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 1 Preface
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Published in Australia. New Zealand. South East Asia. CWTER 1 'WHATGOOD ARE MITES?
Papua New Guinea and Oceania by W h y s t u d y mires?
University o f New South Wales Press Ltd
University o f New South Wales W h a t is a mite?
Sydney 2052 Australia W h a t follows?
www.unswpms.com.au

and in the rest of the world by CHAPTER 2 THE ORIGIN OF MITES: FOSSIL HISTORY AND
CABI Publishing RELATIONSHIPS
CAB International
Wallingford, Oxon OX10 8DE. UK The C a m b r i a n explosion a n d t h e rise o f t h e Cheliceraca
Tel+44 (0) 1491 8321 1 1 Fax +44 (0) 1491 833508 T h e marine merostomes
Email-axbi-nao@cabi.org>
The o r i g i n of the a r a c h n i d s - a p a l a e o f a n r a ~ ~
0 D.E. Walter and H.C. Proctor A r a c h n i d s a n d t h e colonisation of l a n d
First published 1999
Transferred to print on demand 2004 Fossil mites
A r a c h n i d relatives of mires
T h i s book is copyright. Apart from any fair dealing for the purpose
of private study, mearch. criticism o r review. as permitted under the Summary
Copyright Act, no part may be reproduced by any process without
written permission. Inquiries should be addrcsxd to the publisher.
CHAPTER 3 !XSTEMATIC AND MORPHOLOGICAL SURVEY
National Library of Australia Opilioacariforrncs - t h e missing link?
Cataloguing-in-Publication entry:
Parasitiformes - ricks a n d t h e i r relatives
Walter, David Evans 1950-. Acariformes - t h e mite-like m i t e s
Mites: ecology, evolution, and behaviour.
H o w do m i t e s do t h e t h i n g s t h e y do?
Bibliography. Summary
Includes index.
ISBN 0 86840 529 9 (UNSW Press)
ISBN 0 85199 375 3 (CABI) CHAPTER 4 LIFE CYCLES,DEVELOPMENT AND SIZE
Oviposition
1. Plant mites - Ecology. 2. Plant mites - Behavior - Evolution.
3. Water mites - Ecology. 4. Water mites - Behavior - Evolution. Posrcmbryonic d w c l o p m e n c
-
5. Mites. 6. Mites Evolution. 7. Mites - Ecology. Size, d e v e l o p m e n t a l rate and generation rimes
8. Mites - Behavior. I. Proctor, Heather Coreen, 1964-. 11. Title.
Dispersal, m i g r a t i o n a n d phoresy
A catalogue ruord for this book is available from the British Library. Summary
A catalogue record for this book is available from the Library of Congress,
washingon. DC, USA.

595.42

Printed and bound in the UK by Antony Rowe Limited, Eastbourne.

CHAPTER 5 SEX AND CELIBACY 57 CHAPTER 8 MITES ON PLANTS
Modes of sperm transfer 58 1
Mites on plants - where do they come from?
Diversity of sperm-transfer behaviours in mites 61 Plant parasites
Spermatophore strumre and funcuon 73 Hunting on leaves
Sexual selection 75 Mites and leaf domatia
Parthenogenesis 86 Phylloplane scavengers and fungivores
Summary Mites and biological control
92 ,
Summary
CHAPTER G MITES IN DETRITUS A N D SOIL S Y s T E M S
Mites and the rhizosphere CHAPTER 9 ANIMALS AS HABITATS
Deep soil Types of ecological interactions
Mites and decomposition Evolutionary pathways bemeen interactions
Soil mites in a simple system: Antarctica Life with inverrebrates
Feeding guilds and funnional groups Life with vertebrates
Predation in the soil Effcts of parasiac mites on their hosts
Avoiding predation -defences of mites and mite prey Mite-host cowolution: any evidence?
Acarophagy - mites as food for larger animals Summary
The enigma of soil biodiversity
Sensitivity and diversity - soil mites as environmental CHAPTER 10 MITES AND BIOLOGICAL DIVERSITY
indicators Mites and microhabitats
Summary Mites and complementarity
Size and biodiversity
CHAPTER 7 A W W UNDEHWATER, OR, WHY DID MITES I Host specificity, size and diversity
TAKE THE PLUNGE.' 132 I
Summary
Taxonomic distribution of secondarily aquatic arthropods 133
CHAPTER 11 MITES AS MODELS
Repeated invasions of water 134
Theoretical and applied population ecology
Number of invasions into different aquatic habitats 137
The evolution of host specificiry and virulence
(Pre)adaptations to subaquatic life 141 I
Sexual selection and diversification
Predation on water mites - the correlation between foul taste
,. The devolution of sex
and bright colour 155 I Pushing the limits of physiology and morphology
Locomotion 160 I
Selection at more than one level
Sensicivity and diversity -water mites as environmental Summary
indicators 164 Appendix
Summary 168 , Rdirences

