insects, which generally arise from the ejaculatory duct and are involved in forming the
spermatophore (Chapman 1998). Some ostracods (Sigilloidea and Cypridoidea) have a unique
differentiation of the genital duct named Zenker’s organ. In these taxa, part of the vas deferens
is reinforced with muscles to form an ejaculatory pump that acts during mating (Cohen and
Morin 1990, Maddocks 1992).
Fig. 15.8.
Male reproductive systems. (A) Reproductive system of Rhynchocinetes typus (Caridea) showing tes-
tis (T) and vas deferens (VD). (B) Histological section of the vas deferens of Rhynchocinetes typus con-
taining spermatozoa (SPZ) and scarce amount of secretion. EVD, epithelium of the vas deferens. (C)
Reproductive system of Cherax quadricarinatus (Astacida) showing testes (T) and vasa deferentia (VD).
(D) Histological section of the vas deferens of Cherax quadricarinatus showing the secretory epithelium
(EVD). (E) Reproductive system of Cancer setosus (Brachyura) showing testes (T) and vasa deferentia
(VD). (F) Histological section of the vas deferens showing the secretory epithelium (EVD) and the sper-
mazoa (SPZ) in Zilchiopsis collastinensis (Brachyura).
Spermatophores
A common feature that has evolved among invertebrates for sperm transfer is the production
of sperm packets called spermatophores (Hinsch 1991, Subramoniam 1993). In crustaceans,
spermatophores are widespread, and they are placed either externally on the surface of the
female’s body or internally into the seminal receptacles (Bauer 1986; see also Subramonian 1993,
Wortham-Neal 2002, and chapter 13 in this volume). Crustacean spermatophores are transmit-
ted directly to the females, in contrast to many terrestrial arthropods with indirect transfer
mechanisms (Subramoniam 1991).
But what is a spermatophore? As stated by Bauer (1991), the term spermatophore has been
used variably by different authors. Bauer (see Bauer 1986, 1991 for review) referred to spermato-
phores as the structures that are emitted by the male during copulation containing sperma-
tozoa and the surrounding protective and adhesive components from the vas deferens. He
recognized preformed spermatophores and spermatophoric masses, with the latter being the
unstructured contents extruded from the vas deferens as an adherent net of sperm plus crystal-
line fibers found in Leptestheria dahalacensis (Conchostraca) (Scanabissi and Mondini 2000)
and the sperm bundles of the peracarids (Johnson et al. 2001). Other authors (for review, see
Hinsch 1991, Subramoniam 1991, 1993, Longo and Musmeci 2002) defined the spermatophore by
the presence of one or more layers surrounding the sperm mass, defining clear discrete units of
sperm transfer that are recognizable within the vas deferens.
Knowledge about crustacean spermatophores has been summarized by Subramoniam (1993).
They have been extensively reviewed in copepods (Hosfeld 1994, Corni et al. 2000), peracarids
(Itaya 1979, Johnson et al. 2001, Longo and Musmeci 2002), and decapods (Bauer 1991, Bauer and
Cash 1991, Hinsch 1991, Subramoniam 1993, Tudge 1997, 1999a, 1999b). The morphological diver-
sity of spermatophores, origin of components, and hardening mechanisms have been compared
and summarized in Hinsch (1991) and Subramoniam (1991, 1993 and references cited therein),
and the comparative features between spermatophores of crustaceans and other arthropods are
summarized in Subramoniam (1991).
If defined by function (spermatozoa transference) and not from a morphological point
of view, the spermatophore concept discussed in Bauer (1986, 1991) would be better suited to
understand different “designs” for spermatozoa transfer and its relation with mating strategies,
external versus internal fertilization, and time between spermatophore transfer, dehiscence,
and ovulation. Within this framework, some generalizations can be made about the occurrence
and function of spermatophores. The presence or function of spermatophores is not diagnostic
of a given taxon (Fig. 15.9). For example, within Ostracoda, some families have spermatophores
while others do not (Cohen and Morin 1990). Similarly, in most Isopoda, the spermatozoa are
organized into unsheathed bundles that function as spermatophores (for review, see Itaya 1979,
Johnson et al. 2001, Longo and Musmeci 2002, Wilson 2009), but Ligia italica presents a mul-
tilayered and rigid wall around the sperm bundle, which might be related to a more effective
sperm protection (Longo and Musmeci 2002). In freshwater crayfishes, species from the families
Cambaridae and Astacidae have a more complex spermatophore than those of the Parastacidae,
among which in particular the South American species show a simple spermatophore without
layers surrounding the spermatozoa (Noro et al. 2007, L ópez Greco and Lo Nostro 2008). While
most anomurans have complex spermatophores of the pedunculate or ribbonlike type (Bauer
1986, Hinsch 1991, Subramoniam 1991, 1993, Tudge 1997, 1999a, 1999b), aeglids also lack layers sur-
rounding the spermatozoa (see Sokolowicz et al. 2007 for review). In penaeid shrimps, females
with open thelyca generally receive a spermatophore with complicated sperm-free accessory
structures (e.g., the so-called wings), whereas in the close-thelyca species the males produce
simpler spermatophores (for review, see Bauer 1986, 1991, Subramoniam 1993).
Fig. 15.9.
Crustacean spermatophores. (A and B) Spermatophores (SPF) within the distal vas deferens of
Rhynchocinetes typus (Caridea) (A) and detail of the spermatophore with scarce amount of secretory (S)
components (B). SPZ, spermatozoa. (C and D) Spermatophore (SPF) within the distal vas deferens of
Cherax quadricarinatus (Astacida) (C) and detail of the spermatophore with abundant amount of secre-
tory (S) components (D). SPZ, spermatozoa. (E and F) Spermatophores (SPF) within the distal vas defer-
ens: with seminal plasma in Neohelice granulata (Brachyura) (E), and in Xiphopenaeus kroyeri (Penaeoidea)
(F). S, secretion of the vas deferens; SPZ, spermatozoa (courtesy of V. Fransozo).
In the same sense, unrelated groups can share similar morphology of the spermatophores.
For example, the elliptic spermatophores of the eubrachyuran crabs are similar to those of the
closed-thelycum penaeid species Xiphopenaeus kroyeri (Fransozo 2008) (Fig. 15.9E,F). This
does not appear to be related to the fertilization type, since eubrachyuran crabs have internal
fertilization and penaeid shrimps have external fertilization. In species with internal fertilization,
the adhesive components are reduced, as in the spermatophores of the eubrachyurans.
In species with external fertilization, the complexity of the spermatophore appears related
to the time involved between spermatophore transfer and ovulation. For example, in caridean
and stenopodidean shrimps in which sperm transfer is closely coupled with ovulation, the
spermatophore is very simple, without a sheath surrounding spermatozoa, and the amount of
secretion is scarce (for review, see Bauer 1986, Subramoniam 1993, Gregati 2009). In marine
lobsters, complex spermatophore sheaths seem to bear a direct relation with the time the
spermatophore is attached to the female (Hinsch 1991). According to Subramoniam (1993),
spermatophore hardening in palinurid lobsters might have evolved in response to shallow and
turbulent conditions where a soft spermatophore would be washed off. The complexity of the
spermatophore wall could be related to a protective function for the maintenance of the sper-
matozoa. Stabilizing processes such as hardening, blackening, chitinization, and phenolic
tanning occur in the spermatophores of many crustacean species where the spermatophore
is attached to the female (for review, see Hinsch 1991, Subramoniam 1991, 1993). Furthermore,
in species with internal fertilization, the complexity of the spermatophore wall appears to be
related to the time between mating and the dehiscence of spermatophores. In the eubrachy-
uran crab Chionoecetes opilio two types of spermatophores were found. Those with smooth
and thin walls are used for immediate fertilization of oocytes at mating. In contrast, those
with wrinkled spermatophoric walls are stored within the seminal receptacle for posterior
fertilizations (Moriyasu and Benhalima 1998). In the same majoid species, Sainte-Marie and
Sainte-Marie (1999) describe segregative processes for spermathecal storage of the various
types of amorphous matter and spermatophores. That study also describes for the first time
the presence of one type of spermatophore not carrying spermatozoa but spermatids, and
thus spermiogenesis would not occur in the male reproductive system but in the female’s
seminal receptacles (Sainte-Marie and Sainte-Marie 1999). By contrast, in some Grapsoidea
and Ocypodoidea, spermatophores within the seminal receptacles are rare, probably due to a
quick dehiscence after sperm transfer (L ópez Greco et al. 2009).
As stated by Subramoniam (1993), the morphology and method of spermatophore trans-
fer are so varied that it is difficult to draw conclusions about phylogenetic relationships
within crustaceans. Possibly an ecological approach addressing the environment (aquatic or
terrestrial), type of fertilization, position of the spermatophore, relationship between ovula-
tion and molting, and spermatophore dehiscence could be useful to better understand the
evolution of different types of spermatophores and modes of sperm transfer. In this con-
text, it appears particularly promising to explore the relationship between spermatophore
traits (composition, shape, transfer mechanisms) and mating systems in crustaceans. The
Isopoda would be a very interesting taxon to explore how sperm-bundle form, dehiscence,
and sperm viability might be related to the various forms of seminal receptacles found in the
females of different isopod taxa.
THE GONADS OF HERMAPHRODITES AND SPECIES WITH INTERSEX FORMS
Hermaphrodites are found in several crustacean taxa, including the Cephalocarida, some spe-
cies of Artemia, Remipedia, Cirripedia, many Tanaidacea, and within the Decapoda in many
caridean shrimps and freshwater crayfish (Parastacidae) (Table 15.1). In those species, one
individual may develop both female and male reproductive systems, either sequentially or
simultaneously. In Cephalocarida, the genital ducts of the ovaries and testes join in a common
genital duct (Hessler and Elofsson 1992, Hessler et al. 1995), whereas independent genital ducts
and gonopores for both reproductive systems are the usual pattern in the other taxa. While
Cephalocarida, Remipedia, and Cirripedia are simultaneous hermaphrodites, protogyny is
found in some Tanaidacea (Highsmith 1982) and in the intertidal isopod Gnorimosphaeroma
oregonense (Brook et al. 1994). Different patterns of protandric hermaphroditism are present in
Caridea and Parastacidae (for review, see Bauer 2000, Chiba 2007, Baeza 2008, Laubenheimer
and Rhyne 2008). In the hermaphroditic species of caridean shrimp and crayfish, an ovotestis
is the usual gonad type. The more anterior part of the ovotestis corresponds to the ovary and
produces oocytes, and the posterior part of the ovotestis corresponds to the testis, producing
sperm. This ovotestis has paired female and male genital ducts. Besides hermaphrodites, the
presence of intersex individuals has been reported from several crustacean species, mainly in
the Parastacidae (Sagi et al. 1996, Rudolph and de Almeida 2000), Hippidae (Subramoniam and
Gunamalai 2003), Diogeneidae (Fantucci et al. 2008), Amphipoda (McCurdy et al. 2004, 2008),
Isopoda (McCurdy et al. 2004), and Mysidae (Yamashita et al. 2001). An intersex individual usu-
ally presents one single type of gonad (either ovaries or testes) but both pairs of gonoducts and
gonopores. Thus, intersex females and intersex males are characterized by the presence of ova-
ries and testes, respectively. In intersex females the female gonoduct is more developed, while in
intersex males the male gonoduct is more developed. In many of these species, only a small pro-
portion of individuals are intersexes, with the exception of the South American Parastacidae,
in which intersexuality is common (Rudolph and De Almeida 2000). Recently, and mainly in
amphipods, it has been suggested that the presence of intersexes is caused by endocrine disrup-
tors (see Ford et al. 2004, 2008 for review). Other factors such as microparasites or environmen-
tal cues could also be involved (McCurdy et al. 2004).
COEVOLUTION OF FEMALE AND MALE REPRODUCTIVE SYSTEMS
Given the large and often parallel variability in both female and male reproductive systems,
there is little doubt that both systems have coevolved to maximize reproduction under a variety
of environmental and population demographic conditions. This female/male coevolution is one
of the least explored aspects in the functional anatomy of reproductive systems in crustaceans.
When comparing external versus internal fertilization, the latter is indeed an advantage
because the sperm is transferred directly to the female system increasing fertilization poten-
tial and reducing the risk of sperm competition. In this context, the evolution of copulatory
structures is favored. However, internal fertilization also opens the risk of sexually transmitted
diseases, particularly dangerous in polyandrous species, but this has not yet been studied in
crustaceans. Mating right after the female molt might at least reduce the risk of diseases accu-
mulating and transferring from the female to the male. In hard-shell mating, a mobile or immo-
bile operculum (Hartnoll 1968) becomes soft only during the mating season. The operculum
opens the gonopore for the time required for mating, closing off the female reproductive tract
against environmental threats outside the mating season (especially in intertidal and more ter-
restrial decapods).
The presence of sperm storage chambers allows females to accumulate sperm from one
or more matings. This provides genetic variability for their offspring and possibly also min-
imizes predation risk because females can mate under safe conditions and might not have
to mate again for each new brood. It also enhances her reproductive opportunities at low
density. Large seminal receptacles permit accumulation of large amounts of sperm and/or
long-term sperm storage. However, one “cost” arising from long-term sperm storage is that
viability and quality of sperm need to be ensured over extended time periods. How long can
females maintain the sperm viable, and how can they achieve and control this? One way could
be to accumulate spermatids and several spermatophores with different dehiscence times, as

found in Chionoecetes opilio (Moriyasu and Benhalima 1998, Sainte-Marie and Sainte-Marie
1999). Providing nourishment to the spermatozoa from the secretory activity of the epithe-
lium of the seminal receptacles and large amounts of secretion are also possible solutions.
This requires the evolution of specific biochemical pathways within the storage chambers to
ensure sperm viability, and it may also have metabolic costs. Furthermore, how can females
“select the best sperm” when they received spermatophores from different males? Does cryp-
tic female choice by sperm selection occur in crustaceans? There is some indication that it
does, as discussed in the following paragraph.
It can be expected that the opportunity of multiple mating leads to adaptations in the ana-
tomical design of storage structure and mechanisms. Once the possibility of sperm storage
within the seminal receptacles has evolved, females may benefit from mating with multiple
males, while males themselves suffer from sperm competition. The risk of sperm competition
may then be followed by the evolution of specialized copulatory structures and behaviors or
structures for pre- and/or postcopulatory mate guarding or mate plugs, which might return
some control over fertilizations to the males (Diesel 1991, Jivoff 1997, Rorandelli et al. 2008).
But what are the “costs” for males in attempting to minimize sperm competition? As stated by
Rondeau and Sainte-Marie (2001, 213), “Sperm economy is predicted by sperm competition
theory for species like the snow crab in which polyandry exists, mechanisms of last-male sperm
precedence are effective, and the probability that one male fertilizes the female’s lifetime pro-
duction of eggs is small.” Increasing mating encounters or “topping off ” the seminal receptacle
with sperm is also a feasible way for males when facing sperm competition. This would require
the production of large amounts of sperm. The proportional size of the testes or sperm size in
closely related species might be an indicator of the risk of sperm competition, similar to that
found in other taxa (for review, see Parker and Ball 2005, Lüpold et al. 2009). Ostracoda, with
the largest reproductive system (Cohen and Morin 1990), and giant sperm, both in Ostracoda
(Cohen and Morin 1990, Matzke-Karasz et al. 2009) and in the sphaeromaid isopod Paracerceis
sculpta (Shuster 1989), are excellent models to test these strategies of counteracting the risk of
sperm competition in crustaceans. In Ostracoda, such energy investment when “size really does
matter” has been proposed as a consequence of strong sperm competition (Matzke-Karasz et al.
2009). Super sperm need large seminal receptacles to store them, and this is probably the “rea-
son” for the unique ejaculatory pump named Zenker’s organ. In the ostracod Eucypris virens,
multiple mating events are proposed to occur during the reproductive lifetime of the female,
although the sex ratio is strongly female biased (Vandekerkhove et al. 2007).
If fertilization is external, males (and females) not only face the risk of sperm competition
but also need to avoid premature loss of the spermatophore: how to design the “sperm package”
to ensure the paternity of the offspring? It is to be expected that optimal packaging has evolved,
which might also involve physiological and morphological adaptations in the male reproduc-
tive tract, especially in the seminal vesicle and/or the vas deferens. Prolonged latency until
fertilization and more complex spermatophores are expected. And is there an optimal relation
among spermatophore size, number of spermatozoa per spermatophore, and number of sper-
matophores? The huge anatomical diversity and reproductive patterns found within and across
crustacean taxa offer excellent opportunities to study these questions.
FUTURE DIRECTIONS
Looking forward, this brief review of the reproductive anatomy of crustaceans shows that more
detailed and comparative studies are needed. These include the study of (a) morphological
diversity, (b) embryology, (c) functional anatomy and integrative principles, and (d) neurohor-
monal pathways.
Crustaceans show a very high diversity in the morphology of their reproductive system,
which has scarcely been studied in nonmalacostracans and only in selected malacostracans.
Comparative studies are necessary to address questions related to the evolution of general and
particular designs, as well as primitive and advanced patterns. In Caridea, for example, these
anatomical studies have solved questions about gonochorism or hermaphroditism in some spe-
cies (Espinoza-Fuenzalida et al. 2008, Terossi et al. 2008, Braga et al. 2009, Lacoursière-Roussel
and Sainte-Marie 2009). This basic information is necessary to understand the morphofunc-
tional features of the reproductive system, which then can be used as a tool for phylogenetic
analysis.
The study of the embryological development of the reproductive system involving the origin
and position of the germ and accessory cells is key to understanding the differences between
and within taxa and for comparative analyses within arthropods. The embryological approach
would allow identifying true homologies between taxa and accordingly help to avoid the confu-
sion caused by different names for the same structures or vice versa.
The anatomy of the reproductive system and the appendages involved in sperm transfer have
evolved to ensure fertilization and minimize the risk of sperm competition. The study of form
is essential to understand the anatomical constraints for physiology and behavior. Likewise, the
synchronization between the activation of sperm in the spermatophores and the receptivity of
the female and the driving factors have not been studied in detail in the context of sperm com-
petition. Within this framework of female-male reproductive anatomy and sperm competition,
complex sexual systems are found in crustaceans, and these are only recently being unveiled
(Sainte-Marie 2007). As stated by Wortham-Neal (2002) and Titelman et al. (2007), studies
on reproductive morphology in a phylogenetic context can show how reproductive structures,
mating behaviors, and fertilization mechanisms have coevolved. This will help us understand
evolutionary trends within the arthropods and their relationship with their morphological and
ecological diversity.
Regulation pathways of gametogenesis are essential to understand the general trends of neu-
rohormonal control within arthropods, including sexual differentiation. Although oogenesis
has been extensively studied mainly in malacostracans, studies on spermatogenesis are scarce
and would be particularly interesting in those species with ontogenetic sex change. The study of
the neurohormonal pathways will also improve the integrative understanding about the action
and impact of endocrine disruptors.
SUMMARY AND CONCLUSIONS
This chapter has presented an overview of the different designs of female and male reproduc-
tive organs involving gonads and gonoducts. The anatomical “architecture” of the crusta-
cean reproductive system is highly variable. Two different positions of germaria and growing
oocytes (reverse positions) are similar to those found in other arthropods. There are at least
two types of “accessory cells,” follicular cells and nurse cells, and they have different embry-
onic origins and participate in a wide variety of tasks, including vitellogenesis and the synthe-
sis of oocyte envelopes. In males, lobular and tubular testes designs resemble those of other
taxa. Sertoli-like cells as accessory cells are involved in regulation of sperm number, elimina-
tion of excessive cytoplasm during spermiogenesis, and synthesis of microtubules. The role of
the Sertoli-like cells is little studied in nonmalacostracans groups. The genital ducts in both
females and males also show large variability of designs related to their functions in gamete
transport, sperm maturation, and sperm storage. In this context, the Isopoda are suggested as
one of the more interesting groups for studying the evolution of sperm storage. They comprise
a huge anatomical diversity in storage structures, which is apparently partly driven by the envi-
ronment. Sperm packaging (e.g., within the spermatophores) is a little explored aspect with
interesting evolutionary perspectives. Phylogenetic studies using these reproductive charac-
ters will gain value with the examination of the reproductive system in more taxa. Finally, the
neurohormonal pathways of reproduction in both gonochoristic and hermaphroditic species
require further research to understand the real relation between morphology and physiology
of crustacean reproduction. Hermaphroditic and intersex species are excellent models to eval-
uate the effect of endocrine disruptors and mechanism involved in sexual differentiation that
are also scarcely studied.
ACKNOWLEDGMENTS
I thank Dr. Kyosuke Ikuta (Department of Biology, Osaka Kyoiku University, Japan) and
Dr. Daniel Roccatagliata (Department of Experimental Biology, University of Buenos Aires,
Argentina) for providing bibliography, my students Ana Bugnot and Fernanda Vazquez for their
help with drawings and mounting photographs, and Martin Thiel and Les Watling for their
comments and suggestions to improve the manuscript. I am most grateful to all authors who
allowed me to use their previously unpublished images.
REFERENCES
Adiyodi, R.G., and T. Subramoniam . 1983. Arthropoda—Crustacea. Pages 443–495 in K.G. Adiyodi and
R.G. Adiyodi, editors. Reproductive biology of invertebrates: Oogenesis, oviposition, and oosorp-
tion. John Wiley and Sons, Chichester, UK .
Aflalo, E.D., T.T. Hoang , V.H. Nguyen, Q. Lam, D.M. Nguyen, Q.S. Trinh, S. Raviv, and A. Sagi. 2006. A
new two-step procedure for mass production of all-male populations of the giant freshwater prawn
Macrobrachium rosenbergii. Aquaculture 256:468 –478.
Anderson, S.L., E.S. Chang , and W.H. Clark Jr. 1984 . Timing of vitellogenic ovarian changes in the ridge-
back prawn Sicyonia ingentis (Penaeidae) determined by ovarian biopsy. Aquaculture 42:257–271.
Ando, H., and T. Makioka. 1998. Structure of the ovary and mode of oogenesis in a freshwater crayfish,
Procambarus clarkii (Girard). Zoological Science 15:863–901.
Anilkumar, G., K. Sudha, E. Anitha, and T. Subramoniam. 1996. Aspects of sperm metabolism in the
spermatheca of the brachyuran crab Metopograpsus messor (Forsk å l). Journal of Crustacean Biology
16:310 –314.
Anilkumar, G., K. Sudha, and T. Subramoniam. 1999. Spermatophore transfer and sperm structure in
the brachyuran crab Metopograpsus messor (Decapoda, Grapsidae). Journal of Crustacean Biology
19:361–370.
Avenant-Oldewage, A., and J.H. Swanepoel. 2005 . The male reproductive system and mechanism of
sperm transfer in Argulus japonicus (Crustacea: Branchiura). Journal of Morphology 215:51–63.
Baeza, J.A. 2008. Protandric simultaneous hermaphroditism in the shrimps Lysmata bahia and Lysmata
intermedia. Invertebrate Biology 127:181–188.
Barki, A., I. Karplus, I. Khalaila, R. Manor, and A. Sagi. 2003. Male-like behavioral patterns and physi-
ological alterations induced by androgenic gland implantation in female crayfish. Journal of
Bauer, R.T. 1986. Phylogenetic trends in sperm transfer and storage complexity in decapod crustaceans.
Bauer, R.T. 1991. Sperm transfer and storage structures in penaeoid shrimps: A functional and phyloge-
netic perspective. Pages 183–207 in R.T. Bauer and J.W. Martin, editors. Crustacean sexual biology.
Bauer, R.T. 2000. Simultaneous hermaphroditism in caridean shrimps: A unique and puzzling sexual
system in the Decapoda. Journal of Crustacean Biology 20:116 –128.
Bauer, R.T., and C.E. Cash. 1991. Spermatophore structure and anatomy of the ejaculatory duct in
Penaeus setiferus, P. duorarum and P. aztecus (Crustacea, Decapoda): Homologies and functional
significance. Transactions of the American Microscopical Society 110:144–162.
Bergström, B.I. 1997. Do protandric pandalid shrimp have environmental sex determination? Marine
Biology 128:397–407.
Bili ń ski, S., B. Szyma ń ska, and K. Miyazaki. 2008. Formation of an egg envelope in the pycnogonid,
Propallene longiceps (Pycnogonida, Callipallenidae). Arthropod Structure and Development
37:155–162.
Birkhead, T.R., and A. P. Møller. 1998. Sperm competition and sexual selection. Academic Press, San
Diego, CA.
Bjork , A., and S. Pitnick. 2006. Intensity of sexual selection along the road to isogamy. Nature
441:742–745.
Blades-Eckelbarger, P.I., and N.H. Marcus. 1992. The origin of cortical vesicles and their role in egg enve-
lope formation in the “spiny” eggs of a calanoid copepod, Centropages velificatus. Biological Bulletin
182:41–53.
Blades-Eckelbarger, P.I., and M.J. Youngbluth. 1984 . The ultrastructure of oogenesis and yolk formation
in Labidocera aestiva (Copepoda: Calanoida). Journal of Morphology 179:33–46.
Boddeke, R., J.R. Bosschieter, and P.C. Goudswaard. 1991. Sex change, mating, and sperm transfer in
Crangon crangon (L.). Pages 164–182 in R.T. Bauer and J.W. Martin, editors. Crustacean sexual biol-
ogy. Columbia University Press, New York.
Borowsky, B. 1991. Patterns of reproduction of some amphipod crustaceans and insights into the nature
of their stimuli. Pages 33–49 in R.T. Bauer and J.W. Martin, editors. Crustacean sexual biology.
Boxshall, G.A. 1992. Copepoda. Pages 347–384 in A.G. Humes and F.W. Harrison, editors. Microscopic
anatomy of invertebrates. Crustacea, Vol. 9. Wiley-Liss, New York.
Braga, A., L.S. L ópez Greco, D.C. Santos, and A. Fransozo. 2009. Morphological evidence for protan-
dric simultaneous hermaphroditism in the caridean Exhippolysmata oplophoroides. Journal of
Brook , H.J., T.A. Rawlings, and R.W. Davies. 1994 . Protogynous sex change in the intertidal isopod
Gnorimosphaeroma oregonense (Crustacea: Isopoda). Biological Bulletin 187:99 –111.
Buckland-Nicks, J., and A. Scheltema. 1995 . Was internal fertilization and innovation of early Bilateria?
Evidence from sperm structure of a mollusk. Proceedings of the Royal Society of London Series B
261:11–18.
Chapman, R.F. 1998. The insects: Structure and function. Cambridge University Press, London.
Charmantier, G., and M. Charmantier-Daures . 2001. Ontogeny of osmoregulation in crustaceans: The
embryonic phase. American Zoologist 41:1078 –1089.
Charniaux-Cotton, H. 1954 . Découverte chez un crustacé amphipode (Orchestia gammarella) d’ une
glande androgène responsable de la différenciation des charactères sexuels primaries et secondar-
ies. Comptes Rendus de l’Académie des Sciences (Paris) 239:780 –782.
Charniaux-Cotton, H., and G. Payen. 1988. Crustacean reproduction. Pages 279–303 in H. Laufer
and R.G. Downer, editors. Endocrinology of selected invertebrate types. Alan R. Liss ,
New York.
Chiba, S. 2007. A review of ecological and evolutionary studies on hermaphroditic decapod crustaceans.
Plankton and Benthos Research 2:107–119.
Clark Jr., W.H., A.I. Yudin, J.W. Lynn, F.J. Griffin, and M.C. Pillai. 1990. Jelly layer formation in penaeoi-
dean shrimp eggs. Biological Bulletin 178:295–299.
Cohen, A.C., and J.G. Morin . 1990. Patterns of reproduction in ostracodes: A review. Journal of
Corni, M.G., V. Vigoni, and F. Scanabissi. 2000. Ultrastructural aspects of the reproductive morphol-
ogy and spermatophore placement of Centropages kroyeri Giesbrecht, 1892 (Copepoda, Calanoida).
Criel, G.R.J. 1991. Morphology of Artemia. Pages 119–153 in R.A. Browne, P.A. Sorgeloos, and C.N.A.
Trotman, editors. Artemia biology. CRC Press, Boca Raton, FL.
Cui, Z.X., H. Liu, T.S. Lo, and K.H. Chu. 2005 . Inhibitory effect of the androgenic gland on ovarian
development in the mud crab Scylla paramamosain. Comparative Biochemistry and Physiology
140:343–348.
Diesel, R. 1991. Sperm competition and the evolution of mating behavior in Brachyura, with special
reference to spider crabs (Decapoda, Majidae). Pages 145–163 in R.T. Bauer and J.W. Martin, editors.
Crustacean sexual biology. Columbia University Press, New York.
Eckelbarger, K.J. 1994 . Diversity of metazoan ovaries and vitellogenic mechanisms: Implications for life
history theory. Proceedings of the Biological Society of Washington 107:193–218.
Elorza, A., and E. Dupré. 1999. Arquitectura del ovario de la langosta de Juan Fernandez ( Jasus frontalis).
Investigaciones Marinas 28:175–194.
Erkan, M.B. 1998. Ultrastructural study on the ovarian wall and the oviduct of the Asellus aquaticus
(Crustacea: Isopoda). Turkish Journal of Zoology 22:351–362.
Erkan, M., Y. Tunali, and S. Sancar-Bas. 2009. Male reproductive system morphology and spermato-
phore formation in Astacus leptodactylus (Eschscholtz, 1823) (Decapoda: Astacidae). Journal of
Espinoza-Fuenzalida, N.L., M. Thiel, E. Dupré, and J.A. Baeza . 2008. Is Hippolyte williamsi gonochoric
or hermaphroditic? A multi-approach study and a review of sexual systems in Hippolyte shrimps.
Fantucci, M.Z., R. Biagi, and F.L.M. Mantelatto. 2008. Intersexuality in the western Atlantic hermit crab
Isocheles sawayai (Anomura: Diogenidae). Journal of the Marine Biological Association of the UK
68:1–3.
Fingerman, M. 1997. Roles of neurotransmitters in regulating reproductive hormone release and
gonadal maturation in decapod crustaceans. Invertebrate Reproduction and Development
31:47–54.
Fisher, W.S., and W.H. Clark Jr. 1983. Eggs of Palaemon macrodactylus: I. Attachment to the pleopods and
formation of the outer investment coat. Biological Bulletin 164:189 –200.
Ford, A.T., T.F. Fernandes, S.A. Rider, P.A. Read, C.D. Robinson, and I.M. Davies. 2004 . Endocrine dis-
ruption in a marine amphipod? Field observations of intersexuality and de-masculinisation. Marine
Environmental Research 58:169 –173.
Ford, A.T., C. Sambles, and P. Kille. 2008. Intersexuality in crustaceans: Genetic, individual and popula-
tion level effects. Marine Environmental Research 66:146 –148.
Fransozo, V. 2008. Morfologia dos caracteres sexuais secundá rios e caracterização gonadal masculina
em Xiphopenaeus kroyeri (Heller, 1862) (Crustacea, Dendrobranchiata, Penaeoidea). MSc thesis,
Universidade Estadual Paulista, Botucatu, São Paulo, Brasil .
Garc ía, C.F., C. Cunningham, J.L. Soulages, H.A. Garda, and R. Pollero. 2006. Structural characteriza-
tion of the lipovitellin from the shrimp Macrobrachium borelli. Comparative Biochemistry and
Garc ía, T.M., and J.R.F. Silva. 2006. Testis and vas deferens morphology of the red-clawed mangrove
tree crab (Goniopsis cruentata) (Latreille, 1803). Brazilian Archives of Biology and Technology
49:339 –345.
Ginsburger-Vogel, T., and H. Charniaux-Cotton. 1982. Sex determination. Pages 257–281 in L.G. Abele,
editor. The biology of crustacea, Vol. 2, Genetics. Academic Press, New York.
Glas, P.S., L.E. Courtney, J.R. Rayburn, and W.S. Fisher. 1997. Embryonic coat of the grass shrimp
Palaemonetes pugio. Biological Bulletin 192:231–242.
Gosselin, T., B. Sainte-Marie, and L. Bernatchez. 2005 . Geographic variation of multiple paternity in the
American lobster, Homarus americanus. Molecular Ecology 14:1517–1525.
Goudeau, M. 1984 . Fertilization in a crab. Cytodifferentiation of vesicles enclosing ring-shaped elements
involved in the cortical reaction. Gamete Research 9:409 –424.
Gregati, R.A. 2009. Estudo da morfologia funcional reprodutiva e desenvolvimiento larval em labo-
ratório de Stenopus hispidus (Olivier, 1811) (Crustacea, Decapoda, Stenopodidea). PhD dissertation,
Universidade Estadual Paulista, Botucatu, São Paulo, Brasil.
Grier, H. 1993. Comparative organization of Sertoli cells including the Sertoli cell barrier. Pages 703–739
in L. Rusell and M. Griswold, editors. The Sertoli cells. Cache River Press, Clearwater, FL.
Grygier, M.J. 1981. Sperm of the ascothoracican parasite Dendrogaster, the most primitive found in
Crustacea. International Journal of Invertebrate Reproduction 3:65–73.
Guglielmo, L., and G. Costanzo. 1983. Diagnostic value of the thelycum in euphausiids. II. Oceanic spe-
cies. Genera Bentheuphausia, Nyctiphanes, Pseudeuphausia, Tessarabrachion, and Nematobrachion.
Journal of Crustacean Biology 3:278 –292.
Guinot, D., and G. Quenette. 2005 . The spermatheca in podotreme crabs (Crustacea, Decapoda,
Brachyura, Podotremata) and its phylogenetic implications. Zoosystema 2:267–342.
Guraya, S.S. 1982. Recent progress in the structure, origin, composition and function of cortical granules
in animal eggs. International Review of Cytology 78:257–360.
Hartnoll, R.G. 1968. Morphology of the genital ducts in female crabs. Journal of the Linnean Society
47:279 –300.
Hasegawa, Y., E. Hirose, and Y. Katakura. 1993. Hormonal control of sexual differentiation and reproduc-
tion in Crustacea. American Zoologist 33:403–411.
Hessler, R.R., and R. Elofsson. 1992. Cephalocarida. Pages 9–24 in A.G. Humes and F.W. Harrison, edi-
tors. Microscopic anatomy of invertebrates. Crustacea, Vol. 9. Wiley-Liss, New York.
Hessler, R.R., R. Elofsson, and A.Y. Hessler. 1995 . Reproductive system of Hutchinsoniella macracantha
(Cephalocarida). Journal of Crustacean Biology 15:493–522.
Highsmith, R.C. 1982. Sex reversal and fighting behavior: Coevolved phenomena in a tanaid crustacean.
Ecology 64:719 –726.
Hinsch, G. 1988. Morphology of the reproductive tract and seasonality of reproduction in the golden crab
Geryon fenneri from the eastern Gulf of Mexico. Journal of Crustacean Biology 8:254–261.
Hinsch, G. 1990. Arthropoda-Crustacea. Pages 121–155 in K.G. Adiyodi and R.G. Adiyodi, editors.
Reproductive biology of invertebrates, Vol. 4, Part B, Fertilization, development and parental care.
Wiley and Sons, New York.
Hinsch, G. 1991. Structure and chemical content of the spermatophores and seminal fluid of reptan-
tian decapods. Pages 290–307 in R.T. Bauer and J.W. Martin, editors. Crustacean sexual biology.
Hinsch, G. 1993. Comparative organization and cytology of Sertoli cells in invertebrates. Pages 660–683
in L. Russell and M. Griswold, editors. The Sertoli cells. Cache River Press, Clearwater, FL.
Hirose, E., H. Toda, Y. Saito, and H. Watanabe. 1992. Formation of the multiple-layered fertilization
envelope in the embryo of Calanus sinicus Brodsky (Copepoda: Calanoida). Journal of Crustacean
Biology 12:186 –192.
Hobbs, H., Jr., C. Harvey, and H. Hobbs. 2007. A comparative study of functional morphology of male
reproductive system en the Astacidae with emphasis on the freshwater crayfish (Crustacea,
Decapoda). Smithsonian Contributions to Zoology, Vol. 624. Smithsonian Institution,
Washington, DC.
Høeg , J.T. 1991. Functional and evolutionary aspects of the sexual system in the Rhizocephala
(Thecostraca: Cirripedia). Pages 208–227 in R.T. Bauer and J.W. Martin, editors. Crustacean sexual
biology. Columbia University Press, New York.
Hosfeld, B. 1994 . On sperm ultrastructure, spermiogenesis and the spermatophore of Heterolaophonte
minuta (Copepoda, Harpacticoida). Zoomorphology 114:195–202.
Ikuta, K., and T. Makioka . 1997. Structure of the adult ovary and oogenesis in Argulus japonicus Thiele
(Crustacea: Branchiura). Journal of Morphology 231:29 –39.
Ikuta, K., and T. Makioka . 1999a . Evolution of ovarian structure and oogenesis in maxillopodan
crustaceans. Pages 91–100 in F.R. Schram and J.C. von Vaupel Klein, editors. Crustaceans and the
biodiversity crisis. Proceedings of the Fourth International Crustacean Congress, Amsterdam, The
Netherlands, 20–24 July 1998, Vol. 1. Brill, Leiden.
Ikuta, K., and T. Makioka . 1999b. Ovarian structure and oogenesis in the myodocopid ostracod Vargula
hilgendorfii. Journal of Crustacean Biology 19:730 –737.
Ikuta, K., and T. Makioka . 2004 . Structure of ovary and oogenesis in the halocyprid ostracod Conchoecia
imbricata. Journal of Crustacean Biology 24:72–80.
Ikuta, K., F. Maruo, T. Tsutsumi, and T. Makioka. 2007. Structure of the ovary and “nurse cells” in a
freshwater ostracod, Cyprinotus uenoi Brehm (Podocopida: Cypridoidea). Zoological Science
24:906 –912.
Itaya, P.W. 1979. Electron microscopic investigation of the formation of spermatophores of Armadillidium
vulgare. Cell and Tissue Research 196:95–102.
Jamieson, B.G.M. 1991. Ultrastructure and phylogeny of crustacean spermatozoa. Memoirs of the
Queensland Museum 31:109 –142.
Jamieson, B.G.M., and C.C. Tudge. 2000. Crustacea-Decapoda. Pages 1–95 in B.G.M. Jamieson, editor.
Progress in male gamete ultrastructure and phylogeny. Reproductive Biology of the Invertebrates,
Vol. 9, Part C. John Wiley and Sons, Chichester, UK .
Jayasankar, V., and T. Subramoniam. 1997. Proteolytic activity in the seminal plasma of the mud crab,
Scylla serrata (Forskal). Comparative Biochemistry and Physiology 116:347–352.
Jayasankar, V., and T. Subramoniam. 1999. Antibacterial activity of seminal plasma of the mud crab Scylla
serrata (Forskal). Journal of Experimental Marine Biology and Ecology 236:253–259.
Jivoff, P. 1997. The relative roles of predation and sperm competition on the duration of the
post-copulatory association between the sexes in the blue crab, Callinectes sapidus. Behavioral
Ecology and Sociobiology 40:175–185.
Johnson, C. 1982. Multiple insemination and sperm storage in the isopod Venezillo evergladensis Schultz,
1963. Crustaceana 42:225–232.
Johnson, W.S., Stevens, M., and L. Watling. 2001. Reproduction and development of marine peracari-
dans. Advances in Marine Biology 39:105–260.
Khayat, M., P.J. Babin, B. Funkenstein, M. Sammar, H. Nagasawa, A. Tietz, and E. Lubzens. 2001. Molecular
characterization and high expression during oocyte development of a shrimp ovarian cortical rod
protein homologous to insect intestinal peritrophins. Biology of Reproduction 64:1090–1099.
Krol, R.M., W.E. Hawkins, and R.M. Overstreet. 1992. Reproductive components. Pages 295–343 in
A.G. Humes and F.W. Harrison, editors. Microscopic anatomy of invertebrates. Crustacea, Vol. 10.
Wiley-Liss, New York.
Kronenberger, K., D. Brandis, M. Turkay, and V. Storch. 2004 . Functional morphology of reproductive
system of Galathea intermedia (Decapoda: Anomura). Journal of Morphology 262:500 –516.
Lacoursière-Roussel, A., and B. Sainte-Marie . 2009. Sexual system and female spawning frequency in the
sculptured shrimp Sclerocrangon boreas (Decapoda: Caridea: Crangonidae). Journal of Crustacean
Biology 29:192–200.
Laubenheimer, H., and A.L. Rhyne. 2008. Experimental confirmation of protandric simultaneous her-
maphroditism in a caridean shrimp outside of the genus Lysmata. Journal of the Marine Biological
Legrand, J.J., and P. Juchault. 1994 . Ontogenèse du sexe et physiologie sexuelle. Pages 631–715 in J.
Forest, editor. Traité de Zoologie, Tome VII, Crustacés, Fascicule 1, Morphologie, Physiologie,
Reproduction, Embryologie. Masson, Paris.
Legrand, J.J., E. Legrand-Hamelin, and P. Juchault. 1987. Sex determination in Crustacea. Biological
Reviews of the Cambridge Philosophical Society 62:439 –470.
Li ñá n-Cabello, M.A., M. Paniagua, and P.M. Hopkins. 2002. Bioactive roles of carotenoids and retinoids
in crustaceans. Aquaculture Nutrition 8:299 –309.
Longo, G., and R. Musmeci. 2002. Ultrastructural characteristics of the spermatophore in Isopoda
Oniscidea (Crustacea). Italian Journal of Zoology 69:1–11.
Loongyai, W., J.C. Avarre, M. Cerutti, E. Lubzens, and W. Chotigeat. 2007. Isolation and functional char-
acterization of a new shrimp ovarian peritrophin with antimicrobial activity from Fenneropenaeus
merguiensis. Marine Biotechnology 9:624–637.
L ópez Greco, L.S., and F.L. Lo Nostro. 2008. Structural changes of the spermatophore in the freshwater
“red claw” crayfish Cherax quadricarinatus (von Martens, 1898) (Decapoda, Parastacidae). Acta
Zoologica 89:149 –155.
L ópez Greco, L.S., V. Fransozo, M.L. Negreiros-Fransozo, and D. Carvalho. 2009. Comparative
morphology of the seminal receptacles of Ocypode quadrata (Fabricius, 1787) (Brachyura,
Ocypodoidea). Zootaxa 2106:41–50.
L ópez Greco, L.S., F.J. Vazquez , and E. Rodr íguez. 2007. Morphology of the male reproductive system
and spermatophore formation in the freshwater “red claw” crayfish Cherax quadricarinatus
(von Martens, 1898) (Decapoda, Parastacidae). Acta Zoologica 88:223–229.
Lu, J.P., X.H. Zhang , and X.Y. Yu. 2006. Structural changes of oviduct of freshwater shrimp, Macrobrachium
nipponense (Decapoda, Palaemonidae), during spawning. Journal of Zhejiang University 7:64–69.
Lüpold, S., G.M. Linz , J.W. Rivers, D.F. Westneat, and T.R. Birkhead. 2009. Sperm competition selects
beyond relative testes size in birds. Evolution 63:391–402.
Machida, R. 2006. Evidence from embryology for reconstructing the relationships of hexapod basal
clades. Arthropod Systematics and Phylogeny 64:95–104.
Maddocks, R.F. 1992. Ostracoda. Pages 415–441 in A.G. Humes and F.W. Harrison, editors. Microscopic
anatomy of invertebrates. Crustacea, Vol. 9. Wiley, New York.
Makioka, T. 1988. Ovarian structure and oogenesis in chelicerates and other arthropods. Proceedings of
the Arthropodan Embryological Society of Japan 23:1–11.
Manor, R., E.D. Aflalo, C. Segall, S. Weil, D. Azulay, T. Ventura, and A. Sagi. 2004 . Androgenic gland
implantation promotes growth and inhibits vitellogenesis in Cherax quadricarinatus females held in
individual compartments. Invertebrate Reproduction and Development 45:151–159.
Manor, R., S. Weil, S. Oren, L. Glazer, E. Aflalo, T. Ventura, V. Chalifa-Caspi, and A. Sagi. 2007. Insulin
and gender: An insulin-like gene expressed exclusively in the androgenic gland of the male crayfish.
General and Comparative Endocrinology 150:326 –336.
Martin G., R. Raimond, M. Laulier, and P. Juchault. 1996. Ultrastructural and experimental stud-
ies on the androgenic gland in juvenile and puberal males of Sphaeromona serratum (Isopoda,
Flabellifera). Crustaceana 69:349 –358.
Martin, J.J. 1992. Branchiopoda. Pages 25–224 in A.G. Humes and F.W. Harrison, editors. Microscopic
anatomy of invertebrates. Crustacea, Vol. 9. Wiley-Liss, New York.
Matzke-Karasz , R., R.J. Smith, R. Symonova, C. Miller, and P. Tafforeau. 2009. Sexual intercourse
involving giant sperm in Cretaceous Ostracoda. Science 324:1535 .
McCabe, J., and A.M. Dunn. 1997. Adaptive significance of environmental sex determination in
Gammarus duebeni. Journal of Evolutionary Biology 10:515–527.
McCurdy, D.G., M.R. Forbes, S.P. Logan, M.T., Kopec , and S.I. Mautner. 2004 . The functional signifi-
cance of intersexes in the intertidal amphipod Corophium volutator. Journal of Crustacean Biology
24:261–265.
McCurdy, D.G., D.C. Painter, M.T. Kopec, D. Lancaster, K.A. Cook , and M.R. Forbes. 2008.
Reproductive behavior of intersexes of an intertidal amphipod Corophium volutator. Invertebrate
Biology 127:417–425.
McLaughlin, P.A. 1983. Internal Anatomy and physiological regulation. Pages 1–52 in L.H. Mantel, editor.
The biology of Crustacea, Vol. 5. Academic Press, New York.
McLay, C.L., and L.S. L ópez Greco. 2011. A hypothesis about the origin of sperm storage in the
Eubrachyura, the effects of seminal receptacle structure on mating strategies and the evolu-
tion of crab diversity: How did a race to be first become a race to be last? Zoologischer Anzeiger
250:378 –406.
Meusy, J.J., and H. Charniaux-Cotton. 1984 . Endocrine control of vitellogenesis in Malacostraca crusta-
ceans. Pages 231–242 in W. Engels, editor. Advances in invertebrate reproduction, Vol. 3. Elsevier
Science, Amsterdam .
Miller, G.T., and S. Pitnick. 2002. Sperm-female co-evolution in Drosophila. Science 298:1230–1233
Moreau, J., S. Seguin, Y. Caubet, and T. Rigaud. 2002. Female remating and sperm competition patterns
in a terrestrial crustacean. Animal Behaviour 64:569 –577.
Moriyasu, M., and K. Benhalima. 1998. Snow crabs, Chionoecetes opilio (O. Fabricius, 1788) (Crustacea:
Majidae) have two types of spermatophore: Hypotheses on the mechanism of fertilization, and
population reproductive dynamics in the southern Gulf of St. Lawrence, Canada. Journal of Natural
History 32:1651–1665.
Moriyasu, M., K. Benhalima, D. Duggan, P. Lawton, and D. Robichaud. 2002. Reproductive biology of
male Jonah crab, Cancer borealis Stimpson, 1859 (Decapoda, Cancridae) on the Scotian Shelf, north-
western Atlantic. Crustaceana 75:891–913.
Neubaum, D.M., and M.F. Wolfner. 1999. Wise, winsome, or weird? Mechanisms of sperm storage in
female animals. Current Topics in Developmental Biology 41:67–97.
Niemeyer, J.C., V.C. Santos, P.B. Araujo, and E.M. da Silva . 2009. Reproduction of Cubaris murina
(Crustacea: Isopoda) under laboratory conditions and its use in ecotoxicity tests. Brazilian Journal
of Biology 69:137–142.
Noro, C.K., D. Silva-Castiglioni, L. L ópez Greco, L. Buckup, and G. Bond-Buckup. 2007. The morphol-
ogy of spermatophores of Parastacus defossus Faxon, 1898 and P. varicosus Faxon, 1898 and compari-
son within Parastacidae (Crustacea, Decapoda, Parastacidae). Nauplius 15:43–48.
Nørrevang , A. 1983. Pentastomida. Pages 521–533 in K.G. Adiyodi and R.G. Adiyodi, editors.
Reproductive biology of invertebrates, Vol. 1, Oogenesis, oviposition, and oosorption. John Wiley
and Sons, Chichester, UK .
Okumura, T., H. Nikaido, K. Yoshida, M. Kotaniguchi, Y. Tsuno, Y. Seto, and T. Watanabe. 2005 .
Changes in gonadal development, androgenic gland cell structure, and hemolymph vitellogenin
levels during male phase and sex change in laboratory-maintained protandric shrimp, Pandalus
hypsinotus (Crustacea: Caridea: Pandalidae). Marine Biology 148:347–361.
Overstreet , R.M. , I. Dykova , and W. Hawkins. 1992 . Branchiura. Pages 385–413 in A.G. Humes and
F.W. Harrison , editors. Microscopic anatomy of invertebrates. Crustacea, Vol. 9. Wiley-Liss ,
New York.
Parker, G.A. 1984 . Sperm competition and the evolution of animal mating strategies. Pages 1–60 in R.L.
Smith, editor. Sperm competition and the evolution of animal mating systems. Academic Press,
New York.
Parker, G.A. 1970. Sperm competition and its evolutionary consequences in the insects. Biological
Reviews 45:525–567.
Parker, G.A., and M.A. Ball. 2005 . Sperm competition, mating rate and the evolution of testis and ejacu-
late sizes: A population model. Biological Letters 1:235–237
Peixoto, S., G. Coman, S. Arnold, P. Crocos, and N. Preston. 2005 . Histological examination of final
oocyte maturation and atresia in wild and domesticated Penaeus monodon (Fabricius) broodstock.
Aquaculture Research 36:666 –673.
Pochon-Masson, J. 1994 . Les gamétogenèses. Pages 727–783 in J. Forest, editor. Traité de Zoologie,
Tome VII, Crustacés, Fascicule 1, Morphologie, physiologie, reproduction, embryologie. Masson,
Paris.
Rankin, S.M., and R.W. Davis. 1990. Ultrastructure of oocytes of the shrimp, Penaeus vannamei: Cortical
specialization formation. Tissue and Cell 22:879 –893.
Rigaud, T., P. Juchault, and J.P. Mocquard. 1997. The evolution of sex determination in isopod crusta-
ceans. Bioessays 19:409 –416.
R öder, G., and K.E. Linsenmair. 1999. The mating system in the subsocial desert woodlouse, Hemilepistus
elongates (Isopoda Oniscidea): A model of an evolutionary step towards monogamy in the genus
Hemilepistus sensu stricto. Ethology, Ecology and Evolution 11:349 –369.
Rondeau, A., and B. Sainte-Marie. 2001. Variable mate-guarding time and sperm allocation by male snow
crabs (Chionoecetes opilio) in response to sexual competition, and their impact on the mating suc-
cess of females. Biological Bulletin 201:204–217.
Rorandelli, R., F. Paoli, S. Cannicci, D. Mercati, and F. Giusti. 2008. Characteristics and fate of the sper-
matozoa of Inachus phalangium (Decapoda, Majidae): Description of novel sperm structures and
evidence for an additional mechanism of sperm competition in Brachyura. Journal of Morphology
269:259 –271.
Rosati, F. 1995 . Sperm-egg interactions during fertilization in invertebrates. Bollettino di Zoolog ía
62:323–334.
Rossi, F. 1980. Comparative observations on the female reproductive system and parthenogenesis oogen-
esis in Cladocera. Bollettino di Zoolog ía 47:21–38.
Rudolph, E., and A. De Almeida. 2000. On the sexuality of South American Parastacidae (Crustacea,
Decapoda). Invertebrate Reproduction and Development 37:249 –257.
Sagi, A., and I. Khalaila. 2001. The crustacean androgen: A hormone in an isopod and androgenic activity
in decapods. American Zoologist 41:477–484.
Sagi, A., I. Khalaila, A. Barki, G. Hulata, and I. Karplus. 1996. Intersex red claw crayfish, Cherax quad-
ricarinatus (von Martens): Functional males with pre-vitellogenic ovaries. Biological Bulletin
190:16 –23.
Sagi, A., R. Manor, C. Segall, C. Davis, and I. Khalaila. 2002. On intersexuality in the crayfish Cherax
quadricarinatus: An inducible sexual plasticity model. Invertebrate Reproduction and Development
41:27–33.
Sagi, A., E. Snir, and I. Khalaila. 1997. Sexual differentiation in decapod crustaceans: Role of the andro-
genic gland. Invertebrate Reproduction and Development 31:55–61.
Saigusa, M., M. Terajima, and M. Yamamoto. 2002. Structure, formation, mechanical properties and
disposal of the embryo attachment system of an estuarine crab, Sesarma haematocheir. Biological
Bulletin 203:289 –306.
Sainte-Marie, B. 2007. Sperm demand and allocation in decapod crustaceans. Pages 191–210 in J.E. Duffy
and M. Thiel, editors. Evolutionary ecology of social and sexual systems: Crustaceans as model
systems. Oxford University Press, New York.
Sainte-Marie, G., and B. Sainte-Marie. 1999. Reproductive products in the adult snow crab (Chionoecetes
opilio). II. Multiple types of sperm cells and of spermatophores in the spermathecae of mated
females. Canadian Journal of Zoology 77:451–462.
Santella, L., and A. Ianora. 1992. Fertilization envelope in diapause eggs of Pontella mediterranea
(Crustacea, Copepoda). Molecular Reproduction and Development 33:463–469.
Sato, T., and S. Goshima. 2007. Effects of risk of sperm competition, female size and male size on
number of ejaculated sperm in the stone crab Hapalogaster dentata. Journal of Crustacean Biology
27:570 –575.
Scanabissi, F., and C. Mondini. 2000. Sperm transference and occurrence of spermatophore in the
Conchostraca Leptestheriidae (Crustacea: Branchiopoda). Invertebrate Reproduction and
Development 38:99 –106.
Shuster, S.M. 1989. Female sexual receptivity associated with molting and differences in copulatory
behavior among the three male morphs in Paracerceis sculpta (Crustacea: Isopoda). Biological
Bulletin 177:331–337.
Shuster, S.M. 1991. Changes in female anatomy associated with the reproductive moult in Paracerceis
sculpta, a semelparous isopod crustacean. Journal of Zoology 225:365–379.
Silkovsky, J., R. Chayoth, and A. Sagi. 1998. Comparative study of effects of prostaglandin E2 on c-AMP
levels in gonads of the prawn Macrobrachium rosembergii and the crayfish Cherax quadricarinatus.
Silva-Castiglioni, D., L. L ópez Greco, G. Oliveira, and G. Bond-Buckup . 2008. Characterization of the
sexual pattern of Parastacus varicosus Faxon, 1898 (Crustacea: Decapoda: Parastacidae) through
macro and microscopic analysis of its reproductive system. Invertebrate Biology 127:426 –432.
Simeó, C.G., E. Ribes, and G. Rotlant. 2009. Internal anatomy and ultrastructure of the male reproductive
system of the spider crab Maja brachydactyla (Decapoda: Brachyura). Tissue and Cell 41:345–361.
Sokolowicz , C.C., L. L ópez-Greco, R.S. Gonçalves, and G. Bond-Buckup. 2007. The gonads of Aegla plat-
ensis Schmitt through a macroscopic and histological perspective (Decapoda, Anomura, Aeglidae).
Acta Zoologica 88:71–79.
Soranzo, L., R. Stockmann, N. Lautie, and C. Fayet. 2000. Structure of the ovariuterus of the scorpion
Euscorpius carpathicus (L.) (Euscorpiidae) before fertilization. Pages 91–96 in S. Toft and N. Scharff,
editors. Proceedings of the 19th European Colloquium of Arachnology. European Arachnology
2000. Aarhus University Press, Å rhus, Denmark .
Spaziani, E.P., G.W. Hinsch, and S.C. Edwards. 1995 . The effect of prostaglandin E2 and prostaglandin
F2 alpha on ovarian tissue in the Florida crayfish Procambarus paeninsulanus. Prostaglandins
50:189 –200.
Subramoniam, T. 1991. Chemical composition of spermatophores in decapod crustaceans. Pages 308–321
in R.T. Bauer and J.W. Martin, editors. Crustacean sexual biology. Columbia University Press,
New York.
Subramoniam, T. 1995 . Light and electron microscopic studies on the seminal secretions and the vas
deferens of the penaeoidean shrimp, Sicyonia ingentis. Journal of Biosciences 20:691–706.
Subramoniam, T. 1993. Spermatophores and sperm transfer in marine crustaceans. Advances in Marine
Biology 29:129 –214.
Subramoniam, T., and V. Gunamalai. 2003. Breeding biology of the intertidal sand crab, Emerita
(Decapoda: Anomura). Advances in Marine Biology 46:91–182.
Suzuki, S., and K. Yamasaki. 1998. Sex reversal by implantation of ethanol-treated androgenic glands
of female isopods, Armadillidium vulgare (Malacostraca, Crustacea). General and Comparative
Endocrinology 111:367–375.
Suzuki, S., and A. Ziegler. 2005 . Structural investigation of the female genitalia and sperm-storage sites
in the terrestrial isopod Armadillidium vulgare (Crustacea, Isopoda). Arthropod Structure and
Talbot, P. 1981. Collagenase solutions induce in vitro ovulation in lobsters (Homarus americanus). Journal
of Experimental Biology 216:181–185.
Talbot, P. 1991. Ovulation, attachment and retention of lobster eggs. Pages 9–17 in A. Wenner and A.
Kuris, editors. Crustacean egg production. Balkema, Rotterdam.
Terossi, M., L.S. L ópez Greco, and F.L. Mantelatto. 2008. Hippolyte obliquimanus (Decapoda: Caridea:
Hippolytidae): A gonochoric or hermaphrodite species? Marine Biology 154:127–135.
Titelman, J., O. Varpe, S. Eliassen, and O. Fiksen. 2007. Copepod mating: Chance or choice. Journal of
Plankton Research 29:1023–1030.
Tiu, S.H.K., H.L. Hui, B. Tsukimura, S.S. Tobe, J.G. He, and S.M. Chan. 2009. Cloning and expression
study of the lobster (Homarus americanus) vitellogenin: Conservation in gene structure among
decapods. General and Comparative Endocrinology 160:36 –46.
Torfs, P., R. Nachman, C. Poulos, A. De Loof, and L. Schoofs. 2002. Activity of crustacean myotropic
neuropeptides on the oviduct and hindgut of the crayfish Astacus leptodactylus. Invertebrate
Reproduction and Development 41:137–142.
Trentini, M., and F. Sabelli Scanabissi . 1982. Follicle duct cell ultrastructure and egg shell formation in
Triops cancriformis (Crustacea, Notostraca). Journal of Morphology 172:113–121.
Tsukimura, B. 2001. Crustacean vitellogenesis: Its role in oocyte development. American Zoologist
41:465–476.
Tudge, C.C. 1995 . Ultrastructure and phylogeny of the spermatozoa of the infraorders Thalassinidea and
Anomura (Decapoda, Crustacea). Memoires du Museum National d’Histoire Naturelle (Paris)
166:251–263.
Tudge, C.C. 1997. Phylogeny of the Anomura (Decapoda: Crustacea): Spermatozoa and spermatophore
morphological evidence. Contributions to Zoology 67:125–141.
Tudge, C.C. 1999a . Ultrastructure of the spermatophore lateral ridge in hermit crabs (Decapoda,
Anomura, Paguroidea). Crustaceana 72:77–84.
Tudge, C.C. 1999b. Spermatophore morphology in the hermit crab families, Paguridae and
Parapaguridae (Paguroidea, Anomura, Decapoda). Invertebrate Reproduction and Development
35:203–214.
Tudge, C.C. 2009. Spermatozoal morphology and its bearing on decapod phylogeny. In J. Martin, K.
Crandall, and D. Felder editors. Decapod crustacean phylogenetics. Proceedings of a symposium in
San Antonio, Texas, January 2008. Crustacean issues. CRC Press, Boca Raton, FL.
Urbani, N., B. Sainte-Marie, J.M. Sévigny, D. Zadworny, and U. Kuhnlein. 1998. Sperm competition
and paternity assurance during the first breeding period of female snow crab (Chionoecetes opilio)
(Brachyura: Majidae). Canadian Journal of Fisheries and Aquatic Science 55:1104–1113.
Vandekerkhove, J., R. Matzke-Karasz , F. Mezquita, and G. Rossetti. 2007. Experimental assessment of
the fecundity of Eucypris virens (Ostracoda, Crustacea) under natural sex ratios. Freshwater Biology
52:1058 –1064.
Vazquez , F.J., C. Tropea, and L. L ópez Greco. 2008. Differentiation of the female reproductive sys-
tem and the onset of maturity in the freshwater crayfish “red claw” Cherax quadricarinatus (von
Martens, 1898) (Decapoda, Parastacidae) through a macroscopic and microscopic approach.
Invertebrate Biology 127:433–443.
Vogt, G. 2002. Functional anatomy. Pages 53–151 in D.M. Holdich, editor. Biology of freshwater crayfish.
Blackwell Science, Cambridge.
W ägele, J.W. 1992. Isopoda. Pages 529–617 in R.T. Bauer and J.W. Martin, editors. Crustacean sexual
Walker, G. 1992. Cirripedia. Pages 249–311 in R.T. Bauer and J.W. Martin, editors. Crustacean sexual
Walker, A., S. Ando, G.D. Smith, and R.F. Lee. 2006. The utilization of lipovitellin during blue crab
(Callinectes sapidus) embryogenesis. Comparative Biochemistry and Physiology 143:201–208
Wilder, M.N., T. Subramonian, and K. Aida. 2002. Yolk proteins of Crustacea. Pages 131–174 in A.S.
Raikhel and T.W. Sappington, editors. Reproductive biology of invertebrates, Vol. 12, Part A,
Progress in vitellogenesis. Science Publishers, Plymouth, UK.
Wilson, G.D.F. 1991. Functional morphology and evolution of isopod genitalia. Pages 221–245 in R.T.
Wilson, G.D.F. 2009. The phylogenetic position of the Isopoda in the Peracarida (Crustacea:
Malacostraca). Arthropod Systematics and Phylogeny 67:159 –198.
Wortham-Neal, J.L. 2002. Reproductive morphology and biology of male and female mantis shrimp
(Stomatopoda: Squillidae). Journal of Crustacean Biology 22:728 –741.
Yager, J. 1991. The reproductive biology of two species of remipedes. Pages 271–289 in R.T. Bauer and
J.W. Martin, editors. Crustacean sexual biology. Columbia University Press, New York.
Yamashita, Y., T. Okumura, and H. Yamada . 2001. Intersexuality in Acanthomysis mitsukurii (Mysidae) in
Sendai Bay, Northeast Japan. Plankton Biology and Ecology 128:132.
Zerbib, C. 1980. Ultrastructural observation of oogenesis in the crustacean Amphipoda Orchestia gamma-
rellus (Pallas). Tissue and Cell 12:47–62.
Ziegler, A., and S. Suzuki S. 2011. Sperm storage, sperm translocation and genitalia formation in females
of the terrestrial isopod Armadillidium vulgare (Crustacea, Peracarida, Isopoda). Arthropod
Zimmer, M. 2001. Why do male terrestrial isopods (Isopoda: Oniscidea) not guard females? Animal
Zmora, N., J. Trant, S.M. Chan, and J.S. Chung. 2007. Vitellogenin and its messenger RNA during
ovarian development in the female blue crab, Callinectes sapidus: Gene expression, synthesis,
transport and cleavage. Biology of Reproduction 77:136 –146.
16
STRUCTURE OF THE NERVOUS SYSTEM: GENERAL DESIGN
AND GROSS ANATOMY
Jeremy M. Sullivan and Jens Herberholz
Abstract
The myriad behaviors characteristic of crustaceans reflect the diverse lifestyles (pelagic, ben-
thic, terrestrial, parasitic, sessile) of this large taxon. These behaviors are controlled by nervous
systems whose basic structure is conserved across the Crustacea. Crustacean nervous systems
are also characterized by extensive taxon-specific adaptations, including marked reductions
(e.g., sessile barnacles) and increases (e.g., territorial stomatopods) in complexity. This chapter
outlines the organization of the sensory and central nervous systems of the principal crustacean
taxa, highlighting both conserved and specialized features.
INTRODUCTION
The central nervous system (CNS) of crustaceans comprises an anteriorly located brain con-
nected to a ventral nerve cord by two connectives that pass around the esophagus (Fig. 16.1).
The brain consists of three regions, protocerebrum, deutocerebrum, and tritocerebrum, cor-
responding to the three anteriormost elements of the head: the protocerebral/ocular region,
the deutocerebral (antenna I) segment, and tritocerebral (antenna II) segment. Posteriorly
directed circumesophageal connectives connect the brain to the ventral nerve cord. The ven-
tral nerve cord is a ladderlike structure comprising paired segmental ganglia (one pair per
embryonic segment) joined across the midline by anterior and posterior commissures and to
the ganglia of adjacent segments by longitudinal connectives. Three peripheral nerves arise
from each ganglion: the main segmental nerve, a smaller posterior nerve, and the interseg-
mental nerve.
The structure of the ventral nerve cord of many adult branchiopods (e.g., Branchipus,
Anostraca) reflects this basic pattern of organization, laid down in embryogenesis in all
451
A C D E
B F
Fig. 16.1.
Structure of the central nervous system across crustacean taxa. Dashed lines indicate the location of
the circumesophageal connectives connecting the brain and ventral nerve cord. (A) Branchipus venalis
(Branchiopoda, Anostraca). (B) A pedunculate barnacle (Maxillopoda, Cirripedia). (C) Squilla mantis
(Malacostraca, Hoplocarida, Stomatopoda). (D) Mysis relicta (Malacostraca, Mysidacea). (E) Homarus
species (Malacostraca, Decapoda, Homarida). (F) Carcinus species (Malacostraca, Decapoda, Brachyura).
Modified from Bullock and Horridge (1965).
crustaceans (Fig. 16.1A) (Harzsch 2003b). In most crustacean taxa, however, the bilateral gan-
glia of each segment fuse during embryonic development (Fig. 16.1B–F). Fusion of adjacent
segmental ganglia is also characteristic of the ventral nerve cord of many crustaceans, particu-
larly within the Decapoda. This fusion occurs predominantly between the anterior ganglia
of the ventral nerve cord and often reflects the fusion of body segments. Condensation of the
ventral nerve cord is most pronounced in the Brachyura, where the entire cord is fused into a
single ganglionic mass (Fig. 16.1F).
The CNS contains three principal neuronal types: sensory neurons, interneurons, and
motor neurons (Fig. 16.2A). The somata of most sensory neurons are located in the periphery
of the animal and give rise to axons that project to, and branch within, the CNS. The CNS con-
tains the somata of all interneurons and motor neurons. The dendritic branches of interneurons
are entirely restricted to the CNS, though many interneurons possess axons interconnecting
different regions of the CNS. Motor neurons possess somata and dendritic arbors within the
CNS and axons that project via the peripheral nerves to the musculature of the animal.
Within individual ganglia, neuronal somata are clustered around the periphery surrounding
a central neuropil region in which neuronal branches and synapses occur. Synapses are rarely
present on neuronal somata in the crustacean CNS. Crustacean neurons form both chemical
and electrical synapses (Atwood 1982). Chemical synapses are characterized by electron-dense
pre- and postsynaptic membranes and conspicuous presynaptic vesicles. Most presynaptic ter-
minals contain clear synaptic vesicles (30–35 nm in diameter), though a small number possess
both clear and dense-cored vesicles (60–100 nm in diameter) (Govind 1992). Synapses occur
mostly on thin neuronal processes, and input and output synapses are generally distributed
over the same branches without clear spatial segregation (Atwood 1982). Electrical synapses
occur much less frequently in crustaceans than chemical synapses. Electrical communication
Structure of the Nervous System 453
A B ganglionic
sheath
perineurium
basement
glial membrane
sensory cell
blood vessel
neuron
glial cell
glial cell
interneuron neuron soma
glial glial cell