T he average mite is minuscule, barely perceptible to even the sharpest eyes.
When enough are present, however, mites can exerc effects disproportion-
ate to their size. When a crop disappears under a blanket of silk or stored
food turns into a seething mass of hairy motes, then the numbers of mites will be
legion. If the mite is an itch mite burrowing in one's skin or a tick injecting viru-
lent rickettsia into one's blood, then 'enough' can be a single mite. Because of their
economic importance, we will always need to understand mites but the study of
mites - 'acnrology' - is a disappearing science.
Some ahan' were known to the more perceptive of ancient Greeks (Kevan
1985) and some of their effects were understood early on (for example, the cause
of scabics has been known since 1689) but few mites caused comment until the
late 1700s (Prasad 1982). Fewer than 100 species of 'ticks', stored-product pests
and brightly wloured plant and water mites had been discussed in the literature
before Linnaeus (Baker & Whmon 1952), and he included only 29 species of
Acarus in the 10th Edition of his Systma Naturae. Not until the late 1800s was the
term 'acarologist' coined to describe those who study mites and it was another 50
years before the word appeared in dictionaries (Krana 1997).
Advances in microscopy contributed to the birth of this new science but even
more important was the industry and imagination of acarologists G. Canestrini,
A D . Michael, A Nalepa, E. Trouessart and, in particular, Antonio Berlese in the
late 1800s. It is largely through Berlese's work that scientists first began to appre-
ciate the ubiquity and diversity of the Acari -and how intricately they are linked
to every aspect of terresuial life.
Acarology prospered during its first century, nurtured by the excitement of
discovery and by medical, veterinary and agricultural needs. In the last few
decades, however, like other important disciplines that require an understanding
of whole organisms (such as entomology and nematology), acarology has been
eclipsed by molecular mania. As a result, no marrer how well versed they may be
in cellular biology and genetics, many of today's students are not trained to deal
with living organisms or the problems those organisms can cause. As retirement
and death thin the ranks of acarologists, there are few new students who know
what a mite is, let alone understand them enough to work as acarologiscs.
Our goal in writing this book is to attract new students to acarology by show-
ing them that mica do interesting and excicing things. We highlight the roles that
mites have played in the development of imporrant theoretical concepts in ewlo-
gy and evolution (e.g. local mate competition, prey refugia, multi-level selection
and tritrophic level interactions) and also emphasise that, as Dana Wrensch has
said, 'mites do things they shouldn't'. In many cases, the lives of mites dearly
demonstrate that currently accepted theory is flawed. We also reveal the depth and
breadth to which mites have permeated che world - from sequoias to seamounts
to sea lions - but most of all, we strive to transmit the wonder and afTection that
we feel for these most miniature of arthropods, with the hope that our acarophil-
ia will infea.others.
Quite a few biologists with at least mild cases of this disease have conuibuted
valuable suggestions after reading draFtr of chapters, when reviewing earlier works
or during discussions (semi-sober and otherwise). We think it safe to say that none
of these friends and colleagues would agree with everything we say in this book but
all have contributed to its more lucid and informative sections. We would espe-
cially like to thank Valerie Behan-Pelletier, John Clarke, Matt Colloff, Rob
Colwell, John Cooke, Doug Craig, Jason Dunlop, Norm Fashing, Diana
Freckman. Gordon Gordh, Bruce Halliday, Mark Harvey, Mark Judson. Jim
Kierans, Hans Klompen, Jerry Krana, Evert Lindquist, Rogelio Macias-Ord6fiez,
Jim McMurtry, Roy Norton, Barry OConnor, Norm Platnick, Frank Radovsky,
Susanne Randolf, Owen Seeman, Matthew Shaw, Bruce Smith and Ian Smith. We
would also like to thank Michael Caldwell for allowing us to use his striking draw-
ing of a rampant eurypterid and our students Catherine Bryant and Juanita Ch o
for their help with many of the line drawings. Anthony O'Toole and Car me
41
Meacham contributed considerably to our meager skills at the scanning e ctron
microscope. We would also like to thank Louise Egerton for her editorial Input.
Additionally, our knowledge and appreciation of mites has grovb;l in d i m
proportion to our ability to study these fascinating animals. We have Funded some
of our studies out-of-pocket but that largess has never been sufficient to tackle
more than interesting sidelines. Fortunately, mites are major components of all ter-
resuial ecosystems and there are few research projects that cannot be used to learn
something exciting about mites. The senior author is especially appreciative of the
support he received from the National Science Foundation (Graduate Research
Scholarship and Postdoctoral Fellowship), the USDA Agr'rcultural Raearch
Service (Postdoctoral Fellowship), the Australian Research Council (Postdocrod
Fellowship, Large and Small Grant Schemes), che Australian Biological Resources
Survey and the Deparrment of Entomology at the University of Queensland. The
junior author wishes to thank the Natural Sciences and Engineering Research
Council of Canada, the Department of Biology at Queen's University, the
Australian Research Council's Small Grant Scheme and the Australian School of
Environmend Studies at Griffirh University for their support.
 Man ir cerrulinly crrraz)c He rouki not make a mi&
be makcsgodr by thc doen
(M..E& Montaigu. 1580)
WHY STUDY MITES?
I
n a world simultaneously fasdnated by the wonders of biological diversity
and aghast at its accelerating destruction, it is typically mammals and birds
that are the icons of our loss. A case is sometimes made fbr saving a but-
terfly or fish, and fiophave recently leapt to our attention - canaries in
our environmentalcoal mine. Rainforests and their plants arc argued to be worth
praew-ng for their potential as pharmacological cornucopias but what of the
worms, slugs, bugs, maggots and mites that fixd on and are the bod fbr the rain-
forests' larger inhabitants?Can these s c d y seen symbionts be worth consider-
ation?
A vertebrocmtric view of a n i d diversity is randy questioned bw it cannot
toleratc dose scrutiny. Approximately40 000 species of vertebrates, half of them
fish, are alive today (Wheeler 1990). Compare this p a I q sum to the number of
-
named invertebrate species more than a million! Thus when m d simply
as species richness, invertebrates make up 95% of animal biodiversiy. Recent
estimates suggest that there may be as many as 30 million species of insects in
cropid rainforests alone. Inxcts are rhe most obvious of the idvertebrate p u p s
but other minute animals, some of which pass rhcir entirr lives on one insect, arc
also rich in undescribed taxa. Thii contrasts with vertebrates, where the discov-
ay of a new species is a rare thing indeed. For example, in the decade fiom 1978
to 1987 only 5 new speck of birds were described compand to more than 2300
beetles (Groombridge 1992).
One might expect that with so little known about invertebrates most biolo-
gists would be rushing to study them. This is not the case. Despite their over-
whelming numerical superiority, invertebrates are studied by disproportionately
fkv systematists. Consider the ratios of the number of named species of animals
to the number of taxonomisrs in the United States that study them. For fish and
b i , this ratio is about 30:1, while for mammals it is a low 7:l (Caculatcd from
Whecler 1990). For the group that is both most diverse and least described, the
invurcbrates, the ratio is a scagqxbg 307:l. The most divasc group within the
invertebrates, insects. has an even higher ratio of 42S:l.
Vertebrate bias is not limited to systematistx it is also pervasive among #ol-
ogists, ethologists and evolutionary biologists. We examined 15 recent issues of
three major journals - -
Erology. Animal &bavwur and EtrOfncion and classi-
fied artides according to the taxa they discussed. An accurate tctloccion of species
diversity would be a ratio of about one artide mentioning vertebrates to cvyr
24 that mentioned invertebrates. Ya, of the 1221 articles anmind 615
involved birds, fish, mammals, reptiles or amphibians, while only 410 included
invertebrates of any kind - a ratio of 1.5 vertebrate1 invextebrate.
Scienrific bias is not spread evenly among the invertebrates. Gaudy or med-
ically important groups like butterflies and mosquitoes are relatively well-stud-
i d , while many other equally worthy taxa have been given short shcift. In this
book we attempt to redress the balance for one particularly species-rich and bio-
loejcalty Fascinating group of invertebrates - the mitts.
The word 'mite', l i i the word 'spider' (meaning 'spinner'), comes to us from
Old English and means a very small creature. Compared to the spider, or even
the scorpion, the mite's contribution to idiomatic English is but a fraction
Bartlctc's FItnriliar Quotuthfu (1992) has 17 born mots about spiders and three
about scorpions but (except for the quotation above from the French) mvlagts
H d y one mention of a mite in English. Thii spot on the language is mirrord
in the more fbdk meaning of mite - a very small quantity. Thc 'widow's
mite' fiom I;br C o p 1 Acconiing to Saint Mark 1242 was actually borrowed in