cell
motor neuron neuropil
Fig. 16.2.
Cellular organization of the nervous system. (A) Detail of the brain of the ghost shrimp Calocaris macan-
dreae (Malacostraca, Decapoda) showing the three neuronal cell types present in the crustacean nervous
system (modified from Hanström 1947, with permission from the Royal Physiographic Society, Sweden).
(B) Structural features of the brain of the crab Carcinus maenas (Malacostraca, Decapoda). Asterisks indi-
cate extracellular spaces (modified from Abbott 1970, with permission from Macmillan).
between neurons is mediated by gap junctions located at regions of close (2–5 nm) membrane
apposition (Atwood 1982, Govind 1992). Both rectifying (unidirectional) and nonrectifying
(bidirectional) electrical synapses are present in the crustacean CNS.
The CNS and peripheral nerves of crustaceans are enclosed by an acellular layer of con-
nective tissue, known as the ganglionic sheath or neural lamella (Fig. 16.2B) (Abbott 1971,
Sandeman 1982). The ganglionic sheath overlies a distinct layer, known as the perineurium,
formed by specialized glial cells (Fig. 16.2B) (Abbott 1971, Lane and Abbott 1975). The perineu-
rium is most elaborate in the CNS but is reduced to a single or incomplete cell layer in the
peripheral nerves (Lane and Abbott 1975). Several additional glial types occur within the crus-
tacean CNS, differing in their morphology and distribution (Fig. 16.2B) (Sandeman 1982). The
CNS of malacostracans also contains complex systems of afferent and efferent hemolymph
vessels (Sandeman 1982).
STRUCTURE OF THE SENSORY NERVOUS SYSTEM
Photoreceptors
Compound eyes serve as the visual sense organs of crustaceans and occur in the
Malacostraca, Branchiopoda, Branchiura, and Myodocopida (Ostracoda) but are absent in
other taxa (Shaw and Stowe 1982, Meyer-Rochow 2001). Crustacean eyes are generally stalked
but are sessile in several taxa (e.g., Isopoda, Amphipoda). The compound eye is an array of sen-
sory units, called ommatidia, each with its own optical elements (Fig. 16.3A). The number of
ommatidia comprising the eye varies markedly across the Crustacea, from four in the isopod
Asellus aquaticus (Shaw and Stowe 1982) to several thousand in some terrestrial crabs (Sztarker
A B
Ci Cii D
E F
motorneuron
accessory
neuron
mechanosensory
neuron
receptor
muscle
Fig. 16.3.
Structure of the sensory nervous system. (A) Electron micrograph of the compound eye of Leptodora
kindtii (Branchiopoda, Cladocera) showing the rhabdom (rh), the crystalline cone (cc) of the dioptric
apparatus, and photoreceptor axons (a) emerging from the eye (from Nilsson et al. 1983, with permission
from Springer Science + Business Media). (B) Detail of a longitudinal section through the rhabdom of the
crayfish Procambarus clarkii (Malacostraca, Decapoda) showing the photopigment-containing micro-
villi (from Meyer-Rochow 2001, with permission from the Zoological Society of Japan). (C) Light micro-
graph of the reduced frontal eyes (brain photoreceptors) of the crayfish Cherax destructor (Malacostraca,
Decapoda) (i) and an electron micrograph showing the pigment granules and interdigitating microvillae
characteristic of these cells (ii) (from Sullivan et al. 2009, with permission from the Taylor and Francis
Group). (D) Intracellular labeling of the caudal photoreceptors in the terminal abdominal ganglion of
C. destructor (JM Sullivan, unpublished). (E) An aesthetasc (white arrow) innervated by a cluster of
olfactory receptor neurons (black arrow) in the crayfish Cherax destructor (modified from Sandeman
and Sandeman 1996, with permission from the Company of Biologists, Ltd.). (F) Detail of an abdomi-
nal muscle receptor organ in the crayfish Astacus fluviatilis (modified from Florey and Florey 1955, with
permission from Rockefeller University Press). Scale bars, A and E, 50 μm; B and Cii, 1 μm; Ci, 10 μm; D,
200 μm; F, 100 μm.
et al. 2009). Individual ommatidia are composed of photoreceptors, pigment cells, and cells
contributing to the dioptric apparatus. The number of cells of each type varies across taxa, but
is constant within the eye of each species. The photoreceptors possess specialized membrane
regions (rhabdomeres) consisting of thousands of photopigment-containing microvilli that join
in the center of the ommatidium, forming the rhabdom (Fig. 16.3B). Ommatidia in decapods
and stomatopods contain eight photoreceptors, but the range per ommatidium is 5–16 across the
Crustacea (Oakley 2003). Photoreceptor axons project caudally to the optic ganglia.
The compound eyes of crustaceans are of two types, apposition and superposition, char-
acterized by differing connections between the photoreceptors and the dioptric apparatus
(Meyer-Rochow 2001). While individual ommatidia are optically isolated in apposition eyes,
the structure of the superposition eye enables light to be redirected across ommatidia. The
apposition eye is thought to represent the ancestral structure of the crustacean compound eye,
with superposition eyes evolving subsequently within the Decapoda, Mysidacea, Euphausiacea,
and Anaspidacea (Richter 2002).
In addition to the compound eyes, two other photoreceptor types occur in crustaceans:
frontal eyes and caudal photoreceptors (Meyer-Rochow 2001, Elofsson 2006). The frontal
eyes of crustaceans are simple eyes (ocelli) whose photoreceptors project to the median pro-
tocerebrum in the brain (Fig. 16.3C) (Elofsson 2006). The caudal photoreceptors are a pair
of ascending interneurons whose somata are situated in the terminal abdominal ganglion of
several species of decapods, including blind cave-dwelling species (Fig. 16.3D) (Wilkens 1988).
The axons of the caudal photoreceptors project to the brain, where they terminate in the deu-
tocerebrum (Simon and Edwards 1990).
Olfactory Receptor Neurons
Olfactory cues serve important functions in a variety of crustacean behaviors (e.g., identifica-
tion of food, predators, and mates) and are perceived by olfactory receptor neurons sensitive
to specific odorants (Schmidt and Mellon 2011). Olfactory receptor neurons in carnivorous
crustaceans are particularly sensitive to nitrogen-containing compounds present in their prey
(e.g., amino acids, nucleotides), while those of herbivorous and omnivorous species are sensi-
tive to sugars common to plants, algae, and bacteria and to certain amino acids (Derby and
Sorensen 2008). The active molecules in the chemicals mediating inter- and intraspecific rec-
ognition have not yet been fully characterized. The dendrites of the olfactory receptor neu-
rons innervate specialized cuticular sensillae, known as aesthetascs, arranged along the length
of the olfactory organ, the antennae I (also known as the first antennae or the antennules).
Aesthetascs occur in most crustacean taxa but are absent in the Anostraca, Branchiura, and
adult Cirripedia (Hallberg et al. 1997). While aesthetascs vary across taxa in their fine struc-
ture, they are all characterized by their long, hose-shaped shaft and thin cuticle (Hallberg et al.
1997). The aesthetascs of terrestrial crabs differ from those of aquatic crustaceans, however, in
being shorter and possessing only restricted regions of thin cuticle (Stensmyr et al. 2005).
The number of aesthetascs distributed along the antenna I varies between three to six
in the isopod Asellus aquaticus (Heiman 1984) and approximately 1,800 in the spiny lobster
Panulirus argus (Beltz et al. 2003). Individual aesthetascs are innervated by four to several
hundred olfactory receptor neurons whose somata form discrete clusters within the antenna I
(Fig. 16.3E) (Schachtner et al. 2005). The axons of the olfactory receptor neurons project ipsi-
laterally to the brain, where they terminate within the olfactory lobe glomeruli (Schachtner
et al. 2005). The projections of most olfactory receptor neurons are uniglomerular. The anten-
nae I of some male mysids also possess threadlike sensilla innervated by sensory neurons,
thought to represent pheromone receptors, whose axons project to a male-specific deutocer-
ebral neuropil (Hallberg et al. 1997).
Nonolfactory Chemosensory Neurons
While the aesthetascs and olfactory receptor neurons of the antennae I constitute the olfac-
tory organs of crustaceans, nonolfactory chemosensory neurons innervate a variety of other
setal types on the antennae I, antennae II, mouthparts, esophagus, and pereopods (see also
chapter 6 in this volume). These neurons have been shown to play roles in the identification
and location of food, gustation, grooming behaviors, and certain intraspecific interactions
(Derby and Sorensen 2008). Unlike aesthetascs, most of the setae innervated by nonolfactory
chemosensory neurons also receive innervation from mechanosensory neurons and are thus
bimodal (Cate and Derby 2002). The axons of nonolfactory chemosensory neurons innervat-
ing setae on the antenna I project to the deutocerebrum, while those from the antenna II termi-
nate in the tritocerebrum (Sandeman et al. 1992, Schmidt et al. 1992). Little is known about the
central projections of chemosensory neurons innervating setae on the mouthparts, esophagus,
and pereopods.
Statocyst Sensory Neurons
The statocysts of eumalacostracan crustaceans function as vestibular organs but have also been
proposed to play a role in the monitoring of hydrostatic pressure (Sekiguchi and Terazawa 1997,
Fraser and Takahata 2002). The statocyst is a saclike invagination of the dorsal cuticle contain-
ing mechanosensory setae associated with one or more concretions, the statoliths. Statocyst
setae can be free to move or are cemented to the statolith. The morphology, number, and spa-
tial arrangement of setae within the statocyst vary among species (Sekiguchi and Terazawa
1997). The statocysts of the Decapoda and Anaspidacea are located in the basal segment of
the antenna I, and the axons of sensory neurons innervating statocyst setae project to the deu-
tocerebrum via the antenna I nerve. In contrast, statocysts in the Mysidacea and Isopoda are
situated on the tail fan. Statocyst sensory neurons in these animals project to the terminal
abdominal ganglion.
Hydrodynamic and Tactile Receptors
The cuticle of the body and appendages of crustaceans contain several types of articulated
setae innervated by mechanosensory neurons (typically two) sensitive to setal def lection
by hydrodynamic or tactile stimuli (Govind 1992). Many of these setae are articulated such
that their movement is restricted to a single plane, thus providing directional information.
Individual sensory neurons are typically connected to setae such that they are activated by
setal def lection in only a single direction. Setae sensitive to near-field water movements occur
along the antennae I and II and across the dorsal surfaces of the chelae, cephalothorax, abdo-
men, and tail fan. Tactile setae are widely distributed but are particularly numerous on the
mouthparts and antennae II, where many are also innervated by nonolfactory chemosensory
neurons (see above).
Proprioceptors
Movement and posture in crustaceans are monitored by external and internal propriocep-
tive organs and by sensory neurons monitoring cuticular stress (Govind 1992). External
proprioceptors are collections of innervated setae situated next to articulations or opposing
regions of moveable cuticle and include the cuticular articulated peg organs situated at many
pereopod and maxilliped joints and the hair plates of the antennae II. Internal propriocep-
tive organs are composed of mechanosensory neurons innervating muscle (muscle receptor
organs; Fig. 16.3F), connective tissue strands (chordotonal organs, stretch receptors, oval
organs), or the sheath of the ventral nerve cord (cord stretch receptors). Mechanosensory
neurons also innervate the hypodermis in regions of f lexible cuticle, including the labrum,
anus, and abdomen.
STRUCTURE OF THE BRAIN
The crustacean brain consists of three main regions, the protocerebrum, deutocerebrum, and
tritocerebrum, each associated with a specific sensory structure of the head (Hanström 1947,
Bullock and Horridge 1965, Sandeman et al. 1992, Fanenbruck and Harzsch 2005, Kirsch and
Richter 2007). The protocerebrum receives inputs from the compound eyes, the deutocer-
ebrum from the antennae I, and the tritocerebrum from the antennae II. Each region contains
a number of discrete neuropil regions, soma clusters, and axon tracts (Figs. 16.4, 16.5). Many
of these structures can be recognized across taxa on the basis of their location, structure, and
A B
OGT
PB
PB
CB
CB
LL LAN
OL
DC
AnN
CC CC
C PT D
OGT 6 HB
AMPN
PB
CB 8 ON MI
PMPN ME MT
OGTN 11
MAN
LAN AcN OL
TN 14 AL
17
15 AnN
AnN
oc dorsal view CC
Fig. 16.4.
Diagrams of the principal brain structures. (A) Leptodora kindtii (Branchipoda, Cladocera) (modified from
Kirsch and Richter 2007, with permission from Elsevier). (B) Squilla mantis (Malacostraca, Hoplocarida,
Stomatopoda) (modified from Hanström 1947, with permission from the Royal Physiographic Society,
Sweden). (C) Cherax destructor (Malacostraca, Decapoda, Astacida) (modified from Sandeman et al.
1992, with permission from the Marine Biological Laboratory, Woods Hole, MA). (D) Petrolisthes lamarkii
(Malacostraca, Decapoda, Anomura) (modified from Sandeman et al. 1993, with permission from John
Wiley and Sons). Abbreviations: AcN, accessory lobe; AL, accessory lobe; AMPN, anterior medial pro-
tocerebral neuropil; AnN, antenna II neuropil; CB, central body; CC, circumesophageal connective; DC,
deutocerebrum; HB, hemiellipsoid body; L, lamina ganglionaris; LAN, lateral antenna I neuropil; LL,
lateral lobes; MAN, median antenna I neuropil; ME, medulla externa; MI, medulla interna; MT, medulla
terminalis; OGT, olfactory globular tract; OGTN, olfactory globular tract neuropil; OL, olfactory lobe;
ON, olfactory lobe; PB, protocerebral bridge; PMPN, posterior medial protocerebral neuropil; PT, pro-
tocerebral tract; TN, tegumentary neuropil.
Fig. 16.5.
Anatomy of malacostracan brain neuropils. (A) Synapsin labeling of the hemiellipsoid body of the sto-
matopod Gonodactylus bredini (modified from Sullivan and Beltz 2004, with permission from John Wiley
and Sons). (B) Three-dimensional reconstruction of the central complex of the crayfish Cherax destructor.
The arrows indicate fiber tracts entering and exiting the central body (CB) and lateral lobes (LL); OGT,
olfactory globular tract; PB, protocerebral bridge; W, X, Y, Z, protocerebral fiber tracts; 8, soma cluster
8 (from Utting et al. 2000, with permission from John Wiley and Sons). (C) Central body of the shrimp
Lebbeus groenlandicus (from Strausfeld 2009, with permission from the Royal Society of London). (D and
E) Synapsin labeling of the deutocerebrum of the shrimp Macrobrachium australiense (D) and the lobster
Enoplometopus occidentalis (E). The accessory lobe is particularly complex in E. occidentalis (E), show-
ing both columnar and spherical glomeruli. Asterisks indicate the olfactory globular tract neuropil (JM
Sullivan, unpublished). Scale bars (A and D), 100 μm.
connectivity. The size and complexity of the three brain regions, however, vary markedly across
the Crustacea, often reflecting the importance of particular sensory modalities.
The protocerebrum is situated proximal to the optic ganglia (see below) and in most taxa is
subdivided into two regions: the lateral protocerebrum and median protocerebrum. The two
principal neuropils of the lateral protocerebrum are the medulla terminalis and the hemiel-
lipsoid body (Figs. 16.4D, 16.5A). The medulla terminalis contains several interconnected
neuropil regions (Blaustein et al. 1988) and has been described in a variety of malacostracan
taxa (Hanström 1947). In contrast, the hemiellipsoid body consists of layered or glomeru-
lar neuropil (Sullivan and Beltz 2004) and has been identified in both the Remipedia and
Malacostraca (Fanenbruck and Harzsch 2005). The hemiellipsoid body is particularly promi-
nent and complex in benthic malacostracans but is simpler in pelagic species (Sullivan and
Beltz 2004). The lateral protocerebrum of stomatopods exhibits a high degree of complexity
and contains two additional neuropils: the corpo allungato and corpo reniforme (Hanström
1947, Sullivan and Beltz 2004). The lateral protocerebrum of the banded coral shrimp Stenopus
hispidus (Stenopodidea) also contains a complex of neuropils resembling the corpo allungato
(Sullivan and Beltz 2004).
In most stalk-eyed crustaceans, the lateral protocerebrum is located in the eyestalk and is
joined to the median protocerebrum in the central brain by a large tract, known as the pro-
tocerebral tract. In contrast, the lateral protocerebral neuropils of most sessile-eyed species are
located in the central brain. The median protocerebrum is characterized by three interconnected
neuropils: protocerebral bridge, central body, and lateral lobe, known collectively as the central
complex (Figs. 16.4, 16.5B,C) (Utting et al. 2000). The protocerebral bridge and central body are
unpaired neuropils, situated across the midline of the brain. The lateral lobe is a bilaterally paired
neuropil, known also as the lobus paracentralis. Central complex neuropils have been described
in the Branchiopoda, Remipedia, Copepoda, Branchiura, and Malacostraca (Overstreet et al.
1992, Harzsch 2006). While some studies have identified the protocerebral bridge and central
body in ostracods, others have been unable to locate central complex neuropils in these animals
(Homberg 2008).
The deutocerebrum in most crustacean species is dominated by the olfactory lobe, the target
neuropil of the olfactory receptor neurons of the antenna I, which in most taxa is glomerular in
structure (Figs. 16.4, 16.5D) (Schachtner et al. 2005). The number and size of olfactory glomeruli
vary markedly across decapod taxa, though these differences do not seem to correlate with phy-
logeny, habitat, or lifestyle (Beltz et al. 2003, Schachtner et al. 2005). In most eureptantian deca-
pods, an additional glomerular neuropil, the accessory lobe, lies adjacent to the olfactory lobe
(Figs. 16.4C, 16.5E). Accessory lobes appear to have arisen de novo in the Eureptantia and are
among the most prominent neuropils in the brains of lobsters and crayfish (Blaustein et al. 1988,
Sandeman et al. 1993, Sandeman and Scholtz 1995). In crabs, however, they are greatly reduced in
size and complexity (Fig. 16.4D) (Sandeman and Scholtz 1995). The axons of projection interneu-
rons innervating the olfactory lobe and accessory lobe (when present) form a large tract, known
as the olfactory globular tract (OGT), which in most crustaceans is the most prominent axon
tract of the brain (Fig. 16.4B–D). The OGT characteristically forms a distinct chiasma on the
midline of the brain before projecting bilaterally to the lateral protocerebrum (Hanström 1947,
Sullivan and Beltz 2001b, 2004). The innervation patterns of the OGT within the lateral protocer-
ebrum vary markedly across taxa.
Nonolfactory chemosensory, mechanosensory, and statocyst sensory neurons from
the antenna I terminate in the deutocerebrum within the bilaterally paired lateral antenna
I neuropil (LAN) and the unpaired median antenna I neuropil (MAN) (Fig. 16.4B,C).
While chemosensory neurons largely target the LAN (Schmidt and Ache 1996), statocyst
sensory neurons project primarily to the MAN (Cate and Roye 1997). Mechanosensory neu-
rons in nervate both neuropils (Schmidt and Ache 1996). The LAN dominates the brains
of euphausiids and in Euphausia superba is approximately twice the size of the olfactory lobe
(Hanström 1947, Sandeman et al. 1993). In the Mysida, a small male-specific deutocerebral
neuropil occurs adjacent to the LAN (Johansson and Hallberg 1992). Such sexually dimorphic
neuropils have not been described in other malacostracan taxa.
The tritocerebrum, the caudalmost region of the brain, is separated from the protocer-
ebrum and deutocerebrum in several nonmalacostracan taxa (e.g., Branchiopoda, Ostracoda,
Copepoda) but is fused with the deutocerebrum in most of the Malacostraca. The principal
tritocerebral neuropils are the antenna II neuropil innervated by sensory neurons from the
antenna II (via the antenna II nerve) and the tegumentary neuropil targeted by sensory neurons
from the integument of the head (via the tegumentary nerve; Fig. 16.4B–D).
In contrast to most crustaceans, the CNS of adult cirripedes (Maxillopoda) is greatly
reduced and does not exhibit any evidence of identifiable, structured neuropils (Anderson 1994,
Callaway and Stuart 1999). The brain of the giant barnacle Balanus nubilus, for example, contains
only several hundred neurons (Callaway and Stuart 1999). Ocellar photoreceptors represent the
principal source of sensory inputs to the cirripede brain (Anderson 1994). The axons of these
photoreceptors converge on a single pair of interneurons, known as I-cells (Callaway and Stuart
1999). The brain also contains the somata and dendritic processes of motor neurons innervating
the anterior body musculature (Anderson 1994). Structured brain neuropils are also absent in
the Mystacocarida (Maxillopoda) (Elofsson and Hessler 2005).
STRUCTURE OF THE OPTIC GANGLIA
The optic ganglia of crustaceans are situated proximal to the retina (in those species
with compound eyes) and contain a series of retinotopic neuropils linked by axon tracts
(Fig. 16.6). The number of optic neuropils and their patterns of connectivity differ between
nonmalacostracan and malacostracan taxa. The optic ganglia of nonmalacostracans contain
two retinotopic neuropils: the lamina and medulla (Fig. 16.6A,B). The peripherally located
lamina is innervated by photoreceptors from the compound eye and is connected to the
medulla by uncrossed axons. While all photoreceptor axons in cladocerans and notostracans
appear to terminate in the lamina, one photoreceptor from each ommatidium in anostracans
Fig. 16.6.
Anatomy of the optic ganglia. (A) Section through the eyestalk of the branchiopod Artemia salina
(modified from Wildt and Harzsch 2002, with permission from John Wiley and Sons). (B) Schematic
diagram illustrating the principal cell types of the optic ganglia of A. salina . The lamina is the upper
neuropil (modified from Nä ssel et al. 1978, with permission from Springer). (C) Section through the
optic ganglia of a stomatopod Gonodactylus species showing the lamina ganglionaris. Abbreviations: C,
chiasma; ME, medulla externa; MI, medulla interna (from Marshall et al. 2007, with permission from
Elsevier). Scale bars: A, 20 μm; B, 30 μm; C, 75 μm.
projects to the medulla after giving rise to thin side branches in the lamina (Elofsson and
Hagberg 1986, Strausfeld 2005). Connectivity of the optic neuropils of branchiurans and ostra-
cods has not yet been examined.
Eumalacostracans and stomatopods possess three nested retinotopic neuropils (lam-
ina ganglionaris, medulla externa, medulla interna) linked by successive chiasmata (Fig.
16.6C) (Sandeman 1982, Marshall et al. 2007, Sztarker et al. 2009). The most peripheral
optic neuropil, the lamina ganglionaris, receives retinotopically ordered axonal projections
from the retinal photoreceptors. Seven of the photoreceptor axons from each ommatid-
ium terminate in the lamina ganglionaris, while the eighth projects retinotopically to the
medulla externa. The horizontal order of retinotopic projections in the lamina ganglionaris
is reversed in the second optic neuropil, the medulla externa, by the first (outer) optic chi-
asma. The second (inner) optic chiasma reverses this horizontal order again in the third
optic neuropil, the medulla interna. In some isopods in which the eyes are rudimentary
(e.g., Asellus aquaticus), this second chiasma is absent and the medulla interna indistinct
(Hanström 1947, Elofsson and Dahl 1970). The second optic chiasma is also lacking in
amphipods (Hanström 1947). A fourth optic neuropil, connected to the medulla externa by
uncrossed axons, has been described recently in several species, suggesting that it may be
widespread within the Malacostraca (Strausfeld 2009).
The numbers of optic neuropils and chiasmata in the Phyllocarida have been the subject of
debate. The lamina ganglionaris and medulla externa of phyllocarids are linked by a chiasma
(Sinakevitch et al. 2003). Hanström (1947) described a medulla interna in Nebalia bipes con-
nected to the medulla externa by a chiasma. In contrast, Elofsson and Dahl (1970) found no
evidence of either a second chiasma or medulla interna in this species. A third optic neuropil,
however, has been described in Nebalia pugettensis (Sinakevitch et al. 2003; Nebalia pugetten-
sis was declared a nomen nudum by Martin et al. 1996). This neuropil, called the protolobula,
occurs as an outswelling of the lateral protocerebrum and is linked to the medulla externa by
a chiasma. In Nebalia pugettensis, uncrossed axons from the medulla externa supply a small
fourth optic neuropil (Sinakevitch et al. 2003).
STRUCTURE OF THE STOMATOGASTRIC AND CARDIAC NERVOUS SYSTEMS
Stomatogastric Nervous System
The stomatogastric nervous system (STNS) is an extension of the CNS controlling rhythmic
movements of the esophagus and foregut (Harris-Warrick et al. 1992). The neuroanatomy of
the STNS has been examined most extensively in the Decapoda, but several studies have also
described the STNS of stomatopods (Tazaki 1988). The STNS comprises four interconnected
ganglia: the paired commissural ganglia (CoGs; 300–500 neurons each) and the unpaired sto-
matogastric (STG; 19–32 neurons) and esophageal (OG; 10–16 neurons) ganglia. The CoGs are
situated within the bilateral circumesophageal connectives, the OG on the anterior wall of the
esophagus, and the STG within the ophthalmic artery on the dorsal surface of the stomach. The
somata and dendritic processes of motor neurons innervating the musculature of the esophagus
reside in the CoGs and the OG, while those of motor neurons projecting to the stomach are
located within the STG (cardiac sac, pyloric chamber, gastric mill) and the OG (cardiac sac).
The musculature of the hindgut of decapod crustaceans is innervated primarily by motor
neurons originating in the terminal abdominal ganglion (Elekes et al. 1988). The axons of these
motor neurons project to the hindgut via the unpaired seventh nerve of the ganglion. This nerve
also contains the axon of an unpaired neuron whose soma is situated in the fifth abdominal
ganglion (Kondoh and Hisada 1986).
Cardiac Nervous System
The heart in the Branchiopoda is myogenic and does not contain intrinsic neurons (Cooke
2002), though the heart of Daphnia receives innervation by extrinsic neurons (Bullock and
Horridge 1965). In contrast, the heart of the ostracod Vargula hilgendorfii is neurogenic and is
innervated by one intrinsic and several extrinsic neurons (Ando et al. 2001). The heart in the
Malacostraca is also neurogenic and in most taxa has no endogenous rhythmical properties
(Cooke 2002). The contractile rhythm of the heart musculature in malacostracans is driven by
intrinsic neurons whose somata reside within the cardiac ganglion located on the outer (sto-
matopods, mysids, amphipods) or inner (isopods, decapods) surface of the dorsal heart wall.
The number of neurons within the cardiac ganglion ranges from 5–6 in amphipods to 14–16 in
stomatopods (Alexandrowicz 1954, Ando and Kuwasawa 2004). In most decapods, the cardiac
ganglion contains the somata of four local interneurons and five motor neurons (Cooke 2002).
Activity in cardiac ganglion neurons is modulated by extrinsic excitatory and inhibitory neu-
rons arising from the ventral nerve cord. Additional populations of extrinsic neurons innervate
the arterial and aortic valves.
STRUCTURE OF THE VENTRAL NERVE CORD IN DECAPOD CRUSTACEANS
While the structural organization of the brain is well described for many crustacean species,
this information is not as readily available for the remainder of the CNS. Although the thoracic
and abdominal ganglia of decapod crustaceans have received much experimental attention due
to their accessibility for electrophysiological investigation, most studies have focused on small
neural circuits contained in these ganglia. The imbalance in research efforts is reflected in this
chapter, and our comparative descriptions of the anatomical features of the ventral nerve cord
are inevitably more limited than those of the brain. To compensate for this imbalance, descrip-
tions of the gross anatomy of the nerve cord ganglia will be complemented by descriptions of
three well-studied neural circuits located in these ganglia.
Subesophageal Ganglion
The subesophageal ganglion (SOG), the least investigated of all crustacean ganglia, is a mas-
sive fused structure that develops from six embryonic neuromeres and controls the movements
of the mandibles, maxillae, and maxillipeds (Harzsch 2003b). Homologies between the nerves
arising from the SOG and the peripheral nerves of the thoracic and abdominal ganglia are
unclear (Mulloney et al. 2003); however, some core regions of the SOG conform to the pattern
seen in the more caudal ganglia (Fig. 16.7).
Thoracic Ganglia
The neuroanatomical organization of the thoracic ganglia (T1–T5) has been studied only in a small
number of decapods. The thoracic ganglia innervate the chelae (where present), walking legs,
thoracic musculature, and heart. Each ganglion has three paired nerves, N1–N3: N1 innervates
the chelae or walking legs, N2 the extensor musculature of the thorax, and N3 the thoracic
flexor muscles. The number of axons in N1 varies among ganglia. In crayfish, N1 of the first
thoracic ganglion (innervating the chelae) has the largest number of axons (~80,000), whereas
N1 of T2–T5 (innervating the walking legs) contains about 20,000 axons (Laverack 1988). There
are many more axons in the N1 of the thoracic ganglia than in the N1 of the abdominal gan-
glia (~2400), where this nerve innervates the pleopods. Since the number of motor neurons
Fig. 16.7.
Core anatomy of crayfish ventral nerve cord ganglia, stained with osmium-ethyl gallate: transverse sec-
tions through the neuropil region of the subesophageal ganglion (A), the third thoracic ganglion (B) and
the third abdominal ganglion (C). Abbreviations: aVN, anterior ventral neuropil; HN, horseshoe neuropil;
LN, lateral neuropil; N1, first segmental nerve. Modified from Mulloney et al. (2003), with permission
from John Wiley and Sons.
innervating the legs and pleopods is similar (Faulkes and Paul 1997, Mulloney and Hall 2000),
this difference must be due to a higher number of sensory neurons projecting from the chelae
and walking legs.
The most detailed anatomical description of crustacean thoracic ganglia has been provided
by Elson (1996) for T3 and T4 of the crayfish Pacifastacus leniusculus. The core organization of
thoracic ganglia in crayfish is similar to that of the more completely described abdominal gan-
glia (see below); however, there are also a number of important differences and some interesting
homologies to insects (Fig. 16.7B).
The lateral neuropils (LNs) that receive sensory inputs from the walking legs are much
larger in thoracic ganglia than in abdominal ganglia. This is in agreement with the much larger
number of axons found in N1 of thoracic compared to abdominal ganglia. Bilateral neuropils
located ventral to the base of N1, termed ventral neuropils (Elson 1996), seem to be an exten-
sion of the thoracic homologue of the horseshoe neuropil of the abdominal ganglia (see below).
More anterior and close to the midline of the ganglia, especially dense sensory neuropil struc-
tures are found that receive specific sensory neuron projections via N1. These symmetrical,
“ball”-shaped neuropils, termed anterior ventral neuropils (Elson 1996), are probably elabora-
tions of the horseshoe neuropil, and they have homologues in the SOG (Mulloney et al. 2003).
Anatomical structures similar to the anterior ventral neuropils of crayfish have also been
described in the thoracic ganglia of insects (Pflüger et al. 1988). There is at least one addi-
tional ventral commissure in the thoracic ganglia of crayfish that has not been described in
the abdominal ganglia, and the thoracic ventral commissures more closely resemble those of
insects. In addition, there is also a pair of ascending and diverging tracts found only in the tho-
racic ganglia that is likely to be homologous to “T-tracts” seen in insects (Tyrer and Gregory
1982, Elson 1996).
Abdominal Ganglia
The structural organization of the abdominal ganglia of crustaceans has been most extensively
studied in the crayfish (Mulloney et al. 2003). Five of the six serially homologous abdominal
ganglia (A1–A5) of crayfish are unfused and innervate muscles of the abdomen and the pleo-
pods. While these ganglia are each derived from single embryonic neuromeres, the terminal
abdominal ganglion (A6) is the fusion product of three embryonic ganglion anlagen: the sixth
and seventh abdominal ganglia and a partial eighth ganglion (Whitington 2004).
The abdominal ganglia A1–A5 contain a similar number of neuronal somata (600–700),
and each has three paired segmental nerves (N1–N3) (Kondoh and Hisada, 1986). N1 is a mixed
sensory-motor nerve innervating the pleopods; N2 is a sensory-motor nerve innervating the
abdominal extensor muscles, muscle receptor organs, and the cuticular surface; and N3, the
most caudally located nerve, is a pure motor nerve innervating the abdominal flexor muscles.
The terminal abdominal ganglion contains the same number of neuronal somata as the more
anterior abdominal ganglia but has six paired peripheral nerves (R1–R6) innervating the tail
fan and an unpaired nerve (R7) innervating the hindgut (Kondoh and Hisada 1986). Within
each abdominal ganglion, 40–50% of the neuronal somata belong to local interneurons, 30–40%
are motor neurons, and 20–30% are projection interneurons (Reichert et al. 1982, Kondoh and
Hisada 1986).
The core organization of the anterior abdominal ganglia of crayfish is shown in Fig. 16.7C.
All neuronal somata in these ganglia are located ventrally. Each ganglion contains 5 neuropils
(anterior midline neuropil, horseshoe neuropil, LN, posterior midline neuropil, tract neuropil),
12 axon tracts, and 8 commissures (Mulloney et al. 2003). The horseshoe neuropil integrates
primary sensory information entering the ganglion via N1 and N2, and the paired LNs contain
neural circuits controlling rhythmic movements of the pleopods (see below). Motor neurons
receive synaptic input in the tract neuropil. Nothing is known about the function of the anterior
and posterior midline neuropils.
The core of the terminal abdominal ganglion exhibits an organization similar to that of the
more anterior abdominal ganglia. Some modifications have been noted, however, which arise
primarily through the previously mentioned ganglionic fusion and can also be seen in the fused
ganglia of insects (Tyrer and Gregory 1982, Kondoh and Hisada 1986). These modifications
include the presence of an additional midline neuropil at the anterior part of neuromere A7 and
a large group of neuronal somata associated with R7 (Kondoh and Hisada 1986).
INDIVIDUAL NEURONS AND NEURAL CIRCUITS OF THE VENTRAL NERVE CORD
Several hundred neurons have been individually identified in the crustacean CNS. Some of the
largest and most accessible of these neurons lie in the ventral nerve cord and control stereotyped
and discrete motor patterns. For a number of these motor patterns, the organization of the sensory
input pathways, integrating interneurons, and activated motor neurons, has been fully character-
ized. An overview of the neuroanatomical features of three of these neural circuits is presented
here.
Lateral Giant Escape Circuit
When exposed to predatory attacks, crayfish respond with rapid and powerful escape move-
ments (Fig. 16.8) (Herberholz et al. 2004b). If an attack is directed to the rear of the animal,
escape responses are mediated by pairs of bilateral command neurons, the lateral giant interneu-
rons (LGs) (Wine and Krasne 1982, Edwards et al. 1999). A single action potential produced by
the LGs is sufficient to initiate an escape tail-flip that pitches the animal upward and forward
away from the threatening stimulus. This stereotyped behavior can be elicited by attacks from
natural predators or electrical stimulation of sensory input pathways (Wine and Krasne 1972,
Herberholz et al. 2004b).
The LGs have large somata and extensive dendrites in each of the abdominal ganglia. Their
axons are the largest found in the ventral nerve cord (~150 μm diameter in adults), and are organ-
ized in a ladderlike network in which sequential pairs of LGs are coupled both longitudinally
and across the midline. Nonrectifying coupling allows these cells to act like a single neuron. The
LGs receive direct electrical inputs from approximately 1000 mechanosensory neurons inner-
vating tactile setae on the abdomen, as well as additional electrical inputs from interneurons that
are also activated by mechanosensory neurons (Krasne 1969, Zucker 1972). Mechanosensory
neurons contact these latter interneurons via chemical synapses but are also electrically cou-
pled to each other, thus amplifying sensory inputs to the LGs (Fig. 16.8A) (Herberholz et al.
2002, Antonsen et al. 2005). The LGs travel the length of the nervous system and make power-
ful electrical output connections to pairs of giant motor neurons (MoGs) in each of the first
three abdominal ganglia. The MoGs have the largest somata in the abdominal ganglia (>150 μm
diameter in adults). The axons of the MoGs project through N3 and innervate fast flexor mus-
cles that produce abdominal bending around the thoracic-abdominal joint (Fig. 16.8B) (Roberts
et al. 1982). This causes the “jackknife” motion characteristic of LG mediated tail-flips. The
LGs are also electrically coupled to another pair of giant neurons in each abdominal ganglion,
the segmental giants (SGs). The SGs make electrical synapses onto fast flexor motor neurons
that activate the flexor musculature. The SGs appear to have evolved from limb motor neurons
that lost their motor function over evolutionary time as the escape response changed from being
powered by the pleopods to being controlled by abdominal flexion (Heitler and Darrig 1986,
Faulkes 2008).
The effectiveness of the LG system for escape is based on its structural organization. Large,
fast-propagating axons and electrical transmission between most circuit components under-
lie this effective escape behavior. Although the LG escape circuit has been most intensively
studied in crayfish and clawed lobsters, components of this circuit are also present in prawns,
caridean shrimp, and the Stenopodidea; the LGs in these latter animals are myelinated, and all
caridean shrimp have fused MoG axons. On the other hand, the LGs seem to have been lost in
spiny lobsters, ghost shrimp, and crabs. In these animals, neural components controlling other
escape behaviors, for example, nongiant or medial giant circuits, are sometimes still present
(Faulkes 2008).
50 μm
50 μm
N1 N2
B Fast flexor
muscles
Motor giant
motor neuron
Lateral giant
interneuron
Sensory
interneuron
Tail afferent
Fig. 16.8.
Neuroanatomy of the crayfish lateral giant interneuron (LG) escape circuit. (A) Sensory neurons are elec-
trically coupled to each other and to the LG. One sensory neuron of the crayfish Procambarus clarkii was
injected with a green fluorescent dye (light gray), and the LG, with a red dye (dark gray). Confocal micro-
graphs of the terminal abdominal ganglion are shown. Dye injected into one sensory neuron (solid arrow)
spread into five other sensory neurons (left). The contact point between the injected neuron and the LG
occurs at the tip of an LG dendrite (open arrow). In the right panel, the solid arrow indicates the injected
sensory neuron, and solid arrowheads indicate the coupled sensory neurons. The coupling site with the LG
(open arrow) is proximal to the coupling site between the sensory neurons (open arrowhead). N1, N2, sen-
sory nerves 1, 2 (modified from Herberholz et al. 2002, with permission from the Society for Neuroscience;
see their fig. 3 for color images). (B) Schematic diagram of the LG escape circuit in the abdominal gan-
glia. Tail afferents provide input to sensory interneurons via chemical synapses. Interneurons activate LG
via electrical synapses. An action potential in LG activates the motor giant motor neurons that project
through the third ganglionic nerve and innervate the flexor muscles (modified from Wine and Krasne
1982, with permission from Sinauer Associates).
Swimmeret (Pleopod) Beating
Swimmerets (“swimming legs,” or pleopods) are paired abdominal limbs used for swimming,
burrowing, egg aeration, and other behaviors. The swimmerets of the first abdominal seg-
ment of many decapods are sexually dimorphic structures used in reproduction, while those
of the last abdominal segment have been replaced by uropods, the paired outer appendages
of the tail fan.
Swimmerets are activated sequentially from posterior to anterior, producing a metachronal
wave (Davis 1969). Rhythmic movements of each swimmeret are controlled by pattern-generat-
ing circuits located in each ganglion, whose activity is coordinated by projection interneurons
(Paul and Mulloney 1986, Smarandache et al. 2009). Each swimmeret contains power-stroke
and return-stroke muscles innervated by approximately 70 motor neurons belonging to four
subtypes: power-stroke and return-stroke excitors, and power-stroke and return-stroke inhibi-
tors (Mulloney and Hall 2003). The somata of most power-stroke motor neurons are located
posterior to the base of N1, whereas those of most return-stroke motor neurons are located ante-
rior to the base of N1 (Fig. 16.9A,B) (Mulloney and Hall 2000). The somata of all but two of
these motor neurons are located ipsilateral to the swimmeret they innervate; one has a midline
soma, and one has a contralateral soma. The axons of all swimmeret motor neurons originate
in the LN, where the neurons receive their sensory inputs. Some motor neurons have branches
that project to the contralateral LN and may be involved in coordinating the movements of the
left and right swimmeret in each segment. Thus, the idea of a modular swimmeret system where
each swimmeret is controlled by its own pattern-generating circuit is supported by this neuro-
anatomical analysis.
The distribution of the swimmeret motor neurons in the abdominal ganglia (A2–A5) is simi-
lar to that of the motor neurons responsible for movement of the uropods and walking legs. The
uropods have their own pool of motor neurons restricted to the ipsilateral side of the terminal
abdominal ganglion that innervate the ipsilateral LN (Kondoh and Hisada 1986). On the other
hand, the distribution of the swimmeret motor neurons is markedly different from the more dis-
persed pattern found for motor neurons innervating the abdominal musculature. Here, flexor
and extensor motor neurons have both ipsi- and contralateral somata and a small number of
somata located in the next posterior ganglion (Fig. 16.9C) (Mulloney and Hall 2003). In the
thoracic ganglia, however, each walking leg has its own discrete set of motor neurons restricted
to the ipsilateral hemiganglion. Leg motor neurons, similar in number to the swimmeret motor
neurons, possess somata located in discrete clusters near N1 (Faulkes and Paul 1997). Thus,
the structural organization underlying the motor innervation of the swimmerets seems to be
homologous to the walking leg system (see below).
Walking
Homologous to the central pattern generators that control the movement of each swimmeret,
the motion of each leg is controlled by a pattern-generating circuit located in the ipsilateral
thoracic hemiganglion (Sillar and Skorupski 1986). Although the muscles of the walking legs
and pleopods are innervated by roughly the same number of motor neurons (Mulloney et al.
2003), walking legs are appendages with multiple segments and joints that provide different
ranges of motion, and the coordination of these joints is inevitably more complex than that of
the swimmerets.
Each walking leg contains groups of proximal and distal muscles that operate on the vari-
ous leg joints (Cattaert and Le Ray 2001). The axons of motor neurons and sensory neurons
innervating different parts of the leg are separated into individual branches of N1 (Fig. 16.10A)
A B
N1a
N1
N1p
N2 200 μm
N3
C
Swimmerets Extensors Flexors
N1
N2
N3
Fig. 16.9.
Neuroanatomy of swimmeret beating. (A) Schematic of a posterior abdominal ganglion showing
the three ganglionic nerves. The first nerve (N1) innervates a swimmeret and bifurcates into an ante-
rior (N1a) and posterior (N1p) branch. (B) Cobalt backfills of the left anterior (left) and left posterior
(right) branch of the first nerve in the fourth and fifth abdominal ganglion, respectively, of the crayfish
Pacifastacus leniusculus. Ventral view of the ganglion shows the segregation of somata whose axons run in
different branches. (C) Positions of somata of three different types of motor neurons that occur in each
abdominal ganglion. Most swimmeret motor neurons have somata near the base of the first nerve (N1);
one has a midline soma, and one has a contralateral soma. Many f lexor and extensor motor neurons have
somata contralateral to the nerves that contain their axons (arrowheads); one extensor motor neuron and
four f lexor motor neurons have somata in the next posterior ganglion (modified from Mulloney and Hall
2000, with permission from John Wiley and Sons).
(Chrachri and Clarac 1989, Elson 1996). Proximal leg muscles are innervated by “pools” of motor
neurons, whereas distal leg muscles receive innervation from only a small number of motor neu-
rons. This difference may reflect a decrease in the complexity of the muscles from proximal to
distal (Hill and Cattaert 2008). While 17 distal motor neurons innervate each leg in most deca-
pods, the number of proximal leg motor neurons (51–90) varies both across and within species
(Fig. 16.10B) (Faulkes and Paul 1997, Hill and Cattaert 2008).
Sensory-motor integration in the walking system has been studied in detail in decapod crus-
taceans, and structural and functional similarities to other species ranging from insects to mam-
mals have been highlighted (Bschges and El Manira 1998, Clarac et al. 2000). Each leg contains a
variety of proprioceptors and exteroceptors, including cuticular stress detectors, muscle recep-
tor organs, and chordotonal organs; the sensory structures associated with the swimmerets,
such as tactile setae and nonspiking stretch receptors, appear to be more limited (Heitler 1986,
Macmillan and Deller 1989).
anterior
TG3 CBCO levator
promotor
anterior
distal root
TG4 posterior distal root