transbcion from a Flemish coin wotth a third of a penny - a usage that cap-
rives the essence of being a mite. Above dl, mites are very small. Most arc less,
usually much less, than a millimeue in length, and none gmw larger than a fiw
centimetres long
Although not the equal of inseas, mites do rank high in species ridmess.
There are over 40 000 named species of Acari and, when estimates of unnamed
species am indudcd, this rises to anywhere beween half to one million species
(3arna 1989. Groombridge 1992). Thcre are only about 50 mite systematists in
the USA (data from Wclbourn 1992), that is one for every 800 described species!
As Lhe insect:cntomologist ratio is 4251, this suggests that on a per species basis,
mites arc lcss well known than insects. This is certainly true in Australia. where
fewer than 3000 mitc species have been described (Halliday 1998) - perhaps
3% of the total acarofium
B i o d i d t y does not simply r c f u to taxonomic diversity, it also indudes the
range of behaviours and Lif;estyIes exhibited by a taxon. Here again,mites a x very
poo;ly represented in ecological, cthologial and evolutionary studies: our survey
found that only nine of the 1221 artides mentioned acarines, and only five of
these had mice biology as their primary focus. This scientific neglect may be
partly the result of ignorance, for acarology is seldom taught in universities and
fkv modem tats discuss mite biology, but biologists would do well to pay atten-
tion to these little arachnids, as much of their behaviour and ecology puts vertc-
bate-based theory to the test. In this volume we present a n ovcrvicw of mitc
behaviour, evolution and ecology. We hope that readers will be both enlightened
by past restarch and stimulated ro pursue their own theorerid interests using
mites as models.
WHAT IS A MITE?
Although tiny themselves, mites belong to the largest and most impressive line-
age of aaimas,the arthropods. Within the Arthropods, mites are the most diverse
repracnabvcs of an ancient lineage, the Chdicczat~
The cheliceriut body plan is prohundly &&rent from that of other archto-
pods. Perhaps the most s d r h g difhcnce is that chclicaavs do not have a sepa-
rate head. Insread an anterior body region, the prosoma ('front body'),combines
the functions of sensing, fieding and locomotion. Antennae, the most character-
kdc sense organ of orher arthropods, also arc absent, as arc mandibles and max-
illae. Rather, in fiont of the oral opening are a pair of often pincer-like
MITES: ECOLOGY.EVOLUTION
A N D BEHAVIOUR
mouthparts, the chclicaac; behind the mouth are a pair of pedipalps, which can
be pincer-like or leg-lik, and b u r pairs of legs. Digestion, gamete production
occur in the posterior body region or opisth-ma
and gas exchange
('hid body');
Many cheliceratcs arc tamiliar inhabitants of homes, gardens and parks, and
most people know of spiders, spider mites, ticks, daddy longlegs and scorpions.
Others, including vinegarroons, sun-spiders, whip-scorpions and horseshoe crabs,
are often large and look menacing enough to cause comment and attract common
names. The remainder - most mites, pseudoxorpions, palpigrades and ricin-
uleids - scurry about in obscurity or havc I& traces only as bssils (cg. the
&a taxa Trigonorarbida, Kustara* M m r b i , Eurypcerida, Haptopoda).
Ludcing at the margins of the Chelicerata is a b i i marine group, the
~ ~ c n o ~ o nor
i dsea
a spidk. Although they seem to possess the basic &elicerate
characters -chelicerae rather than antennae and a body divided into a orosorna
and opisthosoma - their many unique features. such as a proboscis, a strongly
reduced opisthosorna and extraneous limbs, leave workers unco&rtable with
thcir placement in the Chcliemta (Annaud & Bambcr 1987).
The application of modem dadistic techniques to the problem of rheliemte
phylogeny is a recent phenomenon (Wheeler & Hayashi 1998, Beall &
Labandeira 1990, Shula 1990) and no sacisfictory hypothesis of relationships
currentlv exists. Tradiaonallv, termtrial chelicerate a~thromdshave been treated
as mun& of the Class A&hnida. Living arachnids ha;e been variously dassi-
ficd in 10-20 major groups (orders), many of which are easily rcwgnised For
example, the order Araneae indudes the spiders and the ordu Scorpionida, the
scorpions. However, mites arc so diverse in brm that in order to accommodate
them they require three orders: Opilioacariformts, Parasitiforma and
Acadfbrmes (Grandjtaa 1936. Kraau 1978, Lindquist 1984. Evans 1992). Since
thcse and other mite taxa usuallv lack common names, we will adom the con-
vention used fbr attributing country of origin, membership in an insect order.
etc., and refer to their members as acariformans, parasitihrmans and (slightly
conrracted) ooilioacaraas.
spid& &n be distinguished from other arachnids by several unique m c -
nrres: thcir fangs with poison glands, their opisthosomaI spinnerets that produce
silk, a narrow pedide and the bulbous male palps used in transkrring sperm.
Characterisiig mites, however, is much more difficult and requires an under-
standing of the basic morphology fbr each order (Chapter 3). In this book, we
condnue the tradition of treating the thrcc orders of mites as a s u b of the
Arachnids called the A d , or Im concisely, the Acarina
WHAT FOLLOWS?
Mites are ubiquitous in every sort of aquatic, tmesuial, arboreal and parasitic
habitat but, bdngamong the smallest of arthropods, m n those inhabiting well-
studied systems arc often owloaked Ignoring mites, however, is a mistake.
They arc not passive inhabitants of ecosystems; rather they are strong interactors,
important indicators of disturbance in both aquatic and terrestrial systems, and
major components of biological diversicy (Chapter 10). Most taxonomic effort
has been spent on the groups that directly a f f m humans, our crops and live-
WHATG O O D ARE MITES
stock, or on those mites that are associated with vertebrates. To mites, larger ani-
mals reprebent habimts and a single bird, beetle or butterfly may host a multi-
species community of a dozen or more mite species (Chapter 9). Even a single
feather from a b id may have three or four mite species living in strictly circum-
scribed microhabitats and exhibiting as many di&rcnt i n i ~ c t i o n swith their
host.
Plants, too, are mite habitats (Chapter 8). Plant-parasitic mites use stylet-like
mouthparts to stab individual plant cells and to suck out their contents, and some
species arc able ro modifL the growth of host tissues to provide rhemxlves with a
home In agricultural systuns, plant-parasitic mites are ammcly damagbg pests
with rapid generation times, high fecundity and a tendency to over-acploit their
hosrs. Fommatdy, acarine predators have followed their prey onto plants and
many arc important biological control agents. Collections from amber and fossil
leaf packs indicate that mites have l i d on vees at least since the Cretaceous.
Today,an incredible diversity and abundance of mites, inducting miuoherbivore-
demtivorcs, plant-parasites and pndaton, arc suspended on vegetation as they
scurry through the canopies of rainEonsp like an arboreal lankt ton, many even
drif&g on air currents from tree to trte.
The original home of mites was probably decaying vegetation and soil, and
that is where one s t i l l finds mites in their most dazzling diversity (Chapter 6). A
handful of fbrcst humus can literally contain mites from a hundred species, each
earning a living in a complex world that is u s d y beneath our notice but essen-
tia for our s u r v i d Mites are cnginars of soil strucrure, indicators of the health
of soil systems and major intuacrors with nematodes and miuobes in decompo-
sition. Any bit of decomposing matter, from a penguin corpse in the Antarctic to
a maggot-riddled mushroom in a tropical rainforest, is liktly to con& an uncr-
pccted diversity of mites.
Although we chink of mites as being quintessentially terrestrial, many acarine
lineages have suwessfully invaded aquatic habitats (Chapter 7). We arc not speak-
ing merely of the surfice-film dwellers or of the many species that dwell in the
ooze of rotting vegetation. Ratha, we speak of those mites chat have become uue
sub-aquacic denizens of streams, lakes and seas. Thw tiny arthropods may be
found in the chilly runoff of mdcing glaciers, or the steaming margins of hot
springs, in the shallow water trapped by plants or the still and frigid depths of the
occanic abyss.
In order to understand the complexity of their interactions with other organ-
isms, it is first nacrsary to know something about mites. Chapter 3 gives a brief
overview of the major kinds of mites, shows what they look lik,and provides an
i n d u c t i o n to their morphology, that is the structures mites use to interact with
their wodd Chapter 4 explores the limits to which mites have pushed their phys-
iology and size, and shows clearly that theory based on large vertebrates ofren tells
us little about life at a smaller scale. Chapter 5, Sex and Celibacy, continues this
thnne in lurid detail and demonstrates both that mites makc d e n t models fbr
invcscigathg evolutionary patterns in sexual selection and that sex is nor as essen-
tial as we like to think. The find chapter reviews what we chink is our most
important point - that mites arc aracllent organisms for comparative and
manipulative experimentation. But bebrt all this. we need to explor~the origins
of mites (Chapter 2) and that means starting with a bang.
M I T T : ECOLOGY,E V O L U T I O N
AND RIIIIAVIOUII WHAT GOOD ARE M1.1.~