posterior
levator
remoter
TG5 depressor
B C
Opener O C Closer
Stretcher S B Bender
Extensor E F Flexor
aF
Accessory
Flexor
Reductor Rd
Distal
Proximal
L D d
Levator Depressor
P R
d 100 μm
Promoter Remoter
Cl
Fig. 16.10.
Neuroanatomy of walking. (A) Branches of the first thoracic nerve that control different leg joints in cray-
fish. Motor neurons in the anterior and posterior distal roots project to parts of the leg distal to the coxa. All
other branches are associated with movement of the proximal leg segments. CBCO, coxo-basipodite chor-
dotonal organ; TG3–5, thoracic ganglia 3–5 (modified from Chrachri and Clarac 1989, with permission from
the Journal of Neurophysiology). (B) Innervation pattern of the proximal and distal leg muscles. Each distal
leg muscle is innervated by one to four motor neurons, whereas each proximal muscle is innervated by a pool
of 7–20 motor neurons (circles) (modified from Faulkes and Paul 1997, with permission from S. Karger AG,
Basel). (C) Anatomical characterization of a single depressor motor neuron in the fifth thoracic ganglion of
the crayfish Procambarus clarkii. The neuron was injected with dye and imaged with confocal microscopy.
The neuron is shown from three different viewpoints. The gray area indicates neuropil regions in which this
motor neuron receives monosynaptic sensory input from the coxo-basipodite chordotonal organ. d, dorsal
(from Hill and Cattaert 2008, with permission from the Journal of Experimental Biology).
A number of the sensory-motor circuits of the walking legs have been thoroughly
described, including a neural circuit detecting leg position and movement (Clarac et al. 2000).
The coxo-basipodite leg joint is responsible for upward and downward movements of the leg
during walking. The coxo-basipodite chordotonal organ (CBCO) is composed of an inner-
vated elastic strand crossing this joint. Twenty identified CBCO sensory neurons respond
when the strand is stretched during downward leg movements, and a further 20 respond when
the strand is released during upward leg movements. The two populations of sensory neu-
rons project to the thoracic ganglia and connect to antagonistic sets of depressor and leva-
tor motor neurons (El Manira et al. 1991). Recently, all 12 excitatory motor neurons in the leg
depressor nerve have been anatomically and physiologically described (Fig. 16.10C) (Hill and
Cattaert 2008).
STRUCTURE OF THE NEUROENDOCRINE SYSTEM
Neurosecretory cells form an important part of the endocrine system, as the majority of crusta-
cean hormones are of neural origin (Fingerman 1987). Relatively little is known about the neuro-
secretory systems of nonmalacostracans, and although presumptive neurosecretory cells have
been identified in a number of species, these have not been examined in detail. In contrast, sev-
eral neuroendocrine organs have been described in malacostracans, including the X-organ-sinus
gland complex, pericardial organ, postcommissural organ, and neurohemal release sites in the
ventral nerve cord and peripheral nerves (Cooke and Sullivan 1982).
X-Organ-Sinus Gland Complex
The X-organ-sinus gland complex is the major neuroendocrine organ of malacostracans and
regulates a variety of physiological processes in these animals, including the molt cycle, energy
metabolism, osmoregulation, and vitellogenesis (Cooke and Sullivan 1982, Fingerman 1987).
The sinus gland is a neurohemal organ located adjacent to the optic neuropils innervated pri-
marily by a group of neurosecretory cells whose somata form a cluster, the X-organ, situated
near the medulla terminalis (Fig. 16.11A). The sinus gland is also innervated by neurons origi-
nating from the optic ganglia and the brain, though it remains unclear whether these cells are
neurosecretory. The axon terminals of neurons innervating the sinus gland form clusters sepa-
rated by glial cells and contain a variety of morphologically distinct types of neurosecretory
granules and vesicles (Fig. 16.11B).
Pericardial Organ
The paired pericardial organs are neurohemal structures located in the venous cavity sur-
rounding the heart that release a variety of cardioacceleratory peptides and hormones into the
hemolymph (Fig. 16.11C) (Cooke and Sullivan 1982). Although several of the hormones present
in the pericardial organ also occur in the sinus gland, evidence suggests that distinct isoforms
with differing functions are present in the two organs (Hsu et al. 2006). The specific functions
of the isoforms present in the pericardial organ are currently being elucidated. The pericardial
organ is innervated by extrinsic neurosecretory neurons projecting from the thoracic ganglia,
thoracic segmental nerves, and the commissural ganglion. The terminals of these neurons form
an elaborate cortical layer within the pericardial organ (Fig. 16.11D). The pericardial organ also
contains a number of intrinsic neurosecretory cells.
Postcommissural Organ
The postcommissural organ is a paired neurohemal organ containing chromoactive hormones

that is located lateral to the esophagus and consists of a network of fine dendritic branches
adjoining a dorsoventral venous channel (Fig. 16.11C) (Maynard 1961, Cooke and Sullivan 1982).
A sinus gland C D hemolymph

space
PT brain
MT MI ME LG
CG
X-organ
PCO
B hemolymph
sinus
TGM
PO
E F G
Fig. 16.11.
Structure of the neuroendocrine system. (A) Schematic diagram illustrating the anatomy of the
decapod X-organ-sinus gland complex. For abbreviations, see Fig. 16.4 caption (modified from Serrano
et al. 2004, with permission from the Journal of Histochemistry and Cytochemistry). (B) Electron micro-
graph of the sinus gland of the crab Cancer productus . White asterisks indicate nerve terminals contain-
ing membrane bound dense core vesicles; black asterisks show terminals containing only electron-lucent
vesicles. Abbreviations: ep, epineurium; g, glial cells; m, mitochondria (from Fu et al. 2005, with
permission from John Wiley and Sons). (C) Schematic diagram of the nervous system of a brachyuran
crab showing the relative locations of the pericardial organ (PC) and postcommissural organ (PCO).
CG, commissural ganglion; TGM, thoracic ganglionic mass (modified from Cooke and Sullivan 1982).
(D) Electron micrograph of the pericardial organ of C. productus . The arrowhead indicates a vesicle
docked to the plasma membrane. Asterisks indicate electron-lucent vesicles. Abbreviations: DCV,
dense core vesicle; ELV, electron-lucent vesicle; ep, epineurium (modified from Fu et al. 2005, with per-
mission from John Wiley and Sons). (E) Substance P-like immunolabeling of the anterior commissural
organ (boxed) of C. productus . Labeled neuropilar processes in the commissural ganglion are indicated
by the star (modified from Messinger et al. 2005, with permission from the Company of Biologists,
Ltd.). (F) Mandibular organ-inhibiting hormone-like immunolabeling of the anterior cardiac plexus
(ACP) of C. productus . This neuroendocrine release center is located in the anterior cardiac nerve (acn)
of the stomatogastric nervous system (stn) (from Hsu et al. 2006, with permission from the Company of
Biologists, Ltd.). (G) Neurosecretory cell (arrow) in the second nerve of the third thoracic ganglion
of the lobster Homarus americanus immunolabeled for crustacean hyperglycemic hormone (modified
from Chang et al. 1999, with permission from John Wiley and Sons). Scale bars: B, 2 μm; D and E, 200
μm; F, 75 μm; G, 100 μm.
The axons of the neurosecretory cells innervating the postcommissural organ exit the CNS via
the paired postcommissural nerves of the tritocerebral commissure. The location of the somata
of these cells, however, has not been established definitively.
Neurohemal Release Sites
In addition to the main neuroendocrine organs, several neurohemal structures have been
identified within the central ganglia and peripheral nerves of decapods that are thought to
modulate local neural circuits and musculature. The anterior commissural organ is a club- or
fork-shaped neurohemal structure present in the commissural ganglion that contains hemol-
ymph lacunae apposed by the terminals of neurons ascending from the thoracic ganglia (Fig.
16.11E) (Messinger et al. 2005). Neuroendocrine release sites also occur within the intercon-
necting and peripheral nerves of the STNS (Fig. 16.11F) (Christie et al. 2004), the sheath of the
ventral nerve cord (Kobierski et al. 1987), and the second nerve roots of the thoracic ganglia
(Fig. 16.11G) (Chang et al. 1999).
DEVELOPMENT OF THE NERVOUS SYSTEM
Central Nervous System
The CNS of malacostracans forms during embryonic development through the mitotic activ-
ity of large precursor cells, known as neuroblasts, located in the ventral ectoderm (Fig. 16.12A)
(Ungerer and Scholtz 2008). Neuroblasts divide repeatedly and asymmetrically giving rise to
columns of ganglion mother cells towards the center of the embryo. Ganglion mother cells in
turn undergo a single symmetric division, giving rise to two ganglion cells that subsequently
differentiate into neurons. It remains unclear whether ganglion cells also differentiate into glial
cells. Neuroblasts in each segment are arranged in a regular pattern and give rise to specific
cell lineages (Harzsch 2003a, Ungerer and Scholtz 2008). Mitotic activity in the neuroblasts of
the developing ventral nerve cord ceases during late embryonic or early postembryonic devel-
opment. Large, mitotically active cells resembling neuroblasts have been reported in develop-
ing branchiopods (Ungerer and Scholtz 2008). However, it remains unclear whether they are
homologous to the neuroblasts of malacostracans. Corresponding studies of embryonic neuro-
nal proliferation in the remaining crustacean taxa have not yet been undertaken.
The sequence of cell divisions giving rise to neurons in the developing brain appears
to differ from that characteristic of the ventral nerve cord (Benton and Beltz 2002). Large
precursor cells in the embryonic deutocerebrum give rise to intermediate precursor cells
that undergo multiple cell divisions, giving rise to several neurons. Neurogenesis in discrete
regions of the decapod brain persists through hatching and continues throughout postem-
bryonic life (Fig. 16.12B,C) (Sandeman et al. 2011, Schmidt and Mellon 2011). Adult neuro-
genesis is characteristic of the central olfactory pathways of decapods and also occurs in the
visual pathway in some species. The identity of the precursor cells maintaining life-long neu-
ronal proliferation in the olfactory pathway remains unclear, with some studies suggesting
they are persistent neuroblasts (Schmidt 2007) and others suggesting they are adult-specific
precursors with glial characteristics (Sullivan et al. 2007b). These studies agree, however,
in recognizing the close association of identified clusters of glia-like cells, known originally
as the deutocerebral organs (Bazin 1970), with the restricted regions in which proliferative
activity occurs (Fig. 16.12D). The specific roles of these cells in adult neurogenesis are cur-
rently being investigated.
A B
MPZ
Optic ganglia and

protocerebrum
Olfactory
LPZ lobe
Deutocerebrum Accessory
lobe
Esophageal
Tritocerebrum connectives
Fig. 16.12.
Development of the central nervous system. (A) Bromodeoxyuridine labeling of proliferating cells in
the central nervous system of the crayfish Cherax destructor at 85% of embryonic development. Discrete
clusters of proliferating cells occur throughout the nervous system. Each cluster is composed of a single
neuroblast (N) and the smaller nuclei of its progeny (inset); (modified from Sullivan and Macmillan
2001, with permission from John Wiley and Sons). (B) Schematic diagram of the crayfish brain show-
ing the location of the lateral (LPZ) and medial (MPZ) proliferation zones of the olfactory pathway in
which mitotic activity is maintained throughout life (modified from Sullivan et al. 2007b, with per-
mission from Springer). (C) Bromodeoxyuridine labeling of proliferating cells in the lateral (LPZ) and
medial (MPZ) proliferation zones of the crayfish Procambarus clarkii (modified from Sullivan et al.
2007a, with permission from John Wiley and Sons). (D) The lateral (LPZ) and medial (MPZ) prolif-
eration zones of P. clarkii are contacted by the processes of a population of glia-like cells that exhibit
glutamine synthetase immunoreactivity. The somata of these cells form a cluster on the ventral surface
of the brain (boxed) (from Sullivan et al. 2007a, with permission from John Wiley and Sons). Scale bars:
A, 500 μm; A inset, 10 μm; C, 100 μm; D, 75 μm.
Maturation of the nervous system during embryonic development follows a rostrocau-

dal gradient (Fig. 16.13A) and begins with the formation of the brain anlage as a nerve ring
around the stomodeum (Harzsch 2003b). The axon tracts of the developing CNS and periph-
eral nerves are established by early differentiating pioneer neurons, many of which can be
identified across taxa (Whitington 1996, Ungerer and Scholtz 2008, Simanton et al. 2009).
Individual neuropils arise at separate and distinct stages of embryonic development. The
olfactory lobe and medulla terminalis of Homarus americanus, for example, form during the
initial stages of embryogenesis, whereas the anlagen of the accessory lobe and hemiellipsoid
Distal tip
Loss of annuli
Loss of aesthetascs
Death of ORNs
Senescence zone
Decrease in odor
sensitivity of ORNs
Aging of aesthetascs
Mature zone and ORNs
Maturation zone Functional maturation

of ORNs
Proliferation zone Differentiation of
aesthetascs and ORNs
wave
Lateral side
Mesial side
8.0 mm Addition of annuli
ORN clusters of emerged