Box 1.1
urionary relationships
dmc to watch spcriacion in progrcsc, we must
a n c a m r d c s c ~ n d a nreladonships.
r To con-
rrruct such phylogenetic hypotheses, systcmarisn coUccr lnformation ahour
morphology, bchaviour, DNA sequcnca and biochemistry of thc group
whose relationships they an: inrerested in untangling (the ingroup). Each
of scruam, bchaviour, ccc. is termed a character, and the m n i k a t i o n
of that charaaer tn a given Dxon 1s its state. For cxamplc, 'leg nurnbci is a
character and in arachnids thc usual adult .-re k 'eight'. Systemadsn a h cnl-
lect the same information for one or more taxa rhat arc related to the ingroup
hut chat have d+ fmm it at an earlicr time (the outgronps). For oram-
plc, to r c c o w c c rhe phylogeny of warer mites (Hydncxha), one would
use terresmal m i i s from the same cohort (Fansitengona) as outgmups
bewuse aquauc parasitengoncs are probably dsccndcd from terrestrial ones.
Afm cnllecdng as many character s a t m as posiblc, the systemadst cnmn
this information into a character scare matrix in which cach statc IS d c d as
a number. Tj.pically, rhe ouyronp sews arc ser ar '0' and arc mnridered to he
a n c n t a l stata.