Proximal aesthetascs
ORN clusters of developing,
non=emerged aesthetascs
Fig. 16.13.
Development of the central and sensory nervous systems. (A) F-actin labeling of the developing nervous
system of C. destructor at 50% of embryonic development (C50%). Note the rostrocaudal gradient in the
extent of development of the maxillary (M1 and M2) and thoracic (T1 and T2) neuromeres of the ven-
tral nerve cord. Abbreviations: DC, deutocerebrum; LBM, longitudinal body musculature; LPC, lateral
protocerebrum; MD, mandibular neuromere; MPC, median protocerebrum; PC, post-esophageal com-
missure; PT, protocerebral tract; TC, tritocerebrum; VAM, ventral anterior muscles. Scale bar, 50 μm
(modified from Vilpoux et al. 2006, with permission from Springer). (B) Schematic diagram summarizing
the turnover of olfactory receptor neurons (ORNs) and aesthetascs in the antenna I of the adult spiny lob-
ster Panulirus argus (modified from Derby et al. 2003, with permission from Elsevier).
body do not emerge until midembryonic development (Helluy et al. 1995, Sullivan and Beltz
2001a). Glomerular formation in the olfactory and accessory lobes also follow distinct tempo-
ral patterns (Helluy et al. 1996).
Visual System (Ommatidia and the Optic Neuropils)
Embryonic development of the visual system has been examined in detail in both the
Malacostraca and Branchiopoda. In malacostracans, stem cells residing in three proliferation
zones give rise synchronously to the ommatidia and the neurons of the lamina ganglionaris and
medulla externa (Harzsch and Hafner 2006). Similarly arranged proliferation zones also give
rise to the ommatidia and the two optic neuropils of branchiopods (Harzsch and Hafner 2006).
The third optic neuropil of malacostracans, the medulla interna, is of protocerebral origin and
arises from the anlage of the lateral protocerebrum (Harzsch 2002). The number of ommatidia
in the compound eyes of malacostracans increases through postembryonic development as the
animals grow (Keskinen et al. 2002). New neurons are also continually added to the optic gan-
glia of some adult decapods (Sullivan et al. 2007b).
Sensory Nervous System
Sensory neurons in arthropods are the progeny of ectodermal precursor cells (Bate 1978). While
these cells have been characterized in Drosophila (Lai and Orgogozo 2004), the identity of the
precursor cells giving rise to the sensory nervous systems of crustaceans remains unclear. In
decapods, postembryonic increases in the numbers of setae and associated sensory neurons
have been described on the telson, mouthparts, pereopods, antennae I, and statocysts (Finley
and Macmillan 2000). Developmental increases in innervation also occur in chordotonal
organs (Hartman and Cooper 1994). The lifelong addition of olfactory receptor neurons (and
aesthetascs) to the antennae I of adult decapods occurs in parallel with the loss of older neurons,
resulting in a continuous turnover and replenishment of these neurons (Fig. 16.13B) (Sandeman
and Sandeman 1996, Steullet et al. 2000). The generation of new olfactory receptor neurons
occurs at the proximal end of the antenna I within a restricted proliferation zone (Harrison
et al. 2001). The oldest olfactory receptor neurons and aesthetascs, located at the distal end of
the antenna I, are lost at each molt (Sandeman and Sandeman 1996, Steullet et al. 2000). The
birth, differentiation, and death of olfactory receptor neurons therefore occur in a spatiotempo-
ral wave along the length of the antenna.
COMPARATIVE ANATOMY OF THE CRUSTACEAN BRAIN
Comparative neuroanatomists have long recognized structural features of crustacean brains

that are shared by other animal taxa, particularly insects. The question of whether these shared
characters represent homologies or reflect convergent evolution due to functional constraints
(homoplasies) has been the subject of extensive study and debate. The glomerular organiza-
tion of the crustacean olfactory lobe is also characteristic of the primary olfactory neuropils
of a diverse range of both invertebrate and vertebrate species (Fig. 16.14A–C) (Strausfeld and
Hildebrand 1999). Several features of the cellular organization of the olfactory lobes of decapods
and remipedes (e.g., uniglomerular projections of olfactory receptor neurons) are also present
in the olfactory (antennal) lobes of insects (Schachtner et al. 2005, Harzsch 2006). Secondary
olfactory neuropils, comparable to the medulla terminalis and hemiellipsoid body, have been
identified in dicondylic insects (lateral horn) and in the most basal living insects, the Machilidae
(lateral protocerebrum) (Strausfeld and Reisenman 2009). There is little to suggest homology,
however, between the crustacean hemiellipsoid body and the mushroom bodies of insects
(Strausfeld 2009).
The optic neuropils of malacostracans and insects share a basic organization that differs
from that of the optic neuropils of nonmalacostracans (Fig. 16.14D). As in the Malacostraca,
insects possess three nested retinotopic neuropils linked by successive chiasmata and a fourth
neuropil connected by an uncrossed axon tract (Harzsch 2006, Strausfeld 2009). The organiza-
tion of the optic neuropils of nonmalacostracans (two retinotopic neuropils, no chiasmata) is
shared by scutigerid centipedes (Fig. 16.14E) (Sinakevitch et al. 2003, Strausfeld 2005). It has
been proposed that the more complex organization of the optic neuropils of malacostracans and
insects arose through ancestral duplications of cell lineages (Strausfeld 2005, 2009).
Protocerebral midline neuropils comparable to the central body of crustaceans are present
in all arthropods, with the exception of millipedes (Fig. 16.14E–H) (Loesel 2004, Homberg
2008). The central body of insects, like that of crustaceans, forms part of an interconnected
Scutigeromorpha
Branchiopoda
Phyllocarida
Decapoda
Protocerebrum
1st (lamina) Isopoda
2nd (outer
medulla) Archeognatha
inner medulla
protolobula
3rd (lobula/medulla Hymenoptera
externa)
4th (lobula plate/
Diptera
visual tectum)
Fig. 16.14.
Comparative anatomy of the crustacean and arthropod central nervous system. (A) Synapsin labe-
ling of the olfactory lobe (OL) of the shrimp Palaemonetes pugio (Crustacea) (from Sullivan and Beltz
2004, with permission from John Wiley and Sons). (B) Allatostatin and synapsin labeling of the olfac-
tory (antennal) lobe (OL) of the honeybee Apis mellifera (Insecta) (modified from Schachtner et al. 2005,
with permission from Elsevier). (C) Serotonin labeling of the olfactory lobe (Olf Lo) of the velvet worm
Euperipatoides rowelli (Onychophora) (modified from Strausfeld et al. 2006b, with permission from
Elsevier). (D) Proposed arthropod relationships with reference to optic neuropil organization. Myriapod,
crustacean (bold), and insect taxa are shown from top to bottom (modified from Sinakevitch et al. 2003,
with permission from John Wiley and Sons). (E–H) Midline brain neuropils (arrows) of the centipede
Scolopendra polymorpha (Myriapoda) (E), the crab Hemigrapsus oregonensis (Crustacea, Decapoda)
(F), the bristletail Machilis germanicus (Insecta, Archaeognatha, Machilidae) (G), and the cockroach
Periplaneta americana (Insecta, Pterygota) (H) (modified from Strausfeld et al. 2006a, with permission
from the Royal Society of London). The arrowhead in E indicates a perpendicular neuron extending
through the midline brain neuropil. Scale bars: A, 100 μm; B and E–H, 50 μm; C, 40 μm.
system of protocerebral neuropils known as the central complex (Harzsch 2006, Homberg 2008,
Strausfeld 2009). The central complex is thought to function as a higher control center for sen-
sory integration and motor behavior (Homberg 2008). While the neuroanatomy of the central
complex in most insects (Fig. 16.14H) is more intricate than in crustaceans (Fig. 16.14F), perhaps
reflecting the more elaborate behavioral repertoires of terrestrial species, the central complex of
basal insects (Fig. 16.14G; Machilidae) and decapods (Fig. 16.14F) exhibit extensive similarities
(Strausfeld 2009).
FUTURE DIRECTIONS
Further characterization of the cellular organization of the crustacean nervous system will
require the application of molecular biological techniques. Elucidation of the innervation
patterns of individual olfactory receptor neuron types, for example, will involve the cloning
and characterization of crustacean odorant receptor proteins. This characterization will also
enable detailed comparative studies of the olfactory pathways of crustacean taxa differing in the
number and/or size of their olfactory lobe glomeruli. The recent sequencing of the genome of
the branchiopod Daphnia pulex has led to the bioinformatic identification of 58 gustatory recep-
tor proteins (Pealva-Arana et al. 2009). Genes encoding olfactory receptor proteins comparable
to those of other invertebrates, however, have not been identified in D. pulex. Because our under-
standing of the crustacean nervous system is based largely on studies of decapods, sequencing of
the genome of a representative of this group will rapidly accelerate molecular biological analyses
of these animals by facilitating in silico identification of neuronal proteins. One candidate for
such studies is the marbled crayfish (Procambarus sp.), a recently discovered species that repro-
duces by parthenogenesis (Scholtz et al. 2003). Individuals of this species are highly fertile and
genetically uniform.
In addition, future research should target the anatomical and functional organization of
brain areas underlying behaviors such as aggression, communication, learning, and memory, all
of which have been studied extensively in crustaceans. Initial attempts have led to the develop-
ment and application of new noninvasive imaging techniques. Manganese-enhanced magnetic
resonance imaging (MEMRI), for example, has been used successfully to label brain areas of
live crayfish (Herberholz et al. 2004a, Brinkley et al. 2005). Manganese is a calcium analogue
and can enter active neurons through calcium channels. In addition, manganese ions (Mn 2+) are
paramagnetic, making them detectable in magnetic resonance images. Crayfish are well suited
for these studies because they can be injected with manganese outside the scanner while they
are freely behaving, and they can be imaged using strong magnetic fields. This results in brain
images of high spatial resolution. In the future, this technique may also aid in functional analy-
ses of brain activity. Since manganese is taken up by neurons that are activated in freely behav-
ing animals, MEMRI may provide a means to noninvasively identify patterns of neural activity
in crustacean brains. Because crustaceans have a long history as model systems for investigating
neural mechanisms of behavior, noninvasive imaging techniques are expected to play a central
role in the continued elucidation of these mechanisms.
REFERENCES
Abbott, J. 1970. Absence of a blood-brain barrier in a crustacean, Carcinus maenas L. Nature 225:291–293.
Abbott, N.J. 1971. The organization of the cerebral ganglion in the shore crab, Carcinus maenus. I.
Morphology. Zeitschrift f ü r Zellforschung und mikroskopische Anatomie 120:386 –400.
Alexandrowicz , J.S. 1954 . Innervation of an amphipod heart. Journal of the Marine Biological
Association of the UK 33:709 –719.
Anderson, D.T. 1994 . Barnacles: Structure, function, development, and evolution. Chapman and Hall,
London.
Ando, H., and K. Kuwasawa. 2004 . Neuronal and neurohormonal control of the heart in the stomatopod
crustacean, Squilla oratoria. Journal of Experimental Biology 207:4663–4677.
Ando, Y., O. Matsuzaki, and H. Yamagishi. 2001. Cardiac nervous system in the ostracod crustacean
Vargula hilgendorfii. Zoological Science 18:651–658.
Antonsen, B.L., J. Herberholz , and D.H. Edwards. 2005 . The retrograde spread of synaptic potentials and
recruitment of presynaptic inputs. Journal of Neuroscience 25:3086 –3094.
Atwood, H.L. 1982. Synapses and neurotransmitters. Pages 105–150 in H.L. Atwood and D.C. Sandeman,
editors. The biology of Crustacea, Vol. 3, Neurobiology: Structure and function. Academic Press,
New York.
Bate, C.M. 1978. Development of sensory systems in arthropods. Pages 1–53 in M. Jacobson, editor.
Handbook of sensory physiology. Springer, Berlin.
Bazin, F. 1970. Étude comparée de l’organe deutocérébral des macroures reptantia et des anomoures
(crustacés, décapodes). Archives de zoologie expérimentale et générale 111:245–264.
Beltz , B.S., K. Kordas, M.M. Lee, J.B. Long, J.L. Benton, and D.C. Sandeman. 2003. Ecological, evolu-
tionary, and functional correlates of sensilla number and glomerular density in the olfactory system
of decapod crustaceans. Journal of Comparative Neurology 455:260 –269.
Benton, J.L., and B.S. Beltz. 2002. Patterns of neurogenesis in the midbrain of embryonic lobsters differ
from proliferation in the insect and the crustacean ventral nerve cord. Journal of Neurobiology
53:57–67.
Blaustein, D.N., C.D. Derby, R.B. Simmons, and A.C. Beall. 1988. Structure of the brain and medulla ter-
minalis of the spiny lobster Panulirus argus and the crayfish Procambarus clarkii, with an emphasis
on olfactory centers. Journal of Crustacean Biology 8:493–519.
Brinkley, C.K., N.H. Kolodny, S.J. Kohler, D.C. Sandeman, and B.S. Beltz. 2005 . Magnetic resonance
imaging at 9.4 T as a tool for studying neural anatomy in non-vertebrates. Journal of Neuroscience
Methods 146:124–132.
Bullock , T.H., and G.A. Horridge 1965 . Structure and function in the nervous systems of invertebrates,
Vol. 2. Freeman, San Francisco.
Büschges, A., and A. El Manira . 1998. Sensory pathways and their modulation in the control of locomo-
tion. Current Opinion in Neurobiology 8:733–739.
Callaway, J.C., and A.E. Stuart. 1999. The distribution of histamine and serotonin in the barnacle’s nerv-
ous system. Microscopy Research and Technique 44:94–104.
Cate, H.S., and C.D. Derby. 2002. Ultrastructure and physiology of the hooded sensillum, a bimodal
chemo-mechanosensillum of lobsters. Journal of Comparative Neurology 442:293–307.
Cate, H.S., and D.B. Roye. 1997. Ultrastructure and physiology of the outer row statolith sensilla of the
blue crab Callinectes sapidus. Journal of Crustacean Biology 17:398 –411.
Cattaert, D., and D. Le Ray. 2001. Adaptive motor control in crayfish. Progress in Neurobiology
63:199 –240.
Chang , E.S., S.A. Chang , B.S. Beltz , and E.A. Kravitz. 1999. Crustacean hyperglycemic hormone in the
lobster nervous system: Localization and release from cells in the subesophageal ganglion. Journal
of Comparative Neurology 414:50 –56.
Chrachri, A., and F. Clarac. 1989. Synaptic connections between motor neurons and interneurons in
the fourth thoracic ganglion of the crayfish, Procambarus clarkii. Journal of Neurophysiology
62:1237–1250.
Christie, A.E., S.D. Cain, J.M. Edwards, T.A. Clason, E. Cherny, M. Lin, A.S. Manhas, K.L. Sellereit,
N.G. Cowan, K.A. Nold, H.P. Strassburg , and K. Graubard. 2004 . The anterior cardiac plexus: An
intrinsic neurosecretory site within the stomatogastric nervous system of the crab Cancer productus.
Clarac , F., D. Cattaert, and D. Le Ray. 2000. Central control components of a “simple” stretch reflex.
Trends in Neurosciences 23:1237–1250.
Cooke, I.M. 2002. Reliable, responsive pacemaking and pattern generation with minimal cell numbers:
The crustacean cardiac ganglion. Biological Bulletin 202:108 –136.
Cooke, I.M., and R.E. Sullivan 1982. Hormones and neurosecretion. Pages 206–278 in H.L. Atwood and
D.C. Sandeman, editors. The biology of Crustacea, Vol. 3, Neurobiology: Structure and function.
Academic Press, New York.
Davis, W.J. 1969. Neural control of swimmeret beating in the lobster. Journal of Experimental Biology
50:99 –117.
Derby, C.D., H.S. Cate, P. Steullet, and P.J.H. Harrison. 2003. Comparison of turnover in the olfac-
tory organ of early juvenile stage and adult Caribbean spiny lobsters. Arthropod Structure and
Derby, C.D., and P.W. Sorenson 2008. Neural processing, perception, and behavioral responses to natural
chemical stimuli by fish and crustaceans. Journal of Chemical Ecology 34:898 –914.
Edwards, D.H., W.J. Heitler, and F.B. Krasne. 1999. Fifty years of a command neuron: The neurobiology
of escape behavior in the crayfish. Trends in Neurosciences 22:153–161.
Elekes, K., E. Florey, and M.A. Cahill. 1988. Morphology and central synaptic connections of the efferent
neurons innervating the crayfish hindgut. Cell and Tissue Research 1988:369 –379.
El Manira, A., D. Cattaert, and F. Clarac. 1991. Monosynaptic connections mediate resistance reflex in
crayfish (Procambarus clarkii) walking legs. Journal of Comparative Physiology A 168:337–349.
Elofsson, R. 2006. The frontal eyes of crustaceans. Arthropod Structure and Development 35:275–291.
Elofsson, R., and E. Dahl. 1970. The optic neuropiles and chiasmata of Crustacea. Zeitschrift f ü r
Zellforschung 107:343–360.
Elofsson, R., and M. Hagberg. 1986. Evolutionary aspects on the construction of the first optic neuropil
(lamina) in Crustacea. Zoomorphology 106:174–178.
Elofsson, R., and R.R. Hessler. 2005. The tegumental sensory organ and nervous system of Derocheilocaris
typica (Crustacea: Mystacocarida). Arthropod Structure and Development 34:139 –152.
Elson, R.C. 1996. Neuroanatomy of a crayfish thoracic ganglion: Sensory and motor roots of the walking-
leg nerves and possible homologies with insects. Journal of Comparative Neurology 365:1–17.
Fanenbruck , M., and S. Harzsch. 2005 . A brain atlas of Godzilliognomus frondosus Yager, 1989 (Remipedia,
Godzilliidae) and comparison with the brain of Speleonectes tulumensis Yager 1987 (Remipedia,
Speleonectidae): Implications for arthropod relationships. Arthropod Structure and Development
34:343–378.
Faulkes, Z. 2008. Turning loss into opportunity: The key deletion of an escape circuit in decapod crusta-
ceans. Brain, Behavior and Evolution 72:251–261.
Faulkes, Z., and D.H. Paul. 1997. A map of distal leg motor neurons in the thoracic ganglia of four decapod
crustacean species. Brain, Behavior and Evolution 49:162–178.
Fingerman, M. 1987. The endocrine mechanisms of crustaceans. Journal of Crustacean Biology 7:1–24.
Finley, L., and D.L. Macmillan. 2000. The structure and growth of the statocyst in the Australian cray-
fish Cherax destructor. Biological Bulletin 199:251–256.
Florey, E., and E. Florey. 1955 . Microanatomy of the abdominal stretch receptors of the crayfish (Astacus
fluviatilis L.). Journal of General Physiology 39:69 –85.
Fraser, P.J., and M. Takahata 2002. Statocysts and statocyst control of motor pathways in crayfish
and crabs. Pages 89–108 in K. Wiese, editor. Crustacean experimental systems in neurobiology.
Springer, Berlin.
Fu , Q., K.K. Kutz , J.J. Schmidt, Y.W.A. Hsu, D.I. Messinger, S.D. Cain, H.O. de la Iglesia, A.E. Christie,
and L. Li. 2005 . Hormone complement of the Cancer productus sinus gland and pericardial
organ: An anatomical and mass spectrometric investigation. Journal of Comparative Neurology
493:607–626.
Govind, C.K. 1992. Nervous system. Pages 395–438 in F.W. Harrison and A.G. Humes, editors.
Microscopic anatomy of invertebrates, Vol. 10, Decapod Crustacea. Academic Press, New York.
Hallberg , E., K.U.I. Johansson, and R. Wallén. 1997. Olfactory sensilla in crustaceans: Morphology,
Hanström, B. 1947. The brain, the sense organs, and the incretory organs of the head in the Crustacea
Malacostraca. Kungliga Fysiografiska Sä llskapets Handlingar 58:1–44.
Harrison, P.J., H.S. Cate, E.S. Swanson, and C.D. Derby. 2001. Postembryonic proliferation in the spiny
lobster antennular epithelium: Rate of genesis of olfactory receptor neurons is dependent on molt
stage. Journal of Neurobiology 47:51–66.
Harris-Warrick , R.M., E. Marder, A.I. Selverston, and M. Moulins 1992. Dynamic biological networks:
The stomatogastric nervous system. MIT Press, Cambridge, MA.
Hartman, H.B., and R.L. Cooper. 1994 . Regeneration and molting effects on a proprioceptor organ in the
Dungeness crab, Cancer magister. Journal of Neurobiology 25:461–471.
Harzsch, S. 2002. The phylogenetic significance of crustacean optic neuropils and chiasmata: A re-
examination. Journal of Comparative Neurology 453: 10 –21.
Harzsch, S. 2003a . Neurogenesis in the ventral nerve cord in malacostracan crustaceans: A common plan
for neuronal development in Crustacea, Hexapoda and other Arthropoda? Arthropod Structure
Harzsch, S. 2003b. Ontogeny of the ventral nerve cord in malacostracan crustaceans: A common plan for
neuronal development in Crustacea, Hexapoda and other Arthropoda? Arthropod Structure and
Harzsch, S. 2006. Neurophylogeny: Architecture of the nervous system and a fresh view on arthropod
phylogeny. Integrative and Comparative Biology 46:162–194.
Harzsch, S., and G. Hafner. 2006. Evolution of eye development in arthropods: Phylogenetic aspects.
Arthropod Structure and Development 35:319 –340.
Heiman, P. 1984 . Fine structure and molting of aesthetasc sense organs on the antennules of the isopod,
Asellus aquaticus (Crustacea). Cell and Tissue Research 235:117–128.
Heitler, W.J. 1986. Aspects of sensory integration in the crayfish swimmeret system. Journal of
Heitler, W.J., and S. Darrig. 1986. The segmental giant neurone of the signal crayfish, Pacifasticus lenius-
culus, and its interactions with abdominal fast flexor and swimmeret motor neurones. Journal of
Helluy, S., J.L. Benton, K.A. Langworthy, M.L. Ruchoeft, and B.S. Beltz. 1996. Glomerular organization
in developing olfactory and accessory lobes of American lobsters: Stabilization of numbers and
increase in size after metamorphosis. Journal of Neurobiology 29:459 –472.
Helluy, S., M.L. Ruchoeft, and B.S. Beltz. 1995 . Development of the olfactory and accessory lobes in the
American lobster: An allometric analysis and its implications for the deutocerebral structure of
decapods Journal of Comparative Neurology 357:433–445.
Herberholz , J., B.L. Antonsen, and D.H. Edwards. 2002. A lateral excitatory network in the escape circuit
of crayfish. Journal of Neuroscience 22:9078 –9085.
Herberholz , J., C.J. Mims, X. Zhang, X. Hu, and D.H. Edwards. 2004a . Anatomy of a live invertebrate
revealed by manganese-enhanced magnetic resonance imaging. Journal of Experimental Biology
207:4543–4550.
Herberholz , J., M.M. Sen, and D.H. Edwards. 2004b. Escape behavior and escape circuit activation in
juvenile crayfish during prey-predator interactions. Journal of Experimental Biology 207:1855–1863.
Hill, A.A.V., and D. Cattaert. 2008. Recruitment in a heterogeneous population of motor neurons that
innervates the depressor muscle of the crayfish walking leg muscle. Journal of Experimental
Biology 211:613–629.
Homberg , U. 2008. Evolution of the central complex in the arthropod brain with respect to the visual
system. Arthropod Structure and Development 37:347–362.
Hsu, Y.W.A., D.I. Messinger, J.S. Chung, S.G. Webster, H.O. de la Iglesia, and A.E. Christie. 2006.
Members of the crustacean hyperglycemic hormone (CHH) peptide family are differentially
distributed both between and within the neuroendocrine organs of Cancer crabs: Implications for
differential release and pleiotropic function. Journal of Experimental Biology 209:3241–3256.
Johansson, K.U.I., and E. Hallberg. 1992. The organization of the olfactory lobes in Euphausiacea and
Mysidacea (Crustacea, Malacostraca). Zoomorphology 112:81–90.
Keskinen, E., Y. Takaku, V.B. Meyer-Rochow, and T. Hariyama. 2002. Postembryonic eye growth in the
seashore isopod Ligia exotica (Crustacea, Isopoda). Biological Bulletin 202:223–231.
Kirsch, R., and S. Richter. 2007. The nervous system of Leptodora kindtii (Branchiopoda, Cladocera) sur-
veyed with Confocal Scanning Microscopy (CLSM), including general remarks on the branchio-
pod neuromorphological ground pattern. Arthropod Structure and Development 36:143–156.
Kobierski, L.A., B.S. Beltz , B.A. Trimmer, and E.A. Kravitz. 1987. FMRFamidelike peptides of Homarus
americanus: Distribution, immunocytochemical mapping, and ultrastructural localization in termi-
nal varicosities. Journal of Comparative Neurology 266:1–15.
Kondoh, Y., and M. Hisada. 1986. Neuroanatomy of the terminal (sixth abdominal) ganglion of the cray-
fish, Procambarus clarkii (Girard). Cell and Tissue Research 243:273–288.
Krasne, F.B. 1969. Excitation and habituation of the crayfish escape reflex: The depolarizing response in
lateral giant fibres of the isolated abdomen. Journal of Experimental Biology 50:29 –46.
Lai, E.C., and V. Orgogozo. 2004 . A hidden program in Drosophila peripheral neurogenesis revealed:
Fundamental principles underlying sensory organ diversity. Developmental Biology 269:1–17.
Lane, N.J., and N.J. Abbott. 1975 . The organization of the nervous system in the crayfish Procambarus
clarkii, with emphasis on the blood-brain interface. Cell and Tissue Research 156:173–187.
Laverack , M.S. 1988. The numbers of neurons in decapod Crustacea. Journal of Crustacean Biology
8:1–11.
Loesel, R. 2004 . Comparative morphology of central neuropils in the brain of arthropods and its evolu-
tionary and functional implications. Acta Biologica Hungarica 55:39 –51.
Macmillan, D.L., and S.R.T. Deller. 1989. Sensory systems in the swimmerets of the crayfish Cherax
destructor and their effectiveness in entraining the swimmeret rhythm. Journal of Experimental
Biology 144:279 –301.
Marshall, J., T.W. Cronin, and S. Kleinlogel. 2007. Stomatopod eye structure and function: A review.
Arthropod Structure and Development 36:42 0–448.
Martin, J.W., E.W. Vetter, and C.E. Cash-Clark. 1996. Description, external morphology, and natural
history observations of Nebalia hessleri, new species (Phyllocarida: Leptostraca), from Southern
California, with a key to the extant families and genera of the Leptostraca. Journal of Crustacean
Biology 16:347–372.
Maynard, D.M. 1961. Thoracic neurosecretory structures in Brachyura. I. Gross anatomy. Biological
Bulletin 121:316 –327.
Messinger, D.I., K.K. Kutz , T. Le, D.R. Verley, Y.W.A. Hsu, C.T. Ngo, S.D. Cain, J.T. Birmingham, L. Li,
and A.E. Christie. 2005 . Identification and characterization of a tachykinin-containing neuroen-
docrine organ in the commissural ganglion of the crab Cancer productus. Journal of Comparative
Neurology 208:3303–3319.
Meyer-Rochow, V.B. 2001. The crustacean eye: Dark/light adaptation, polarization sensitivity, flicker
fusion frequency, and photoreceptor damage. Zoological Science 18:1175–1197.
Mulloney, B., and W.M. Hall. 2000. Functional organization of crayfish abdominal ganglia. III.
Swimmeret motor neurons. Journal of Comparative Neurology 419:233–243.
Mulloney, B., and W.M. Hall. 2003. Local commissural interneurons integrate information from
intersegmental coordinating interneurons. Journal of Comparative Neurology 466:366 –376.
Mulloney, B., N. Tschuluun, and W.M. Hall. 2003. Architectonics of crayfish ganglia. Microscopy
Research and Technique 60:253–265.
Nä ssel, D.R., R. Elofsson, and R. Odselius. 1978. Neuronal connectivity patterns in the compound
eyes of Artemia salina and Daphnia magna (Crustacea: Branchiopoda). Cell and Tissue Research
190:435–437.
Nilsson, D.E., R. Odselius, and R. Elofsson. 1983. The compound eye of Leptodora kindtii (Cladocera). An
adaptation to planktonic life. Cell and Tissue Research 230:401–410.
Oakley, T.H. 2003. On homology of arthropod compound eyes. Integrative and Comparative Biology
43:522–530.
Overstreet, R.M., I. Dyková, and W.E. Hawkins 1992. Branchiura. Pages 385–413 in F.W. Harrison and
A.G. Humes, editors. Microscopic anatomy of invertebrates, Vol. 9, Crustacea. Wiley-Liss, New
York.
Paul, D.H., and B. Mulloney. 1986. Intersegmental coordination of swimmeret rhythms in isolated nerve
cords of crayfish. Journal of Comparative Physiology A 158:215–224.
Peñalva-Arana, D.C., M. Lynch, and H.M. Robertson. 2009. The chemoreceptor genes of the waterflea
Daphnia pulex: Many Grs but no Ors. BMC Evolutionary Biology 9:79.
Pflüger, H.J., P. Bräunig , and R. Hustert. 1988. The organization of mechanosensory neuropiles in locust
thoracic ganglia. Philosophical Transactions of the Royal Society of London Series B 321:1–26.
Reichert, H., M.R. Plummer, G. Hagiwara, R.L. Roth, and J.J. Wine. 1982. Local interneurons in the
terminal abdominal ganglion of the crayfish. Journal of Comparative Physiology 149:145–162.
Richter, S. 2002. Evolution of optical design in the Malacostraca (Crustacea). Pages 512–524 in K. Wiese,
editor. The crustacean nervous system. Springer, Berlin.
Roberts, A., F.B. Krasne, G. Hagiwara, J.J. Wine, and A.P. Kramer. 1982. Segmental giant: Evidence for
a driver neuron interposed between command and motor neurons in the crayfish escape system.
Journal of Neurophysiology 47:761–781.
Sandeman, D.C. 1982. Organization of the central nervous system. Pages 1–61 in H.L. Atwood and
D.C. Sandeman, editors. The biology of crustacea, Vol. 3, Neurobiology: Structure and function.
Academic Press, New York.
Sandeman, D.C., F. Bazin, and B.S. Beltz. 2011. Adult neurogenesis: Examples from the decapod crusta-
ceans and comparisons with mammals. Arthropod Structure and Development 40:258 –275.
Sandeman, D.C., R . Sandeman, C. Derby, and M. Schmidt. 1992. Morphology of the brain of crayfish,
crabs, and spiny lobsters: A common nomenclature for homologous structures. Biological Bulletin
183:304–326.
Sandeman, D.C., and G. Scholtz 1995 . Ground plans, evolutionary changes, and homologies in decapod
crustacean brains. Pages 329–347 in O. Breitbach and W. Kutsch, editors. The nervous system of
invertebrates: An evolutionary and comparative approach. Birkhauser, Basel .
Sandeman, D.C., G. Scholtz , and R.E. Sandeman. 1993. Brain evolution in decapod Crustacea. Journal of
Experimental Zoology 265:112–133.
Sandeman, R.E., and D.C. Sandeman. 1996. Pre- and postembryonic development, growth and
turnover of olfactory receptor neurons in crayfish antennules. Journal of Experimental Biology
199:2409 –2418.
Schachtner, J., M. Schmidt, and U. Homberg. 2005 . Organization and evolutionary trends of primary
olfactory centers in Tetraconata (Crustacea + Hexapoda). Arthropod Structure and Development
34:257–299.
Schmidt, M. 2007. The olfactory pathway of decapod crustaceans-an invertebrate model for life-long
neurogenesis. Chemical Senses 32:365–384.
Schmidt, M., and B.W. Ache. 1996. Processing of antennular input in the brain of the spiny lobster,
Panulirus argus. I. Non-olfactory chemosensory and mechanosensory pathway of the lateral and
median antennular neuropils. Journal of Comparative Physiology A 178:579 –604.
Schmidt, M., and D. Mellon. 2011. Neuronal processing of chemical information in crustaceans. Pages
123–148 in T. Breithaupt and M. Thiel, editors. Chemical communication in crustaceans. Springer,
New York.
Schmidt, M., L. Van Ekeris, and B.W. Ache. 1992. Antennular projections to the midbrain of the spiny lob-
ster. I. Sensory innervation of the lateral and medial antennular neuropils. Journal of Comparative
Neurology 318:277–290.
Scholtz , G., A. Braband, L. Tolley, A. Reimann, B. Mittmann, C. Lukhaup, F. Steuerwald, and G. Vogt.
2003. Parthenogenesis in an outsider crayfish. Nature 421:806.
Sekiguchi, H., and T. Terazawa. 1997. Statocyst of Jasus edwardsii pueruli (Crustacea, Palinuridae), with a
review of crustacean statocysts. Marine and Freshwater Research 48:715–719.
Serrano, L., E. Grousset, G. Charmantier, and C. Spanings-Pierrot . 2004 . Occurrence of L- and
D-crustacean hyperglycemic hormone isoforms in the eyestalk X-organ/sinus gland com-
plex during the ontogeny of the crayfish Astacus leptodactylus. Journal of Histochemistry and
Cytochemistry 52:1129 –1140.
Shaw, S.R., and S. Stowe 1982. Photoreception. Pages 291–367 in H.L. Atwood and D.C. Sandeman, edi-
tors. The biology of Crustacea, Vol. 3. Neurobiology: Structure and function. Academic Press, New
York.
Sillar, K.T., and P. Skorupski. 1986. Central input to primary afferent neurons in crayfish, Pacifastacus len-
iusculus, is correlated with rhythmic motor output of thoracic ganglia. Journal of Neurophysiology
55:678–688.
Simanton, W., S. Clark , A. Clemons, C. Jacowski, A. Farrell-VanZomeren, P. Beach, W.E. Browne, and
M. Duman-Scheel. 2009. Conservation of arthropod midline netrin accumulation revealed with a
cross-reactive antibody provides evidence for midline cell homology. Evolution and Development
11:260 –268.
Simon, T.W., and D.H. Edwards. 1990. Light-evoked walking in crayfish: Behavioral and neuronal
responses triggered by the caudal photoreceptor. Journal of Comparative Physiology A 166:745–755.
Sinakevitch, I., J.K. Douglass, G. Scholtz, R. Loesel, and N.J. Strausfeld. 2003. Conserved and conver-
gent organization in the optic lobes of insects and isopods, with reference to other crustacean taxa.
Journal of Comparative Neurology 467:150–172.
Smarandache, C., W.M. Hall, and B. Mulloney. 2009. Coordination of rhythmic motor activity by
gradients of synaptic strength in a neural circuit that couples modular neural oscillators. Journal of
Neuroscience 29:9351–9360.
Stensmyr, M.C., S. Erland, E. Hallberg, R. Wallén, P. Greenaway, and B.S. Hansson. 2005 . Insect-like
olfactory adaptations in the terrestrial giant robber crab. Current Biology 15:116 –121.
Steullet, P., H.S. Cate, and C.D. Derby. 2000. A spatio-temporal wave of turnover and functional matura-
tion of olfactory receptor neurons in the spiny lobster, Panulirus argus. Journal of Neuroscience
20:3282–3294.
Strausfeld, N.J. 2005 . The evolution of crustacean and insect optic lobes and the origins of chiasmata.
Strausfeld, N.J. 2009. Brain organization and the origin of insects: An assessment Proceedings of the
Royal Society of London Series B 276:1929 –1937.
Strausfeld, N.J., and J.G. Hildebrand. 1999. Olfactory systems: Common designs, uncommon origins?
Current Opinion in Neurobiology 9:634–649.
Strausfeld, N.J., and C.E. Reisenman. 2009. Dimorphic olfactory lobes in the Arthropoda. Annals of the
New York Academy of Sciences 1170:487–496.
Strausfeld, N.J., C.M. Strausfeld, R. Loesel, D. Rowell, and S. Stowe. 2006a . Arthropod phylogeny:
Onychophoran brain organization suggests an archaic relationship with a chelicerate stem lineage.
Strausfeld, N.J., C.M. Strausfeld, S. Stowe, D. Rowell, and R. Loesel. 2006b. The organization and evolu-
tionary implications of neuropils and their neurons in the brain of the onychophoran Euperipatoides
rowelli. Arthropod Structure and Development 35:169 –196.
Sullivan, J.M., and B.S. Beltz. 2001a . Development and connectivity of olfactory pathways in the brain of
the lobster Homarus americanus. Journal of Comparative Neurology 441:23–43.
Sullivan, J.M., and B.S. Beltz. 2001b. Neural pathways connecting the deutocerebrum and the lateral
protocerebrum in the brains of decapod crustaceans. Journal of Comparative Neurology 441:9 –22.
Sullivan, J.M., and B.S. Beltz. 2004 . Evolutionary changes in the olfactory projection neuron pathways of
eumalacostracan crustaceans. Journal of Comparative Neurology 470:25–38.
Sullivan, J.M., J.L. Benton, D.C. Sandeman, and B.S. Beltz. 2007a . Adult neurogenesis: A common strat-
egy across diverse species. Journal of Comparative Neurology 500:574–584.
Sullivan, J.M., M.C. Genco, E.D. Marlow, B.S. Beltz , and D.C. Sandeman. 2009. Brain photorecep-
tor pathways contributing to circadian rhythmicity in crayfish. Chronobiology International
26:1136 –1168.
Sullivan, J.M., and D.L. Macmillan. 2001. Embryonic and postembryonic neurogenesis in the ventral
nerve cord of the freshwater crayfish Cherax destructor. Journal of Experimental Zoology 29:49 –60.
Sullivan, J.M., D.C. Sandeman, J.L. Benton, and B.S. Beltz. 2007b. Adult neurogenesis and cell cycle
regulation in the crustacean olfactory pathway: From glial precursors to differentiated neurons.
Journal of Molecular Histology 38:527–542.
Sztarker, J., N.J. Strausfeld, D. Andrew, and D. Tomsic. 2009. Neural organization of first optic neuropils
in the littoral crab Hemigrapsus oregonensis and semiterrestrial species Chasmagnathus granulatus.
Journal of Comparative Neurology 513:129 –150.
Tazaki, K. 1988. The anatomy and physiology of the stomatogastric nervous system of Squilla. II. The
cardiac system. Zoological Science 5:299 –309.
Tyrer, N.M., and G.E. Gregory. 1982. A guide to the neuroanatomy of locust suboesophageal and thoracic
ganglia. Philosophical Transactions of the Royal Society of London Series B 297:91–123.
Ungerer, P., and G. Scholtz. 2008. Filling the gap between identified neuroblasts and neurons in crus-
taceans adds new support for Tetraconata. Proceedings of the Royal Society of London Series B
275:369 –376.
Utting , M., H.J. Agricola, R. Sandeman, and D. Sandeman. 2000. Central complex in the brain of crayfish
and its possible homology with that of insects. Journal of Comparative Neurology 416:245–261.
Vilpoux , K., R. Sandeman, and S. Harzsch. 2006. Early embryonic development of the central nervous
system in the Australian crayfish and the Marbled crayfish (Marmorkrebs). Development Genes
and Evolution 216:209 –223.
Whitington, P.M. 1996. Evolution of neural development in the arthropods. Seminars in Cell and
Whitington, P.M. 2004 . The development of the crustacean nervous system. Pages 136–167 in G. Scholtz,
editor. Evolutionary developmental biology of Crustacea. Balkema, Lisse, The Netherlands.
Wildt, M., and S. Harzsch. 2002. A new look at an old visual system: Structure and development of the
compound eyes and optic ganglia of the brine shrimp Artemia salina Linnaeus, 1758 (Branchiopoda,
Anostraca). Journal of Neurobiology 52:117–132.
Wilkens, L.A. 1988. The crayfish caudal photoreceptor: Advances and questions after the first half cen-
tury. Comparative Biochemistry and Physiology 91C: 61–68.
Wine, J.J., and F.B. Krasne. 1972. Organization of escape behaviour in crayfish. Journal of Experimental
Biology 56:1–18.
Wine, J.J., and F.B. Krasne 1982. The cellular organization of crayfish escape behavior. Pages 241–292 in
D.C. Sandeman and H.L. Atwood, editors. The biology of Crustacea. Academic Press, New York.
Zucker, R.S. 1972. Crayfish escape behavior and central synapses. I. Neural circuit exciting lateral giant
fiber. Journal of Neurophysiology 35:599 –620.
INDEX
Abdomen, 6, 9, 11–13, 16–19, 22, 24, 25, 27, 66, 87, 145, Amphionidacea, 4, 119, 120, 204, 210
191, 220, 280, 283, 284, 288, 305, 321, 330–332, Amphionides, 119, 120
348–351, 358, 360, 362, 365, 366, 456, 464, 465 Amphipoda, 3, 4, 35, 52, 62, 64, 82, 86, 87, 109,
Ablation, 228, 270, 337, 339, 349, 351, 352, 414 127, 178, 204, 210, 215, 219, 225, 226, 238, 239,
Absorption, of digestive products, 237, 238, 248, 251, 245–248, 250, 251, 253, 255, 256, 262, 264, 280,
253–256 281, 283, 284, 286, 287, 296, 320, 323, 325, 327,
Acanthomysis, 314 334, 353, 354, 357, 366, 385, 387, 390, 391, 393,
Acari, 369 395, 401, 404, 414, 418–420, 422, 425, 430, 438,
Acartia, 303–306 453, 461, 462
Acceleration reaction, 267, 269 Amplexus, 362, 363
Accessory cell, 95, 96, 413, 417, 420, 431, 440 Amputation, 270, 339, 346, 349
Acrothoracica, 3, 365 Anaspidacea, 3, 204, 321, 322, 357, 387, 388, 390, 393,
Active Gill Cleaning (AGC), 343, 347, 349–351. See 394, 398, 399, 455, 456
also Grooming Anaspides, 23, 127, 210, 218, 239, 251, 390, 394, 398
Adaptation, 4, 6, 18, 35, 57, 59, 62, 65, 109, 110, 117, 130, Anatomy, 8, 12, 14, 24, 28, 114, 117, 141, 200, 201, 261,
132, 153, 190, 199, 200, 204, 219, 220, 228, 241, 262, 264, 271, 287, 298, 321, 377, 406, 413, 415,
244–248, 261, 267, 269, 272, 276–290, 296–315, 418, 420, 424, 427, 430, 433, 438–441, 451,
337–369, 385, 439, 451 458–477
Aeglidae, 244, 349, 361, 435 Androgenic gland, 414, 415
Aesthetasc, 95, 177, 179, 181, 183, 186, 190, 202–205, Anlage, 11, 13, 14, 19, 22, 87, 91, 121, 122–124, 126, 387,
207, 213–216, 218, 224–226, 338, 339, 346, 347, 464, 473, 474
354, 355, 454–456, 474, 475 Annulus, 34, 41, 42, 44, 47–54, 57–59, 97, 170,
Afferent, 466 173–178, 184, 200–208, 210–215, 218, 219, 224,
Aggregation, 142, 245, 298, 312, 387, 420 228, 321, 326, 425, 474
Agnostus, 15, 38, 41, 45, 46, 48, 50, 51, 62, 68, 187, 188 Annulus ventralis, 425
Albuneidae, 280, 281, 284, 286 Anomopoda, 20, 118, 122, 209
Algivorous, 245 Anomura, 203, 210, 273, 284, 287, 337, 342, 343,
Alicella, 327 347–352, 361, 416, 418, 425, 431, 432, 457
Alima, 251 Anonyx, 251
Allanaspides, 394, 398 Anostraca, 3, 9, 13, 19, 20, 24, 28, 58, 60, 62, 66, 76, 77,
Alpheidae, 206, 285, 287, 349 96, 110, 121, 122, 124, 208, 213, 218, 225, 322, 324,
Alpheus, 285 356, 362, 363, 367, 380, 381, 393, 416, 425, 427,
Ambit, 306, 307 433, 451, 452, 455, 460
Amorphous calcium carbonate, 146, 147 Antarctomysis, 314
485
486 Index
Antenna, 6, 8, 10, 11, 14, 15, 19, 47, 48, 51, 53–58, 62, 64, Atrium oris, 238, 240, 247
65, 108, 110, 111, 115, 120–126, 177, 184–186, 189, Attachment, 10, 11, 17, 43, 95, 107, 110, 129, 146, 172,
199–229, 238–244, 247, 266, 276, 279, 280, 284, 174, 199, 200, 202, 203, 218–224, 263, 265, 271,
285, 288, 300–302, 305, 309, 320–326, 330, 332, 283, 307, 361, 366, 398, 403, 417, 420, 424
338–342, 348, 353, 354, 362–364, 368, 384, 387, Attachment disc, 202, 203, 221, 222
389, 451, 455–460, 474–476 Austropotamobius, 186
Antennal gland, 226 Autogrooming, 339, 341, 354, 368
Antennula, 34, 41, 43, 45, 46 Autotomy, 264, 349
Antennulary flicking, 216, 226, 339 Axon, 451–477
Antizoea, 128, 129
Aorta, 379, 381, 383–390 Balanus, 460
Apodeme, 239, 240, 271, 326, 327 Barnacle. See Cirripedia
Apomorphy, 8, 14, 15, 46, 51, 52, 56–61 Basipod, 34–68
Apoptosis, 95,96 Bathymedon, 215
Appendage, 6, 8, 10–15, 19, 24, 27, 34–68, 79, 80, Bathynellacea, 3, 386, 387, 393, 394
91, 108, 112, 118, 120, 127, 141, 151, 168, 172, 184, Bathynomus, 204, 215
188, 189, 200, 237–248, 255, 261–273, 276–289, Bauplan, 19, 23. See also Body plan
296–315, 320, 321, 324, 325, 331, 333, 337–369, Bentheuphausia, 61, 399
387–392, 440, 456, 467 Bimodal sensor, 177–183, 199, 218, 456
Appendix interna, 359 Biomechanical properties, 140, 142, 148
Appendix masculina, 357–359 Biomechanics, 140–161
Arachnida, 35, 368, 369 Biramous, 11, 13, 14, 19, 21, 22, 26, 27, 34, 35, 46, 63, 74,
Aragonite, 160 82, 84–90, 97, 199, 202, 205, 208–210, 221, 300,
Arcturus, 225 320, 326, 362
Argulus, 10, 17, 223, 365 Biramous limb, patterning, 14, 19, 27, 34, 74, 82–90,
Armadillidium, 146–148, 429 202, 205
Artemia, 12, 14, 19, 83, 314, 433, 460 Birgus, 203, 213, 215, 392, 405, 406
Arteries, 114, 376–380, 383–388, 461, 462 Blepharipoda, 280, 283–285
cardiac, 379, 380, 383–388 Blue crab, 146, 150, 151, 329, 428
Arthrobranchiae, 402 Bochusacea, 204, 402
Arthrodial cuticle, 151 Body plan, 1–29, 130, 261, 276, 429
Arthrodial membrane, 141, 152, 326 Bosmina, 20, 227, 314
Arthrodization, 41 Boundary layer, 113, 243, 299, 313
Arthropoda, 1–18, 25–29, 34–68, 74–87, 93–98, 104, Box crab, 280
109, 130, 140, 141, 160, 161, 167, 168, 174, 187–189, Brachyura, 71, 78, 105, 106, 114, 115, 141, 210, 216, 264,
192, 200, 201, 208, 217, 219, 229, 261, 263, 271, 271, 279, 283, 284, 287, 314, 328, 342–344, 351,
314, 315, 324, 338, 367–369, 377–380, 385, 406, 352, 357, 358, 366, 383, 392, 401, 404, 405, 416,
413, 420, 422, 424, 435, 440, 475, 476 418, 419, 424, 427, 428, 429–437, 452, 471
Arthropoda sensu lato, 37, 40–42 Brain, 221, 384–387, 389, 451–460, 462, 470–477
Arthropoda sensu stricto, 37, 40–42 Branchiae, 399, 400–402, 405, 406
Arthropodium, 41–44 phyllobranchiate, 400–402
Arthropodization, 41 Branchial chamber, 108, 114, 115, 117, 130, 140,
Ascothoracica, 3, 10, 24, 28, 240 151–153, 161, 228, 284, 337, 344, 346, 401–406
Ascothoracida, 10, 106, 118, 119, 202, 223, 248, 365, Branchial chamber cuticle, 151–153
380, 430 Branchinecta, 20, 323, 324, 363
Ascothorax, 119 Branchiopoda, 3, 9, 12–15, 18–22, 26–28, 39, 44, 48,
Asellus, 212, 215, 425, 453, 455, 461 52, 53, 56–67, 76, 82, 83, 85, 87–91, 94, 103–106,
Astacidea, 114, 287, 342, 343, 351, 357, 358, 361, 416, 109–113, 118–124, 130–133, 201, 208, 209, 211,
418, 419, 423, 425, 426, 430–437, 457 213, 218, 220, 221, 227, 238, 323, 324, 356, 362,
Astacilla, 225 367, 380, 384, 386, 390–393, 417, 421, 424, 429,
Astacus, 379, 418, 431, 454 430, 431, 451–454, 459–462, 472, 474–477
Asymmetry, 213, 218, 228, 282, 299, 307, 310, 313, 315, Branchiostegal folds, 131
349, 365, 388, 472 Branchiostegite, 107, 342, 343, 392, 402–405
Index 487
Branchipus, 451, 452 Caridoid, 24, 28, 64, 125, 127, 128, 211, 332
Branchiura, 3, 9, 10, 12, 16–18, 24, 25, 28, 104, 106, Caridoid facies, 125, 127, 211
109, 113, 131–133, 202, 208, 223, 240, 256, 355, Carnivorous, 6, 24, 241, 251, 301, 302, 309–312, 455
365, 380, 415, 417, 420, 423–426, 429, 433, 453, Carpus, 184, 228, 263–265, 272, 283, 329, 339–341,
455, 459, 461 348–350, 353
Bredocaris, 9–11, 15, 38, 55, 56, 58–60, 109, 128, 132, Casco, 245
133, 187, 201, 207 Castracollis, 21, 22, 122
Bristle. See Seta cDNA, 160
Brood chamber (carapace), 104, 106, 118–120, 125, Cell
338, 353, 366, 367 accessory, 95, 96, 413, 417, 420, 431, 440
Brooding, 14, 66, 103, 104, 106, 109, 118–120, 125, 126, dark, 393
132, 199, 220, 225, 226, 265, 338, 353, 354, 357, epithelial, 77, 142, 149, 151, 171, 392, 393, 401, 420,
362, 363, 366, 367, 424, 429, 438 421, 431, 433
Brushes, 228, 300, 337–369 follicular, 417, 419–424, 440
Buoyancy, 267, 269, 307, 312 founder (precursor), 95, 472, 475
Burgess Shale, 22, 37, 38, 201 germ, 420, 421, 431
Burrow. See Burrowing glial, 453, 470–472
Burrowing, 106, 107, 110, 112, 113, 115, 119, 226, 228, intercalary, 431
245–247, 276–290, 337–339, 352, 355, 365, 368, 467 neurosecretory, 470–472
Bursicon, 150 nurse, 417, 420, 421, 424, 431, 440
sensory, 95, 169, 174, 178–183, 190, 209, 213, 216,
Caeca, 237, 249, 251, 253, 255, 256 217, 263
Caenestheriella, 201, 393 sertoli, 413, 417, 431, 440
Calanus, 23, 297, 304, 309, 315, 379, 380 somatic, 414, 420, 421
Calappa, 279, 280 sustentacular, 431
Calceolus, 219 Cement gland, 218, 221, 222, 424
Calcite, 146–148, 151, 156, 160 Central nervous system (CNS), 12, 113, 217, 270, 383,
Calcium carbonate, 140, 146–151, 158–161 385, 451–453, 460–462, 465, 472, 473, 476
Calcium-ATPase, 158 Central pattern generator, 270, 271, 301, 467
Callianassa, 279, 285 Centropages, 243, 305, 356, 364
Callinectes, 105, 110, 141, 142, 144, 145, 150, 152, Centroptilum, 314
157–159, 160, 279, 329 Cephalic, 24, 27, 43, 47, 51, 55, 57, 58, 60, 66, 105, 120,
Callynophore, 215 125, 130–132, 202, 223, 225, 247, 299, 300–311,
Calocaris, 453 387
Cambrian, 10, 11, 15–17, 21, 22, 25, 27, 34–68, 103, 105, Cephalocarida, 3, 4, 9, 12, 15, 16, 18, 22, 23, 26–28,
109, 120, 121, 132, 187, 201, 202, 208 48–60, 66, 67, 201, 205, 208, 209, 211, 213, 216,
Cambropachycope, 50 240, 262, 362, 367, 386, 387, 392, 393, 417, 421,
Cambropachycopidae, 46 430–433, 437, 438
Campylonotus, 359 Cephalothorax, 66, 208, 279, 415
Cancer, 160, 213, 278, 280, 314, 428, 434, 471 Chela, 62, 192, 202, 223, 245, 246, 262, 270, 280, 281,
Candona, 364 337, 340, 347–351, 354, 362, 364, 366, 368, 456,
Caprella, 226 462, 463
Carapace, 17, 19, 20, 22–24, 26, 29, 103–133, 141, 146, Chelicerata, 18, 26, 40, 50, 64, 68, 208
148–160, 227, 267, 268, 280–286, 310, 329, 330, Cheliceriformes, 6
332, 350, 355, 356, 362, 365, 367, 368, 376, 383, Cheliped, 140, 145, 153–156, 161, 244–246, 284, 320,
391, 392, 394, 395, 399–405 329–332, 343, 347–352, 355
Carcinus, 141, 150, 252, 254, 272, 358, 452, 453 Chemoreceptive, 179, 181, 216, 301, 368
Cardiac arteries. See Arteries Chemoreceptor, 51, 178, 180, 183, 184, 186, 190, 212,
Cardiac nervous system, 461, 462 213, 216, 219, 228
Cardiac stomach, 249–251 Chemosensor, 53, 178, 179, 181, 183, 189, 190, 199, 209,
Caridea, 4, 206, 218, 228, 250, 280, 283, 287, 331, 212, 213, 216, 218, 224, 226, 273, 352, 354, 455,
337–343, 352–355, 359, 361, 366, 401, 415, 418, 456, 459
425, 430, 431, 434, 437, 438, 440, 465 Chengjiang, 36–38, 50
488 Index
Chengjiangocaris, 41 Corpo reniforme, 459

Cherax, 173, 186, 207, 210, 228, 384, 419, 421, 423, Cortical rods, 422, 423
426, 432, 434, 436, 454, 457, 458, 473 Corystes, 228
Chilopoda, 6 Coxa, 35, 36, 41, 42, 47, 49, 51–64, 169, 199, 208–211,
Chionoecetes, 358, 437, 439 223, 226, 263, 264, 265, 283, 300, 303, 326, 329,
Chiridotea, 285, 286 342–345, 357, 358, 366, 368, 395, 398–402, 415,
Chitin, 140, 142–151, 155, 161, 237, 240, 248, 255, 263, 469
307, 311, 338, 391, 424, 427, 437 Crab, 78, 104, 110, 113–115, 133, 146, 148–161, 169,
Chitin-protein fibrils, 140, 142–151, 155 186, 213, 226, 228, 244–246, 251, 254, 261, 264,
Cilia, 180–183, 190, 213–217, 237, 238, 251, 339, 342, 265, 267–273, 278–290, 297, 314, 319, 328, 329,
349, 351 332–334, 337, 341–352, 357–359, 361, 366, 368,
Cinerocaris, 61, 203, 204, 210 383, 392, 401, 404, 405, 414, 418, 422, 424–431
Circulation, 114, 115, 156, 332, 339, 351, 355, 366, aeglid, 244, 349, 361, 435
376–391, 402–406 albuneid, 280, 281, 284, 286
Circulatory system, 156, 376–406 anomuran. See Anomura
Cirripedia, 3, 9, 11, 14, 15, 24, 28, 45, 58, 63, 104, 106, blue, 146, 150, 151, 329, 428
109, 130, 202, 203, 210, 216, 218–222, 248, 322, box, 280
365, 380, 391, 392, 415, 417, 419, 425, 427, 429, brachyuran. See Brachyura
430, 431, 433, 437, 452, 455, 460 fiddler, 270, 272
Cladocera, 3, 9, 14, 18, 19, 20, 28, 62, 65, 104, 106, freshwater, 239, 350
110–112, 114, 118–120, 122, 125, 126, 209, 213, 220, galatheid, 184, 244, 348, 361, 401
227, 266, 356, 362, 364, 381, 385, 390, 393, 403, ghost, 267–272
416, 418, 454, 457, 460 grapsid, 113, 154, 271, 272, 405, 429
Clasper, 62, 362, 365, 369 green, 150
Clausocalanus, 306 hermit, 169, 186, 251, 269, 287, 341, 349, 361, 401,
Cleaning, 115, 184, 240, 305, 313, 329, 337–369. See 402, 405
also Grooming horseshoe, 104, 310, 368, 463, 464
Coenobita, 392, 400, 405 king, 269, 271, 349
Coherent, 26, 312, 313 land (terrestrial), 153, 161, 272, 453, 455
Collagen, 272, 387 lithodid, 346, 349, 361, 384
Combs, 189, 285, 337–340, 351, 354–356, 368 mole, 226, 280, 284, 287
Commissure, post-esophageal, 474 ocypodid, 114, 115, 405, 437
Composite pea, 261, 268
material, 140, 142, 148, 158 porcellanid, 244, 297, 349, 392, 401
setae, 167, 170, 173–178, 184, 186–188, 191 portunid, 110, 319, 320, 328, 329, 333, 334
Compound eye, 453–455, 457, 460, 474 raninid, 280
Computational fluid dynamics, 312 red, 272, 332
Conchoecia, 214, 220, 420 robber, 213
Conchostraca, 19, 20, 106, 209, 323, 362, 367, 381, 435 sand bubbler, 245
Condyle, 263, 264 semaphore, 114, 115
Confocal-Raman spectroscopy, 147 semiterrestrial, 115, 153
Copepoda, 2–4, 9, 10, 15, 16, 24, 25, 28, 53, 58, 60, sheep, 148, 153
63–66, 109, 201, 202, 205–228, 239–244, shore, 254
247–249, 253, 255, 256, 261, 266, 267, 296–315, snow, 439
322, 356, 364–380, 386, 389, 391, 392, 415–419, spider, 261, 264, 268, 269, 272, 273
422, 425–427, 429, 431, 435, 459 stone, 153
Copepodologist, 306 xiphosuran, 35, 368
Copulation, 8, 35, 66, 107, 225, 338, 357, 361–366, 429, Crangon, 215, 220, 252, 331
435, 438, 439 Crayfish, 346
Cor frontale, 389 Cruising, 299, 304–307, 312, 313
Corallianassa, 285 Crustacea sensu lato, 40–42, 45, 46, 48, 50
Corophium, 226, 256, 280, 285, 286 Crystallographic plane, 143–145
Corpo allungato, 459 Cubaris, 429
Index 489
Cumacea, 3, 105, 106, 115–117, 131, 189, 204, 210, 224, Digging mechanisms, 280, 289
253, 281, 321, 323, 357, 379, 380, 385, 387, 396, Dilatancy, 277, 280
402, 419, 425, 430 Dimorphism, sexual, 208, 213, 223, 225, 300, 301, 365,
Cuticle, 38, 41, 44, 95, 96, 107, 116, 129, 130, 140–161, 459, 467
167–192, 213, 214, 216–222, 247–251, 263, 282, Dioptric apparatus, 454, 455
288, 328, 338, 352, 357, 377, 378, 383, 389–406, Diplopoda, 6
424, 455, 456. See also Exoskeleton Diplostraca, 62, 65, 66, 110, 121, 122, 322, 362, 367
calcified, 140, 141, 146, 150–156, 158–161, 391 Directional limbs, 319, 330, 333
hardness, 142, 143, 148, 150, 151, 153–155, 158, 161 Distal-less, 14, 79, 80, 82–89, 96
permeability, 158, 159, 161, 213 Diverticulum, 250, 253
tanned, 141 Dolops, 106, 365, 426, 429
uncalcified, 140, 141, 151, 152, 156, 158 Dorsal carapace, 141, 148–151, 153, 157–160, 368
Cuticular glycoprotein, 141, 143, 151, 159–161 Dorsal shield, 106, 120, 130
Cyclestheria, 9, 14, 20, 49, 83, 118, 119, 122–125 Drag, 22, 106, 109, 110, 132, 172, 184, 220, 266, 267,
Cyclestherida, 3, 19, 20, 28, 106, 119, 121, 122, 125, 362 269, 288, 299, 301, 305, 307–309, 312, 313, 319,
Cyclopoid, 4, 307, 364, 365 320, 323–325, 327–333, 338, 339, 351, 354
Cyclops, 12, 13, 364 Drag-based, 309, 313, 319, 320, 324–328, 333
Cyprid larva, 106, 109, 110, 216, 218, 221, 222 Dromia, 343, 357, 358
Cyprinotus, 418, 419, 421 Drosophila, 13, 74–97, 190, 475
Duty factor, 266
Dactyl, 171, 263–265, 268, 271, 272, 280, 283, 287, 288,
324, 329, 341, 342, 346 Ecdysial suture, 149, 155
Daphnia, 65, 83, 110, 112–114, 118–220, 243, 363, 364, Ecdysis, 149, 150, 152, 155, 158–161
402, 403, 462, 477 Echiniphimedia, 247
Decapoda, 4, 14, 35, 62, 64, 104, 107, 110, 113–115, Edge index, 244
127–130, 140, 141, 160, 161, 168, 172, 175–177, 181, Egg, 15, 66, 106, 118–120, 190, 241, 261, 268, 296,
184, 186, 188, 190, 192, 203–207, 210–219, 224, 351–353, 356–358, 362, 366–369, 414, 418, 420,
226, 228, 237–240, 244, 245, 248–256, 264– 422, 424, 425, 439, 467
266, 269, 271–273, 277, 283, 284, 287, 377–394, Egg, winter, 118
399–406, 415, 416, 423–440, 452–459, 461, 462, Emerita, 226, 279, 281–288
467–472, 475–477 Enallagma, 314
Dendrite, 179, 181, 182, 213–218, 455, 465, 466 Encounter (reproductive), 298, 307, 362, 439
Dendrobranchiata, 4, 15, 57, 127–130, 211, 218, 228, Endite, 34, 41, 42, 47–62, 66, 74, 77, 85, 87–91, 96,
280, 283, 351, 357, 361, 366, 400, 404 199, 208, 211, 240, 243–247, 263, 367
Dendrobranchiate shrimp, 130, 351, 366, 404 Endocuticle, 140–143, 146, 148, 150–158
Dendrogaster, 430 Endopod, 14, 34–36, 41–54, 56, 59, 61–65, 68, 82,
Denticle, 38, 51, 79, 80, 82–84, 87, 88, 167, 169–176, 84–86, 97, 116, 184–186, 189, 203, 208–212, 216,
180, 184, 186–189, 192, 339 228, 240, 263, 309, 310, 321, 326, 328, 354–367,
Dentritic sheath, 178–180, 182, 183, 190, 216, 217 392, 397–401, 403
Deposit feeding, 226, 241, 244, 245, 247, 286 Endopodite, 284, 300, 302, 309, 397–399
Descending artery, 381, 384, 387, 388 Enoplometopus, 458
Deutocerebrum, 43, 451, 455–460, 472–474 Entomostraca, 12, 36, 39–44, 48, 52, 55–67
Devonohexapodus, 27, 29 Ephippium, 118, 119
Diapause egg, 118, 119 Epibiont, 337, 338, 354
Diaphragm, dorsal, 378, 379, 383, 389, 390 Epicuticle, 141–148, 150–153, 155, 158, 159
Diaptomus, 364 Epicuticular canals, 144, 146, 159
Diastole, 382 Epicuticular fibers, 144, 146, 159
Diastylis, 106, 116, 117 Epicuticular roots, 144, 146, 159
Diatom, 53, 244, 302, 339, 349 Epidermis, 77, 89, 95, 144, 150, 172, 208, 247, 342,
Digestion, 106, 177, 237–256, 416, 421, 429 367, 378, 403
Digestive gland, 238, 251, 253, 255, 421 Epipenaeon, 358
Digestive strategy, 256 Epipod, 34, 56, 66, 87, 88, 107, 108, 113, 115–118, 263,
Digging, 276–290 342–347, 362, 376, 383, 390–392
490 Index
Epipodite, 66, 106, 115, 117, 263, 376, 383, 390–404 Exoskeleton, 140–142, 145, 149, 158–161, 237–238,
Epithelial cell, 77, 142, 149, 151, 171, 392, 393, 401, 250, 261, 263–265, 269, 273, 276, 280, 282, 307,
420, 421, 431, 433 311, 337–339, 342, 352, 368, 391, 406
Epithelium, 76, 77, 81, 95, 106, 113, 115, 116, 141, Exteroceptor, 468
142, 149, 151, 158, 171, 177, 255, 376, 377, Extra-cellular matrix (ECM), 178
391–393, 395, 397, 398, 401, 403, 420–424, Exuvia, 149, 151, 152, 156, 158, 160, 177
428–434, 439 Eye, 12, 38, 119, 155, 168, 171, 172, 239, 272, 279, 284,
Eriocheir, 392 286, 321, 351, 353, 387, 404, 429, 453–455, 457,
Escape locomotion, 320, 328, 330–333 459–461, 474
Escape reaction, 107, 110, 305, 332 apposition, 455
Escape response, 110, 220, 228, 304, 308, 309, 330, superposition, 455
332, 356, 465
Escaping, 188, 240, 299, 304, 305, 308–312, 332 Facetotecta, 3, 24, 28, 58, 106
Esophagus, 237, 248–250, 253, 285, 389, 451, 455, 456, Falites, 54
461, 470 Farfantepenaeus, 344
Euarthropoda, 34–38, 40–48, 50, 51, 54, 56, 59, 62, Feeding, 10, 11, 14, 15, 34, 40, 44–46, 48, 51–55,
64, 67, 68 57–61, 64, 65, 66, 89, 103, 106, 108–116, 122, 127,
Euarthropodium, 34, 44, 45, 51, 54, 56, 59, 64 132, 167, 184–188, 192, 199, 200, 208, 211, 219,
Eucalanus, 215, 242, 243, 302, 356 220, 225, 226, 228, 237–255, 276, 285, 286, 288,
Eucarida, 4, 216, 226 296, 298, 299, 301, 302, 307–311, 319, 323–325,
Euchaeta, 226, 228, 310, 312 333, 337, 338, 342, 343, 347, 354, 355, 356, 362,
Eucrustacea, 9, 22, 27, 34, 35, 38–42, 45, 48, 51, 365, 368, 369, 394, 421
53–60, 62, 64–67, 208 Feeding function, 44
Eucypris, 439 Feet, 268, 270, 271, 273, 289
Eumalacostraca, 3, 4, 9, 15, 23, 24, 28, 58, 59, 62, Fiddler crab, 270, 272
64–66, 210, 262, 382, 417, 456, 461 Filter basket, 243, 245
Euperipatoides, 476 Filter feeding, 14, 59, 60, 184, 276, 286, 288, 365, 394
Euphausia, 4, 15, 105, 243, 251, 297, 313, 314 Filtration chamber (carapace), 104, 107, 112, 113, 253
Euphausiacea, 15, 57, 61, 64, 105, 107, 127, 204, 210, Flagellum, 57, 177, 185, 199–228, 319–323, 326, 328,
322, 357, 361, 379, 380, 387–389, 393, 395, 399, 333, 338, 339, 342, 354, 355, 362
403, 406, 455, 459 accessory, 203–206, 224, 226
Eurycope, 324, 325 primary, 203–207, 213, 215, 224, 226
Eurythenes, 327, 328 Flexion, 220, 308, 312, 319, 320, 324, 326, 332, 354,
Eusirus, 219 356, 365
Euterpina, 314 Flow field, 311, 312
Evolution, 1, 2, 8, 14, 15, 22, 25, 27, 34–68, 74, 75, 81, Fluid, 110, 177, 179, 219, 226, 241, 247, 250, 251, 255,
85, 87, 91, 93, 96, 97, 103, 105, 109, 112, 120–127, 256, 269, 277, 289, 296, 298–315, 319, 321, 325,
130–133, 168, 171, 172, 175, 187, 188, 191, 237, 238, 327, 332, 333, 390, 429
241, 248, 256, 261, 262, 265, 273, 278, 286, 289, Fluid, mechanical, 301, 304
297, 312, 313, 320, 330, 332, 337, 338, 342, 351, 352, Fluid Dynamics, 301, 304, 312, 319, 321, 325, 327, 333
355, 357, 363, 367, 369, 377, 381, 387, 388, 392, 398, Follicular cells, 417, 419–424, 431, 440
403–406, 413–415, 421, 424, 427, 435, 437–441, Foraging, 301, 304
455, 465, 475, 477 Force
Excretion, 67, 226, 310, 351, 392 compression, 153
Exhalant respiratory current, 112, 116, 117, 401 tensile, 148, 152, 278
Exite, 74, 77, 85, 89–91, 343, 367, 393, 399, 402 Foregut, 171, 172, 237, 238, 240, 246, 248–256, 389,
Exocuticle, 140–159 461
Exopod, 10, 14, 34–36, 41–45, 47–59, 62–65, 77, Fossils, 2, 3, 8, 11, 14–22, 26–29, 34, 36–38, 40–43,
82, 84–89, 97, 110, 115–118, 133, 199, 201, 203, 45–47, 49–51, 55, 56, 61, 64, 67, 104, 105, 120, 121,
208–212, 220, 223, 240, 247, 263, 300, 302, 308, 132, 133, 187, 188, 200, 201, 203, 209, 330, 432
309, 319–323, 326–328, 343–345, 354, 355, 358, Fouling (algal, microbrial, particulate, sediment),
359, 362, 364, 366, 392–403 337–339, 342, 346–357, 367, 368
Exopodite, 300, 302, 319–321, 398, 399, 402 Founder (precursor) cell, 95, 472, 475
Index 491
Fourier-transform infrared spectroscopy, 147 Grandidierella, 401

Freshwater crab, 239, 350 Granular materials, 276, 277, 278, 289
Functional Morphology, 10, 29, 167, 175, 190, 192, Granulocytes, 391
219, 261, 272, 273, 287, 296, 298, 304, 319, 320, Grapsidae, 113, 154, 271, 272, 405, 429
327, 330, 333, 334, 376, 377, 406, 413 Green crab, 150
Fuxianhuia, 41, 43 Grooming, 8, 167, 170, 184–186, 188, 192, 228, 264,
305, 337–369, 456
Gait, 267–270, 296, 299, 305, 307, 312, 324 antennal, 228, 368
Galatheoidae, 184, 244, 348, 361, 401 antennular, 228
Gammarus, 251, 414 embryo, 366
Ganglion, 250, 271, 451–457, 460–477 general, 350
abdominal, 454–456, 461–468 general body (GBG), 347, 348, 350, 351
commissural, 461, 470–472 gill, 349, 351
optic, 454, 458, 460, 470, 473, 475 passive, 342–347, 349, 350. See also Passive Gill
sheath, 453 Cleaning
subesophageal, 462, 463 pereopod, 348, 350
thoracic, 462–464, 467, 469–472 Grooming, active, 342, 343, 347, 349–351. See also
Gas exchange, 107, 108, 113–117, 153, 285, 338, 351, 377, Active Gill Cleaning
392, 399, 401, 403 Ground pattern, 35, 36, 40–46, 50, 54–67, 127, 380
Gastrolith, 160 Growth, 47, 76–81, 86, 87, 120, 122, 132, 140, 149, 338,
Gecarcoidea, 272 339, 346, 351, 352, 414, 415, 421, 422
Genes, 11–15, 18, 19, 22, 24, 28, 74, 75, 77, 79–85, Gustatory receptors, 186, 189, 190, 212, 477
87–94, 96, 97, 141, 200, 208, 240, 415, 438, 477
Geniculated, 225, 301, 365 Hansenomysis, 218
Genitalia, 8, 19, 24, 225, 300, 356, 357, 359–362, Haplopoda, 36, 106, 121, 125, 209, 220, 393
364–366, 369, 413, 415, 424–429, 433, 437, 438, Harpacticoidea, 267, 307, 356, 415
440 Head appendage, 8, 10, 43, 51, 62, 67, 238, 301, 312,
Germarium, 413, 418–421 387
Germ cell, 420, 421, 431 Head shield, 106, 122, 124, 128
Ghost crabs, 267, 268, 269, 271, 272 Head tagma, 65, 66
Gill, 34, 64, 65, 107, 108, 113–116, 118, 140, 141, 152, 153, Heart, 114, 278, 353, 376–390, 404, 462, 470
158, 161, 170, 184, 239, 245, 276, 284, 285, 314, Heart, globular, 380, 381, 385
337, 339, 342–354, 366, 368, 377, 383, 389–395, Heart, tubular, 380, 381, 384, 387
399, 401, 402 Heloecius, 114, 115
active cleaning (AGC), 343, 347, 349–351 Hemigrapsus, 476
book, 368 Hemimysis, 115, 116, 209, 210
branchial. See Branchial chamber Hemisquilla, 398
multilobate, 402 Hemocoel, 387
passive cleaning (PGC), 342–347, 349, 350 Hemocyanin, 391
Glial cell, 453, 470–472 Hemocytes, 390, 391
Glycoprotein, 141, 143, 151, 159–169, 221, 422 Hemoglobin, 113, 391, 403
Gnathite, 52 Hemolymph, 113, 117, 253, 376–378, 382–393,
Gnathobase, 7, 51, 53, 87, 88, 199, 208, 238, 244, 302 396–406, 421, 453, 470–472
Gnathophausia, 116, 321, 325, 326, 384, 395 Hemolymph lacunar system (HLS), 376, 378, 389
Gnathopod, 226, 245, 247, 280, 353, 354 Hemolymph vascular system (HVS), 377, 378, 384
Gnorimosphaeroma, 438 Henningsmoenicaris, 38, 47, 50
Gonochorism, 440 Hepatopancreas, 245, 251, 253, 254, 332, 383, 415,
Gonodactylus, 213, 215, 340, 346, 347, 353, 354, 384, 421, 429
458, 460 Heptacarpus, 339, 340, 348, 349
Gonopod, 337, 357, 358, 361–363, 369 Herbivorous, 244, 302, 311, 312, 455
Gonopore, 6, 7, 9, 16–27, 337, 356, 357, 361, 362, 365, Hermaphrodite, 10, 22, 23, 361, 362, 365, 413,
415, 424–429, 438 415–417, 437, 438, 440, 441
Goticaris, 39, 47, 50 Hermaphroditism, 438, 440
492 Index
Hermit crab, 169, 186, 251, 269, 287, 341, 349, 361, Isopoda, 3, 4, 35, 64, 82, 86, 95, 109, 127, 146–148, 151,
401, 402, 405 156, 161, 177, 182, 190, 203, 204, 208–210, 212,
Hesslandona, 38, 39, 47, 49, 54 213, 215, 218, 225, 240, 246, 248, 250, 251, 253,
Heterochrony, 45, 48, 60, 125, 130 255, 256, 262, 264, 280, 286, 314, 323–326, 352,
Heterorhabid, 302 354, 357, 358, 366, 377, 382, 385, 387, 388, 392,
Heterosaccus, 109, 314 397, 403, 414, 416, 418, 420, 425, 427, 429, 430,
Hexapoda, 6, 16, 18, 22, 26–29, 68, 130, 131, 200, 201, 432, 433, 435, 437–439, 441, 453, 455, 456, 461,
208, 228, 367, 376, 422 462, 476
High Reynolds number, 319, 320, 324, 325, 328, 333, Isotropic, 307
334
Hindgut, 237, 238, 248, 249, 251, 253, 255, 256, 461, Jasus, 418
464 Jet Propulsion, 310, 312, 319, 320, 330, 332, 333
Hippa, 286 Joint, 19, 34, 35, 41–45, 53, 56, 64, 74, 81, 91, 93, 96, 97,
Hippolytidae, 206, 349 151, 154, 210, 262–265, 271, 272, 289, 300, 301,
Holography, 298 309, 327, 333, 342, 362, 365, 456, 465, 467, 469
Homarus, 144, 148, 153, 160, 215, 255, 381, 418, 452, Joint, development, 77, 81
471, 473 Joint membrane, 34, 43, 56, 154
Hopping, 299, 304–311
Hormone, hyperglycemic, 471 Kinematics, 241, 268–270, 272, 298, 299, 302, 306–
Horseshoe crab, 104, 311, 368, 463, 464 309, 312, 315, 319, 321, 324–327, 329–331, 333
Horseshoe vortex, 311 King crab, 269, 271, 349
Hovering, 299, 307, 310–313 Krill, 57, 243, 296–298, 313, 321
Hox genes, 12, 13, 16, 19, 22, 24, 93, 200, 208, 240
Hutchinsoniella, 23, 201, 209, 211, 213, 386, 387, 431, Labidocera, 364, 419
433 Labium, 238, 240, 247
Hydrodynamic, 10, 103–111, 187, 188, 213, 218, 227, Labrophora, 39, 40, 42, 45, 48, 51, 53, 54, 55, 57, 60,
269, 278, 282, 311, 312, 320, 329–331, 333, 339, 66, 67
456 Labrum, 6, 11, 51, 53, 124, 126, 185, 238–240, 247, 252,
Hydrodynamics (carapace), 103–111 389, 456
Hydrostatic skeleton, 149, 156, 177, 178, 263, 456 Lacinia mobilis, 239, 240
Hygroreceptor, 181, 183, 190, 228 Lacuna, 108, 116, 376–378, 383, 389, 390, 397,
Hypodermis, 140, 142, 146, 149–151, 158, 161, 456 404–406, 472
Hypostome, 46, 51 Laevicaudata, 3, 9, 19, 20, 28, 104, 106, 110, 118, 119,
121, 122, 124, 220, 362, 367
Ibacus, 111, 279, 280 Lagerstätte, 36, 37, 65
Idotea, 177, 215, 314 Lamella, 106, 107, 115, 117, 140, 142–145, 148, 149,
Incisor process, 185, 239, 240, 244 151–153, 349, 366, 395, 396, 399–401, 403, 415,
Incubation, 337, 338, 350, 351, 354, 356, 357, 366, 367, 453
424 Laminar, 296, 298, 299, 307, 310–313, 324, 387
Inertia, 241, 298, 299, 304, 312, 313, 315 Land (terrestrial) crab, 153, 161, 272, 453, 455
Ingestion, 237, 238, 241, 243–250, 253–256, 285, 301 Larva, 8, 9, 11, 14, 15, 19, 20, 24, 36, 38, 45, 48, 53, 55, 57,
Inhalant respiratory current, 108, 116, 120 58, 64, 74–81, 89, 91–97, 103, 104, 106, 109, 110,
Inner dentritic segment (IDS), 179, 180, 214, 216 118–125, 127–132, 168, 200–203, 205, 207, 216,
Insecta, 6, 8, 11, 12, 22, 35, 36, 40, 45, 46, 64, 67, 75, 77, 218, 221, 222, 226, 241, 296, 297, 313, 314, 321,
80–82, 91, 95, 96, 130, 140, 141, 149, 150, 154, 160, 322, 325, 349, 365, 399, 414, 424
167, 172, 178, 181, 183, 189–192, 200, 208, 228, cyprid, 106, 109, 110, 216, 218, 221, 222
261–264, 271, 272, 324, 367–369, 419–422, 425, kentrogon, 222
427, 433, 463, 464, 468, 475, 476 nauplius, 8, 11, 14, 15, 19, 20, 45, 53, 56, 57, 106, 109,
Insemination, 338, 356–362, 369 118, 120, 127, 128, 132, 168, 199, 202, 205–211, 220,
Intercalary cell, 431 222, 228, 247, 299, 314, 322
Interneuron, 452, 453, 455, 459, 460, 462, 464–467 trichogon, 222
Interprismatic septum, 144, 146, 149–151, 155, 160 vermigon, 222
Intersexuality, 438 zoea, 14, 57, 78, 128–130, 206, 207, 211, 212, 297
Index 493
Lateral giant escape circuit, 465 Lophogastrida, 3, 107, 115, 116, 127, 204, 215, 321, 323,
Lateralia, 249, 250 384, 386–390, 393, 395, 401, 402, 404
Leakiness, of setae, 216, 242, 243, 301 Loxorhynchus, 148, 153
Leanchoilia, 41–43, 50, 200 Lung, 113, 115, 377, 383, 392, 403–406
Lebbeus, 458 Lung (carapace), 113, 115
Lectin, 36, 43, 156, 157, 160, 186, 221, 383, 429, 430 Lynceus, 20, 119, 124
Lepeophtheirus, 249 Lysiosquilla, 128, 279
Lepidocaris, 9, 21, 28, 63, 65, 66, 121, 122 Lysmata, 215, 361
Lepidopa, 279, 286, 297
Leptestheria, 435 Maceration, 237, 250, 251, 255
Leptochela, 262 Machilis, 476
Leptodora, 20, 62, 63, 83, 118, 122, 125, 126, 220, 227, Macrobrachium, 146, 425, 458
390, 454, 457 Macropetasma, 57, 359
Leptostraca, 24, 104, 105, 107, 112, 127, 129, 132, 204, Malacostraca, 2–5, 8, 9, 12–15, 18, 22–24, 26–28, 35,
205, 210, 280, 282, 322, 367, 387, 393, 394, 398, 36, 38, 40, 42, 44, 46, 50, 52, 55–62, 64–67, 82,
403, 416 83, 87, 103–105, 109, 110, 113, 114, 116, 118, 120,
Leucon, 379 125, 127–133, 167, 176, 177, 190, 191, 199–208,
Leurocyclus, 419, 428 210–216, 218, 228, 237, 240, 249, 250, 252, 253,
Lift, 41, 110, 111, 221, 226, 239, 240, 245, 247, 266, 267, 255, 262, 319–321, 325, 328, 330, 332, 333, 337,
269, 319, 320, 328, 329, 331, 333 352, 354, 357, 366, 367, 377, 379–394, 398, 399,
Lift-based, 319, 320, 328, 329, 333 402–405, 415, 417–421, 424, 425, 429, 440,
Lifting setae, 239, 240, 247 452–454, 456–462, 470, 472, 474, 475
Light cell, 393 Manca, 14
Ligia, 156, 435 Mandible, 8, 10, 11, 14, 18, 38, 47–49, 51, 53–55, 57, 58,
Limb 61–64, 116, 120, 121, 123, 125, 126, 173, 185, 199,
bud, 11, 19, 75–77, 82, 84–89, 91, 94, 96 200, 208, 220, 228, 238–240, 244, 246, 247, 249,
formation, 19, 36, 89 255, 285, 300–302, 323, 354, 368, 419, 420, 462,
larval, 77, 91, 93, 94 471, 474
phyllopodous, 82, 84, 87–89, 113, 323, 362 Mandible incisors, 239, 246, 247
plane, 264 Marsupenaeus, 160, 332
primordia, 79, 80, 84, 90 Marsupium, 14, 226, 265, 354, 357, 358, 366
sensory, 8 Martinssonia, 9, 11, 15, 39, 41, 42, 47, 50
Limnoria, 246 Mating, 104, 119, 199, 200, 219, 223–225, 228, 296,
Linderiella, 363 298, 301, 305, 306, 310, 312, 338, 356, 357, 360–
Liquefaction, 277 369, 414, 415, 427, 429, 433, 435, 437–440, 455
Lithodes, 349 Mating behavior, 200, 365, 414, 415, 440
Lithodidae, 346, 349, 361, 384 Mating strategies, 414, 427, 435
Lobopodians, 41 Matrix proteins, 159, 160
Lobopodium, 37, 41, 45, 64 Maxilla, 8, 11, 21, 22, 26, 53, 55–61, 64–66, 106, 108,
Lobster, 4, 8, 64, 104, 110, 143, 144, 146, 148, 151, 153, 114–116, 120, 121, 128–132, 168, 170, 173, 178, 185,
154, 161, 168, 177, 182, 189, 210, 221, 226, 227, 255, 186, 188, 226, 238–242, 244, 247, 285, 300–302,
261, 280, 284, 287, 320, 321, 330–333, 342, 349, 305, 343, 354–356, 368, 395, 401–403, 462, 474
351, 357, 358, 361, 366, 381, 387, 401, 418, 422, Maxilliped, 11, 16, 17, 24, 26, 60, 61, 64–66, 78, 93,
425–427, 437, 455, 458, 459, 465, 471, 474 107, 108, 115–118, 169, 171–173, 184, 185, 208, 226,
Locomotion, 7, 43–46, 48, 50, 53, 60, 62, 64, 110, 151, 228, 238–240, 242, 244, 245, 272, 284, 285, 287,
167, 184, 200, 219, 261, 263, 264, 266, 267, 269, 288, 300–302, 305, 308–311, 337, 338, 340, 341,
271, 272, 277, 281, 286, 287, 296–315, 319–321, 343–347, 352–356, 393, 395–397, 401–403, 456,
323–333, 337, 338, 355, 357, 362, 368, 369 462
Locomotory, 6, 10, 11, 22, 34, 40, 44, 46, 51, 55, 60, Maxilliphimedia, 247
110, 220, 240, 296–301, 304, 305, 308, 310–313, Maxillopoda, 2–4, 9, 10, 12, 13, 15, 18, 22–25, 27, 28, 57,
315, 321, 323, 342 58, 60, 67, 83, 355, 356, 365, 366, 417, 452, 460
Locomotory function, 220 Maxillula, 42, 49, 52, 53, 55–61, 64, 65, 365
Lophogaster, 215, 224, 384, 386, 390, 401, 402, 404 Mechanoreceptive, 181, 183, 311
494 Index
Mechanoreceptor, 96, 167, 179–184, 189, 190, 192, Molting, 14, 109, 118, 129, 156, 161, 177, 179, 212, 218,
209, 213, 217, 228, 301, 310, 313 286, 337–339, 352, 356, 424, 437
Mechanosensor, 96, 180, 181, 189, 190, 199, 213, Monophyletic group, 2, 8, 15, 16, 19, 20, 25, 26, 29,
216–219, 226, 228, 454, 456, 459, 465 56, 121
Medulla externa, 457, 460, 461, 474, 476 Motor neuron, 250, 265, 273, 452, 453, 460–462,
Medulla interna, 457, 460, 461, 474 464–470
Medulla terminalis, 457, 458, 470, 473, 475 Mouthparts, 16, 17, 55, 58, 60, 61, 91, 107, 108, 115,
Megabalanus, 203, 216, 222 168, 169, 172, 182, 184, 186–188, 226, 238–241,
Meganyctiphanes, 23, 379, 395, 399 245–248, 276, 285, 299, 301, 302, 305, 354, 355,
Melicertus, 359 368, 388, 393, 401, 455, 456, 475
Melita, 401 Mud, 112, 115, 245, 276–280, 285, 289, 290, 342, 349,
Membrane 352
arthrodial, 38, 141, 152, 158, 160, 200, 264, Multifunctionality, 35, 44, 45, 96, 199, 219, 296, 299,
326, 399 301
stridulatory, 227 Multioared, 307
synaptic, 452 Munida, 168, 170, 173, 239, 283
Membranous layer, 140–142, 148, 151 Munneurycope, 324, 325
Menidia, 304 Munnidopsidae, 320, 324
Menippe, 153 Muscle, 42–44, 59, 74, 75, 94, 95, 98, 146, 200, 202,
Meristematic zone, 207, 208, 212 203, 205, 208–210, 220, 223, 238–240, 248–255,
Merostomata, 7 263–265, 267, 270–273, 283, 284, 289, 303, 307,
Merus, 263–265, 272, 283, 284, 329 309, 321, 324–328, 332, 378, 380–383, 386–389,
Mesocyclops, 12, 13 403, 418, 433, 454, 456, 462, 464–469, 474
Mesocypris, 262, 266 Musculature, 42, 44, 107, 200–205, 209, 212, 223,
Mesodermal stroma, 420 238, 255, 265, 299, 301, 303, 325–328, 332, 333,
Mesopodopsis, 223 387, 389, 393, 452, 460–462, 465, 467, 472, 474
Metachronal, 243, 303, 307, 309, 313, 320, 321, 323, Myelination, 309, 465
325–327, 355, 467 Myoarterial formation, 386–389, 404
Metachronal beat, 320, 323, 325–327 Myocardium, 378–385
Metacrangonyx, 215 Myodocopa, 25, 28, 201, 208, 214, 220, 226, 355,
Metaingolfiella, 262 364–367
Metamorphosis, 11, 14, 75, 77, 78, 91, 94, 95, 104, 221, Myodocopida, 3, 453
222 Myriapoda, 6, 8, 11, 14, 18, 27, 35, 36, 40, 45, 46, 64,
Metanauplius, 14, 15, 209, 211 68, 200, 201, 208, 228, 367–369, 376, 422, 424,
Metopograpsus, 154–156, 429 476
Microcrustaceans, 105, 296, 298, 300, 302, 310 Mysida, 3, 64, 95, 105, 115, 116, 127, 177, 218, 223,
Micropacter, 23 224, 240, 249, 251, 297, 314, 321, 323, 332, 354,
Microphytobenthos, 244 386–389, 396, 402, 404, 430, 431, 438, 455, 459,
Microvilli, 142, 149, 150, 454 462
Mictacea, 3, 4, 108, 118, 204, 321, 323, 386–389, 396, Mysidacea, 107, 115, 127, 204, 209, 210, 226, 323, 357,
402 404, 452, 455, 456
Mictocaris, 118, 389 Mysidopsis, 13, 82, 354
Midgut, 114, 237, 238, 248–253, 255 Mysis, 95, 105, 107, 115, 116, 177, 206, 209–212, 218, 452
Migration, 91, 126, 227, 297, 298 Mystacocarida, 3, 4, 9, 10, 12, 15–18, 22, 24–28, 48,
Mineral, 140–161, 244, 245, 254, 256, 263, 392 49, 53, 58, 64–66, 201, 208, 210, 211, 214, 226,
Mole crab, 226, 280, 284, 287 355, 356, 366, 380, 392, 460
Mollusca, 247, 289, 421
Molt, 11, 14, 77, 78, 91, 93, 95, 109, 118, 120, 129, N-acetylglucosamine, 142, 143
141, 142, 144, 146, 149–153, 155–161, 170, 173, Najna, 246
177–179, 189, 206, 207, 211, 212, 218, 222, 247, Nannastacus, 105
250, 286, 337–339, 352, 356, 366, 368, 424, 425, Nanofibrils, 142, 143
437, 438, 470, 475 Natatolana, 215, 218
Molt cycle, 142, 149, 152, 161, 177, 470 Naupliar process, 14, 15, 211
Index 495
Naupliar shield, 109, 120, 128, 132 Orchestia, 82, 83, 86, 87, 401, 414
Nauplius, 8, 11, 14, 15, 19, 20, 56, 57, 168, 206–209, 211, Orconectes, 165, 215
222, 247 Orsten, 15, 16, 27, 34, 36–40, 43, 45, 47, 50, 55–60, 103,
Nebalia, 52, 83, 105, 107, 112, 129, 279, 280, 282, 398, 109, 128, 131–133, 187, 188
461 Orthonauplius, 15, 206
Nematobrachion, 359 Osmoreceptor, 181
Neomysis, 95, 177, 224, 314, 386 Osmoregulation, 66, 106, 113, 114, 376, 377, 392–405,
Neoteny, 125 470
Nephrops, 278, 331, 358 Ossicle, 237, 246, 249–251
Nerve, 75, 114, 217, 219, 385, 388, 451–453, 456, Ostium, 379, 383, 384, 386, 404
460–466, 468–474 Ostracoda, 2, 3, 9, 15, 16, 18, 25, 28, 36, 38, 104, 106,
Nervous system, 12, 96, 106, 113, 192, 217, 270, 333, 113, 118, 119, 130, 201, 208, 216, 220, 240, 247,
383, 385, 451–477 248, 253, 262, 266, 337, 340, 355, 363–365, 367,
Nervous system, cardiac, 461, 462, 471 369, 377, 380, 385, 389, 391, 392, 402, 403, 406,
Neural circuit, 270, 462, 464, 465, 469, 472 415–421, 423, 425, 426, 429, 432, 433, 435, 439,
Neuroanatomy, 461, 462, 465–468, 469, 475, 476 453, 459, 461, 462
Neuroblast, 472, 473 Outer dendritic segment, 169, 178–183, 189, 190, 209,
Neuroendocrine, 470–472 213, 214, 216, 217
Neurogenesis, 472 Ovalipes, 279, 280, 284
Neuron Ovariole, 419, 421
giant motor, 465, 466 Ovary, 353, 358, 414–428, 437, 438
inter-, 452, 453, 455, 459, 460, 462, 464–467 Oviduct, 356–359, 418–429
motor, 250, 265, 273, 452, 453, 460–470
sensory, 95, 183, 218, 452–456, 459, 460, 463–470, Pachygrapsus, 344
475 Pacifastacus, 83, 463, 468
Neurosecretory cell, 470–472 Paddling, 22, 26, 35, 41–45, 47, 50, 53–65, 110, 220,
Notostraca, 3, 9, 19, 20, 28, 78, 104, 106, 110, 120–124, 242, 243, 299–301, 309–313, 319, 321–333, 354
130, 132, 201, 214, 322, 323, 362, 367, 380, 381, Pagurus, 160, 169, 185, 186, 213
403, 421, 460 Palaemon, 171, 177, 206, 340, 348, 476
Nurse cells, 420, 421, 424, 440 Palaemonidae, 206
Palinura, 342, 343, 351, 361, 437
Ocypode, 113, 268, 279, 281, 392, 405, 428 Pancrustacea, 12, 28, 29, 80, 89, 208
Ocypodidae, 114, 115, 405, 437 Pandalus, 339–341, 350
Oelandocaris, 42, 46, 50 Panulirus, 169, 173, 177, 182, 185, 207, 213, 215, 216, 218,
Ogyrides, 283 226, 227, 228, 331, 455, 474
Oithona, 306 Pappose, 167, 173–176, 179, 184, 186, 187, 238
Olfaction, 177, 179, 189, 190, 212, 228, 337, 338, 355, Papposerrate, 167, 173–176, 186
454–459, 472–477 Paracalanus, 306
Olfactory globular tract (OGT), 457–459 Paraceradocus, 245, 353, 354
Olfactory lobe, 455, 457, 459, 473, 475–477 Paracerceis, 427, 432, 439
Olfactory receptor, 177, 228, 454, 455, 459, 474–477 Paragnath, 51, 169, 188, 238, 240
Olfactory receptor neuron (ORN), 177, 454, 455, Paralomis, 384
459, 474–476 Parandania, 247
Ommatidium, 454, 460, 461 Paranthessius, 249
Onesimoides, 246 Parasite, 16, 25, 119, 223, 247, 248, 256, 338, 355, 366,
Onychopoda, 20, 36, 62, 106, 118, 122, 125, 209, 393 367, 414, 438
Oocyte, 413, 418–427, 433, 437, 438, 440 Parasitism, 2, 16, 18, 24, 25, 58, 109, 119, 202, 214, 222,
Oocyte envelopes, 433, 440 223, 225, 239–241, 247, 248, 256, 307, 338, 355,
Oogenesis, 415, 419–422, 424, 440 365–367, 414, 418, 438, 451
Oostegite, 66, 354, 358, 366, 401 Passive Gill Cleaning (PGC), 342–347, 349–350.
Opiliones, 368, 369 See also Grooming
Opisthosoma, 7, 35 Patterning, 74–98
Optic ganglia, 454, 458, 460, 470, 473, 475 Patterning axes, 78, 79, 81, 85, 87, 90, 93, 97, 98
496 Index
Pauropoda, 6, 201 Pleoticus, 206, 212, 423

Pea crab, 261, 268 Pleurobranchiae, 263, 346, 395, 399
Pedaling, 221, 267, 320, 324, 325, 328 Pleuromamma, 216, 217, 228, 311
Pedipalp, 7, 208, 368 Pleuroncodes, 331, 332, 348
Peduncle, 59, 202–206, 210, 213, 214, 218, 219, 223, Plumose, 167, 170, 173–176, 179, 180, 184–188, 191, 210,
224, 286, 322, 323, 326–328, 333, 415, 435, 452 220, 238, 244, 245, 251, 288, 324, 329, 332, 349
Penaeoidea, 250, 339, 342, 343, 346, 357, 360, 361, Podobranchiae, 395
400, 423, 426, 431, 436 Podocop-, 3, 16, 18, 25, 28, 201, 208, 216, 220, 355,
Penaeopsis, 128 363–365, 369, 403
Penaeus, 105, 128–130, 133, 169, 185, 254, 404 Podocopida, 3, 369, 403
Penis, 25, 357, 364–366, 369, 433 Podomeres, 44, 50, 53, 59, 62, 97, 200
Pentastomida, 3, 16–18, 25, 28, 420 Polyartemiella, 363
Peracarida, 3, 4, 14, 62, 64, 66, 77, 82, 86, 87, 113, Polychaete, 247, 256, 289, 421
115–118, 127, 131, 174, 176, 177, 204, 209, 210, 216, Polyspermy, 422
239, 263, 265, 337, 354, 357, 366, 386, 389, 401, Pontoeciella, 225
404, 417–420, 423, 429–431, 433, 435 Porcellana, 244
Pereopod, 52, 64, 110, 114, 115, 153, 184, 228, 244, 262, Porcellanidae, 244, 297, 349, 392, 401
279–288, 303–306, 308–311, 319, 320, 324–332, Porcellio, 12, 13, 82–87, 146, 147, 251, 358, 403
337, 340–350, 354, 358–366, 401, 402, 404, 455, Pore canals, 142–151, 154
456, 475 Portunidae, 110, 319, 320, 328, 329, 333, 334
Pericardial organ, 470, 471 Portunus, 160
Pericardium, 376, 378, 391, 405 Postantennular appendage, 34–36, 41, 48, 60, 67
Perineurium, 385, 453 Postcommissural organ, 470–472
Periplaneta, 476 Postecdysial stages, 158
Petasma, 57, 66, 357, 359, 361 Postecdysis, 159–160
Phenoloxidase, 143 Postmolt, 141, 142, 144, 146, 149–153, 158, 159
Pheromone, 212, 219, 224, 225, 307, 310, 312, 455 Power Stroke, 184, 220, 266, 270, 299, 303, 307–309,
Phosphatocopina, 15, 39, 40, 42, 45, 54, 58–60 312, 313, 321, 323–328, 331, 355, 467
Photoreceptor, 453–455, 460, 461 Praunus, 321, 404
Phreatoicus, 262 Predator, 36, 122, 125, 148, 153, 188, 199, 218, 220,
Phyllobranchiae, 400–402 226–228, 238, 246, 247, 249, 253, 272, 278, 281,
Phyllocarida, 3, 9, 28, 56, 58, 59, 61, 82, 87, 203, 204, 282, 298, 301, 303–313, 324, 328, 330, 331, 333,
210, 367, 417, 461, 476 352, 356, 438, 455, 465
Phyllopodous, 82, 84, 85, 87–90, 107, 112, 113, 320, Predator deterrence, 227
323, 362 Preecdysis, 160
Phylogeny, 12, 18, 25, 26, 34, 37, 40–45, 65, 67, 103, Preening, 337–339, 351, 354, 367, 368. See also
120–122, 127, 128, 131, 192, 208, 273, 325, 333, 334, Grooming
338, 369, 380, 404, 414, 424, 427, 429, 432, 437, Premolt, 141, 142, 146, 149, 150, 152, 153, 156, 158, 177,
440, 441, 459 178, 424
Picojet, 308 Prism, 144, 146–151, 155, 160
Pivot joints, 41, 43 Probopyrus, 366
Plagusia, 272 Proboscis, 7, 16
Plankton, 4, 208, 214, 218, 220, 221, 224, 226, 228, Procambarus, 12, 13, 114, 153, 161, 344–347, 350, 384,
244, 296–299, 305, 311, 313, 315 400, 454, 466, 469, 473, 477
Plaques, 149, 150 Promotor, 238, 265, 299, 328, 469
Pleocyemata, 343, 366 Proprioceptor, 456, 468
Pleon, 9, 12, 13, 24, 25, 61, 66, 110, 125, 387, 392, 405, Propodus, 153, 184, 228, 264, 265, 271, 283, 324, 329,
406 341
Pleopod, 24, 58, 59, 61, 62, 65, 66, 77, 82, 87, 117, 119, Propulsion, 111, 298, 301, 304–312, 319–334
120, 226, 243, 245, 279, 280, 283–285, 287, 288, Prosoma, 6–8, 11, 35, 200, 368, 429
313, 319–328, 332, 333, 337, 348, 351, 352, 354, Prosome, 300–302, 308
357–361, 366, 387, 392–395, 397, 403, 424, 425, Protein, 18, 85, 140–151, 155, 159–161, 180, 181, 189, 221,
462–465, 467 245, 254, 311, 421, 422, 424, 429, 433, 476, 477
Index 497
Protocerebrum, 451, 455, 457, 458, 459, 461, 473–476 Return stroke, 226, 266, 270, 309, 321, 467
Protopod, 199, 202, 205, 208–211, 220, 221, 223, 240, Reynolds number, 113, 184, 241, 296, 298, 314,
263, 322, 362, 366, 393 319–321, 323–325, 328–330, 332–334
Protozoea, 57, 128–130, 206, 208, 211, 212 Rhabdom, 454
Proximal/distal axes, 50, 60, 61, 81, 90, 200, 202 Rhabdomere, 454
Pseudoprotella, 225 Rhizocephala, 3, 4, 202, 222, 223, 248, 349, 391, 430
Pupa, 77, 78, 80, 81, 94, 95 Rhynchocinetes, 359, 431, 434, 436
Pycnogonida, 7, 11, 14, 18, 26, 68, 368, 422 Rimapenaeus, 343–347, 360
Pyloric stomach, 249–251 Robber crab, 213
Rome organ, 216
Quinone cross-linking, 143, 158 Rowing, 309, 320, 321, 323, 326–332
Running, 266–269, 272
Ramus, rami, 9, 14, 22, 34, 35, 41, 42, 44, 51, 54,
57–59, 62, 65, 66, 203, 204, 205, 208–211, 279, Sand, 115, 116, 218, 245, 276–290, 307, 352, 368
287, 291, 300, 308, 309, 322–324, 326–328, 333, Sand bubbler crab, 245
361, 366, 388, 399, 400 Sarcolemma, 381, 382
Raninidae, 280 Sarcomere, 271, 382
Raptorial, 62, 104, 106, 110, 120, 125, 278, 301, 302 Sarcoplasmatic reticulum, 382
Rasp and file, 153, 246, 247 Scaphocerite, 57, 58, 210
Receptor Scaphognathite, 114, 116, 244, 343, 395, 401
chemo-, 51, 178, 180, 183, 184, 186, 190, 212, 213, 216, Scavenging, 122, 218, 238, 246, 247, 286, 311, 327, 328
219, 228 Schlieren, 298, 310, 312
gustatory (taste), 186, 189, 190, 212, 477 Sclerotization, 19, 37, 38, 41, 56, 59, 61, 141–143, 223,
hygro-, 181, 183, 190, 228 391, 402, 403
mechano-, 96, 167, 179–184, 189, 190, 192, 209, 213, Sclerotized, 19, 37, 38, 41, 48, 56, 59, 61, 141, 223, 402,
217, 228, 301, 311, 313 403
olfactory, 177, 228, 454, 455, 459, 474–477 Scolopale, 167, 179–183, 190, 209, 216–218
photo-, 453–455, 460, 461 Scolopendra, 476
thermo-, 183, 190 Scopimera, 245
Recovery Stroke, 184, 220, 299, 307–309, 312, 313, Sculling, 319, 328, 329, 333
323–328, 333 Scyllarid lobsters, 110, 210, 221, 284, 330
Red crab, 272, 332 Scyllarides, 148, 331
Rehbachiella, 9, 11, 15, 21, 22, 28, 38, 39, 49, 52, Secondary shield, 122, 124
55–60, 62, 103, 109, 120–124, 128, 131–133, Sediment, 22, 115, 117, 226, 238, 244–247, 256,
187, 201, 207 276–280, 282, 284–289, 337–339, 342, 343, 346,
Remipedia, 3, 4, 8–12, 15, 16, 18, 22–28, 64, 65, 104, 347, 349, 351, 352, 355
187, 199, 201, 202, 204–206, 208, 214, 314, 322, Semaphore crab, 114, 115
354, 355, 362, 392, 417, 418, 425, 430, 437, 438, Semibalanus, 314
459, 475 Seminal receptacles, 357, 362, 417, 424–429, 433,
Remotor, 238, 265, 299, 328 435, 437–439
Reproductive system, 35, 106, 222, 247, 297, 311, 325, Seminal vesicle, 364, 429, 433, 439
337–339, 351, 352, 356–369, 413–441 Semiterrestrial crab, 115, 153
Reptantia, 4, 64, 218, 459 Sensillum, 218
Resilin, 272, 309 Sensillum, hooded, 218
Respiration, 103, 106–109, 112–117, 127, 132, 199, 220, Sensor, bimodal, 167, 177–183, 183, 189, 190, 192, 199,
228, 276, 325, 376, 391–406, 429 218, 221, 456
Respiration chamber (carapace), 103, 104, 107, 108, Sensory cell, bimodal, 183
113, 114, 132 Sensory cilium, 179, 181, 182, 190
Respiratory filament, 153, 400 Sensory function, 57, 95, 167, 174, 175, 179, 181, 184,
Respiratory function, 106, 113, 114, 392–394, 403 186, 188, 192, 212, 218, 285
Respiratory pores, 108, 116, 117 Sensory nervous system, 453–456, 474, 475
Respiratory system, 103, 106–109, 112–117, 127, 132, Sensory receptor. See Receptor
199, 220, 228, 276, 325, 376, 391–406, 429 Sergestes, 314
498 Index
Sergestoidea, 250, 339, 343, 357, 361, 400 Spelaeogriphacea, 3, 4, 105, 117, 118, 204, 323, 384,
Seriality, 34, 43, 45, 46, 48, 50, 53, 54, 56, 58, 59, 65, 386, 387, 392, 396, 402
91, 362, 393, 405, 464 Spelaeogriphus, 105, 108, 117
Serrate, 81, 141, 167, 171, 173–176, 180, 184–187, 191, Speleonectes, 23, 187, 205, 214, 314, 425, 430
238, 247, 311, 340–342, 349, 351, 366 Sperm, 16, 66, 106, 301, 337, 338, 356–362, 364–366,
Sertoli-like cells, 413, 417, 431, 440 368, 369, 413–415, 417, 422, 425–441
Seta competition, 413, 414, 427, 438–440
articulated, 171, 456 maturation, 413, 433, 441
classification, 174–176 nutrition, 429
cuspidate, 173, 176, 185, 186, 189 plug, 362, 433
development, 95, 96, 177, 178 priority, 427
evolution, 171, 172, 175, 187, 188, 191 viability, 427, 437, 439
formation, 177–179 Spermatheca, 356–358, 360, 361, 365, 366, 425, 429,
fossilized, 187, 188 437
gustatory, 186, 189, 190, 212, 456 Spermatogenesis, 414, 415, 429–431, 440
insect, 95, 189, 190 Spermatophore, 106, 301, 337, 356, 357, 361, 364–366,
multidenticulate, 340, 342, 343, 345, 349, 354 414, 415, 417, 425–429, 431, 433, 435–441
olfactory, 177, 179, 189, 190, 212, 228, 337, 338, 355, Spermatozoa, 413, 414, 417, 425, 427–439
454, 455 Sphaeroma, 358, 418, 427, 432, 438, 439
serrate, 167, 171, 173–176, 180, 184–187, 191, 238, Spherulites, 146
247, 311, 340–342, 349, 351 Spider crab, 261, 264, 268, 269, 272, 273
simple, 173, 175, 176, 182, 186, 188, 191 Spinacopa, 364
spider, 190, 191 Spine, 10, 34, 42–45, 49, 50, 53, 58, 59, 60, 62, 107, 167,
swimming, 34, 57 168, 170–172, 188, 189, 208, 227, 239, 249, 251,
Setobranch, 340, 342–347 271, 329, 333, 338, 355, 362, 365
Setule, 38, 60, 61, 167–180, 184, 186–191, 243, 244, Spinicaudata, 3, 9, 19, 20, 28, 104, 106, 118, 121, 122,
252, 299, 311, 319, 320, 322, 323, 339, 340, 342, 201, 214, 220, 362, 367, 393
345 Spongiocaris, 262
Sex determination, 414 Spring, 261, 268, 272, 310
Sexual differentiation, 414 Squilla, 23, 63, 105, 129, 332, 379, 452, 457
Sexual dimorphism, 208, 213, 223, 225, 300, 301, 365, Stacking angles, 143, 331
459, 467 Stance, 266, 270
Sexual maturity, 199 Statocyst, 218, 219, 456, 459, 475
Sexual tube, 357, 361, 430, 433 Statolith, 218, 219, 456
Shankouia, 41, 42 Stemonopa, 286
Sheath cell, 169, 171, 177–183, 189, 190, 209, 214, 217 Stenopodidea, 4, 228, 250, 342, 343, 349, 351, 361,
Sheep crab, 148, 153 425, 437, 459, 465
Shore crab, 254 Stenopus, 342, 459
Sicyonia, 360 Sternum, 49, 51, 357, 360, 426
Sinelobus, 397, 402 Stimulus transduction, 182, 183, 217, 218, 331, 332
Sinking, 220, 299, 305–307, 332 Stomach, 248–251, 254, 353, 385, 386, 389, 461
Sinus, 108, 113, 114, 376–378, 383, 384, 389, 390, 397, Stomatogastric nervous system, 461, 471
398, 401, 403–406, 470, 471 Stomatopoda, 3, 5, 62–66, 68, 105, 107, 110, 127–129,
Sinus gland, 470, 471 205, 210, 213, 215, 226, 251, 278, 280, 282, 285,
Skara, 9, 11, 16, 17, 28, 38, 41, 47, 66, 103, 132, 133, 187 287, 332, 337, 340, 346, 347, 352, 353, 361, 368,
Skeleton, endophragmal, 283 378–380, 384, 387, 388, 392, 393, 394, 398, 403,
Snow crab, 439 416, 425, 451, 452, 454, 457–462
Sodium-calcium exchanger, 158 Stomodeum, 473
Somata, 216, 452, 455, 460–462, 464, 465, 467, 468, Stone crab, 153
470, 472, 473 Strain rate, 311
Somatic cell, 414, 420, 421 Streamlining, 104, 106, 109, 110, 269, 304–309, 310,
Somite, 6–9, 11, 16, 19, 22, 24, 25, 26, 108, 117, 120, 127, 315, 319, 320, 324, 326, 327, 329–333
130, 200, 240, 255, 300, 303, 354, 362, 366, 415 Streblocerus, 118, 119
Index 499
Streptocephalus, 363 Thixotropy, 277

Stride length, 266, 267 Thoracica, 3, 365, 389
Stride period, 266 Thorax, 6, 8, 11–13, 19, 22, 24, 25, 27, 35, 50, 52, 56, 58,
Stridulation, 227 61, 65, 66, 86, 87, 104, 107, 108, 116, 125–130, 145,
Stygiomysida, 3 202, 238, 264, 265, 270, 280, 288, 299, 303, 308,
Stylocheiron, 297 310, 321, 332, 344, 351, 358, 360, 361, 380, 388,
Suspension feeding, 60, 188, 226, 241, 243–245, 355 404, 456, 462
Sustentacular cell, 431 Thrust, 220, 221, 266, 267, 288, 296, 298, 299,
Swarming, 304 303–305, 308, 309, 312, 323, 324, 329–332, 357
Swimmeret system, 320, 325, 351, 387, 467, 468 Thymops, 426
Swimming, 10, 11, 14, 18, 22, 26, 34, 35, 42, 43, 45, 57, Tigriopus, 255, 356
62, 64–66, 106, 107–115, 118, 119, 132, 184, 187, Titanethes, 182
199, 210, 213, 220, 226, 227, 243, 247, 266, 283, Tonofibers, 144, 146
287, 296–315, 319–334, 337–339, 351, 354–356, Trajectories, 296, 298, 305–307
361, 364–366, 387, 406, 467, 468 Transduction, 167, 179, 181–183, 190, 192, 217, 218
Swing, 43, 48, 220, 240, 266, 270, 321, 365 Transduction, mechano-, 218
Symphyla, 6 Transport filament, 153
Synapomorphy, 8, 124 Trichobothria, 190, 191
Synapse, 452, 453, 465, 466 Trichobranchiae, 400
Synapsis, chemical, 452, 465, 466 Trilobite, 11, 14, 15, 26, 37, 45, 50, 68, 188, 200
Synapsis, electrical, 452, 453, 465, 466 Triops, 14, 53, 78, 82, 83, 84, 87, 88, 104, 121–124, 131,
Syncarida, 3, 23, 203, 204, 210, 251, 322, 357, 417 314, 421
Synchrotron Bragg diffraction, 144, 145 Tritocerebrum, 451, 456, 457, 459, 473, 474
Syncytium, 95 Trunk appendage, 8, 12, 14, 49, 51, 58, 65–67, 355,
Systole, 383, 384 362, 367, 392
Tubule, 106, 144, 146, 150, 152, 180–183, 216–218, 248,
Tactile receptor, 456 251, 253–255, 381, 382, 419, 429–431, 440
Tagmatization, 65, 67, 262 longitudinal, 381, 382
Tagmosis, 11, 12, 46, 320 transverse, 382
Tail Fan, 63, 66, 161, 220, 284, 287, 319, 320, 330, 331, Turbulence, 22, 306, 307
332, 456, 464, 467 Tylos, 277, 281, 288
Tail-flip, 110, 111, 220, 221, 280, 284, 330–332, 465 Typhlatya, 215
Tanaidacea, 3, 62, 108, 115, 116, 117, 204, 323, 357, 379, Typhlocirolana, 209, 210
380, 382, 385, 387, 390, 397, 402, 404, 437, 438
Tanais, 108, 116, 117, 379, 390 Ultrabithorax, 19, 240
Tantulocarida, 3, 10, 24, 28, 58, 202, 208, 248, 366 Uniramous, 11, 14, 35, 43, 46, 57, 64, 65, 82, 84–88, 91,
Telson, 66, 145, 220, 284, 320, 321, 326, 330, 331, 356, 475 209, 210, 320
Temora, 243, 301, 303, 304, 306, 308, 314 Upogebia, 288
Tendon cells, 152 Urcrustacean, 130
Terminal pore, 170, 174, 176, 179, 180, 189, 216, 218 Uropod, 63, 64, 154, 220, 276, 280, 284, 287, 288, 320,
Testes, 245, 286, 364, 413, 417, 429–432, 434, 321, 326, 327, 330, 331, 354, 467
437–440 Urosome, 300–302, 308–312, 364, 365, 427
Testicular lobe, 429, 430
Tethysbaena, 332 Vargula, 113, 247, 340, 353, 355, 374, 402, 403, 418,
Thalassinidea, 184, 245, 256, 281, 282, 284–286, 288, 462
342, 343, 347, 349, 350, 351, 361 Vas deferens, 429, 430, 433–436, 439
Thecostraca, 2, 3, 24, 25, 28, 106, 118, 119, 131, 132, Velocimetry, 298, 310
202, 203, 210, 417 Ventilation, 108, 114, 115, 116, 117, 276, 278, 284, 285,
Thelycum, 359–361, 425, 436 376, 391, 393–397, 401–403
Thermoreceptor, 183, 190 Ventilatory epipod, 108, 117
Thermosbaena, 108, 116, 119, 120 Ventral nerve cord, 114, 385, 388, 451, 452, 456, 462,
Thermosbaenacea, 4, 108, 110, 115–120, 127, 210, 332, 463, 465–474
380, 386, 387, 397 Ventral vessel, 384, 387, 388, 390
500 Index
Vertical fibers, 144, 146, 147, 159 385, 415, 424, 425, 427, 429, 430, 462–464,
Vesicle 467–469
seminal, 364, 429, 433, 439 Walossekia, 11, 55, 57, 58, 103, 133
synaptic, 452 Waptia, 9, 21, 22, 38
Vestrogothia, 54 Wouters organ, 216
Victrola mousetrap, 312
Videography, 303 Xiphopenaeus, 426, 431, 436
Viscosity, 241, 243, 296, 298, 299, 307, 313 Xiphosura, 35, 368
Vision, 453–455, 472, 474, 475 X-Organ-Sinus gland complex, 470, 471
Vitelline envelope, 422–424 X-ray diffraction, 144
Vitellogenesis, 391, 414, 420–424, 440, 470
Vorticity, 311, 312 Yicaris, 39, 49, 50, 52, 55–60, 103, 132, 133
Wake, 296, 298, 305, 307, 310–313, 315 Zenker’s organ, 433, 439
Walking, 7, 11, 35, 36, 41, 50, 62, 64, 77, 85, 87, Zilchiopsis, 431, 434
106, 109, 110, 148, 192, 220, 261–273, Zoea, 14, 57, 78, 128–130, 206, 207, 211, 212, 297
282–284, 314, 320, 324, 349, 351, 355, 365, Zygopa, 286

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Functional Morphology

Functional Morphology and Diversity. Les Watling and Martin Thiel.

Editor ia l A dvisory Boar d:

Functional Morphology and Diversity (Volume 1)

EDITED BY LES WATLING AND MARTIN THIEL

Oxford New York

Published in the United States of America by

© Oxford University Press 2013

All rights reserved. No part of this publication may be reproduced, stored in a

You must not circulate this work in any other form

Library of Congress Cataloging-in-Publication Data

Functional Morphology and Diversity

Jim Belanger Zen Faulkes

Anders Garm Andreas Maas

Laura S. Lopez Greco Frederick R. Schram

Thomas Shafer Terri A . Williams

1. Comments on Crustacean Biodiversity and Disparity of Body Plans • 1

2. Evolution of Crustacean Appendages • 34

3. Mechanisms of Limb Patterning in Crustaceans • 74

4. The Crustacean Carapace: Morphology, Function, Development, and Phylogenetic

5. The Crustacean Integument: Structure and Function • 140

6 . The Crustacean Integument: Setae, Setules, and Other Ornamentation • 167

7. Antennules and Antennae in the Crustacea • 199

8. Feeding and Digestive System • 237

9. Appendage Diversity and Modes of Locomotion: Walking • 261

10. Morphological Adaptations for Digging and Burrowing • 276

11. Appendage Diversity and Modes of Locomotion: Swimming at Intermediate Reynolds

13. Adaptive Modification of Appendages for Grooming (Cleaning, Antifouling) and

14. Circulatory System and Respiration • 376

15. Functional Anatomy of the Reproductive System • 413

Table 1.1. Various estimates of global numbers of species of crustaceans.

Estimated number of species Source

Table 1.2. Census of species numbers in various crustacean groups.

Taxon Number of species

Table 1.2. (Continued)

Taxon Number of species

CRUSTACEAN DISPARIT Y OF BODY PLANS

CAN WE DIAGNOSE A MONOPHYLETIC CRUSTACEA?

“Body consisting of three regions: head, thorax, and ‘abdomen’”

“Trunk appendages primitively multiramous”

lap pb z2 zen Dfd Scr ftz Antp Ubx abd-A abd-B

“Development consisting of a series of discrete larval and/or juvenile stages,

WHAT ARE THE CRUSTACEOMORPH BODY PLANS THAT MIGHT

Short-Bodied Forms (Oligo-Crustacea)

Rehbachiella (Fig. 1.8B) has figured prominently in discussions of branchiopod origins

maxilliped-bearing segment as a modified trunk somite (even though it is completely merged

WHAT MIGHT THE CRUSTACEOMORPH ANCESTOR HAVE LOOKED LIKE?

Table 1.4. A classification of tetraconate arthropods with inclusion of fossil plesions.

Subphylum: Tetraconata (= Crustaceomorpha = Pancrustacea)

Joachim T. Haug, Andreas Maas, Carolin Haug,

HOW DID THE CRUSTACEAN APPENDAGES EVOLVE?

THE “ORSTEN” PERSPECTIVE

Sources for Fossilized Appendages

Table 2.1 Phylogenetic system of Arthropoda.

basipod endopod exopod proximal endite / coxa

The Basis, 2: Appendages at the Level of Euarthropoda

Appendages at the Level of Crustacea sensu lato

1. Antennulae uniramous, composed of a few tubular portions or articles, though large,

However, the most apparent new feature of Crustacea s. l. is the following:

Appendages at the Level of Labrophora

Appendages of the Eucrustacea

• First postmandibular limb is dissimilar in morphology to the preceding and succeeding

Different Evolution of Limb Morphologies in Entomostraca and Malacostraca