Taron I n 111 IV V
o u q m u p sp. 0 0 0 0 0
Ingroup sp. A 1 0 0 0 0
Ingroup sp. B 1 1 0 0 0
Ingroup sp. C I 1 1 1 0
Ingoup sp.D 1 1 1 1 1

I Eys: 0 = prcscnt: I = ahscnt

11 Leg numbcr: 0 = eighr, 1 = six
111 Spcrm rransfcc 0 = bmadcasr spawning: 1 = spcrmarophore
W Food r).pc: 0 = particulate; 1 = Itquid
V MouApam: 0 = chclatc: 1 = rrylet-hkc
THE ORIGIN O F
MITES: FOSSIL ites are members of the arthropod subphylum Cheliceraca, a group
with a long fossil history. The earliest chelicerates are known from
HISTORY AND the late Cambrian, and appear to be close relatives of the trilobites
(Weygoldt & Paulus 1979, Wheeler et al. 1993, Weygoldt 1998), a
RELATIONSHIPS once diversc but now extinct group of arthropods. To undersrand the origin of
mites, we must peer back through the mists of time and seek answers to these basic
questions: What is an arthropod? Why arc the chelicerate arthropods different?
What does it mean to be an arachnid?

THE CAMBRIAN EXPLOSION AND THE RISE OF

THE CHELICERATA
The earliest evidence of complex mul- Figure 2.1
ticellular life appears in rocks formed An acarc~entricvlew of the history of He.
about 600 million years ago (mya) but
the first fossil records of something
Important Events
that could be ancestral to mites begin
more recently (Figure 2. I), during the
so-called 'Cambrian Explosion' about
530 to 550 mya (Gould 1989, Raff
1996). During the Cambrian, all
major phyla undenvent an explosive
diversification. Entombed at more
than 30 sites around the world are
entire communities of often bizarre
organisms, including the earliest crue
arthropods. Much paleontological
work has been devoted m these often
well-preserved fossil beds and as a
MASS EX7lNCTION -
EM) OF THE DINOSAURS
result we have a detailed and informa-
+fossil pnlpigrsdc
tive vision of the dawn of exoskeletal c dinosaurs dominatc land
life (see Briggs et aL 1994).
Recognising an arthropod today is MASS EXTMCTlON
quite easy (Figure 2.2). As well as being
equipped with a chitinous external
skeleton that is periodically shed dur-
ing development, arthropods exhibit
metamerism, that is they are com- cfossil pycnogonids. spidcn
-first eigonorsrbid
posed of serially repeated body seg- Slluriam
c m a r i n e worpiom
menu (or somites) with anterior (the Ordovician
acton) and posterior (the telson) non-
segmental caps. Many groups of ani- C8mbrLn

mals &bit metamerism, including

ourselves, but arrhropod segments are
unique in that each originally came
with a pair of appendages that were
also composed of segments (arthropod
means 'jointed foot').
 Each ancestral appendage had a basal piece that articulated with the body (the
coxa) and gave rise to two branches, each cornposed of a number of segments. The
inner branch of this biramous appendage usually formed a leg and is called the
walking or leg branch. The outer branch was modified for gas exchange (the gill
branch) and often for swimming. The inner faces of the come were opposed along
the ventral mid-line of the body and typically had spines and processes that
allowed them to act as grinding or filtering surfaces. In the 'dawn-arthropod', all
segments and pain of limbs were probably very similar in design but over evolu-
tionary time they havc been variously fused, suppressed or modified for special
3 functions.
When segments join together to form discrete units of an arrhroood's skeleton
they are called tagmata (singular,
ragma) and the pro- is called tag-
mosis. Cheliccrates are recognised by
having only two body tagmata (Figure
2.2): an anterior prosoma and a postc-
rior opisthosoma. The prosoma is not
a true head but rather it is a tagma
that combines the sensing and fecding
functions of a head with the locomo-
tory function of a thorax and is somc-
times referred to as a cephalothorar.
The prosoma consists of an acron,
which is assumed rather than clearly
demonstrated, and six segments, each
bearing a pair of uniramous limbs,
none of which arc antennae or
mandibles. The first pair of limbs, the
chelicerae, give their name to the Chelicerata and are the primary organs of fecd-
ing. Generally they are short (2-3 segments) and pincer-likc but they can be mod-
ified into fangs, stylets or slicing organs. T h e second pair of limbs, the pedipalps
or palps, arc usually sensory andlor fecding appendages, and may also be pinccr-
like. T h e third through to the sixth pair of limbs are usually walking legs. Antennae
are absent in the Chelicerata because the chcliceral and antennal segments are
homologous (Telford & Thomas 1998) and the ancestral chelicerate opted for
feeding ovcr sensing with this limb.
Body segment VII occurs at the juncture of the prosoma and the opisthosoma
and is usually strongly reduced or absent. In spiders, segment VII forms the pcdi-
cel, while in scorpions this segment and its appendages appcar fleetingly in the
embryo but arc absent in other stages (Hjelle 1990). The chclicerate opisthosoma
is composed of 10-13 segments and a tail-spine, with body segment VIII bearing
the genitalia. Like the abdomen of insects, the opisthosoma contains most of the
digestive, excretory, respiratory and reproductive organs. The limbs of the opistho-
somal segments are strongly reduced and have been variously modified for breath-
ing (book gills, book lungs) or for specialised functions (spinnerets, gcniral
papillae, pectines) or have been lost. An anus opens at the end of rhe opisthosoma
and may be followed by a telson-like region (e.g. the scorpion's sting or the whip-
scorpion's flagellum).
The earliest known animal that has becn attributed to the Chelicerata is
Sunccacaris uucara Briggs and Collins, a medium-sized (5-10 cm long) swimming
predator from the middle Cambrian (Briggs & Collins 1988). Sattctacaris had an
anterior region with six pairs of binmous limbs (the outer rami ofwhich arc antcn-
na-likc) and a posterior region with 1 1 segments (the first 10 of which bear bira-
mous appendages) ending in a flattened telson. Sarrctacarishad no antennae, as one
would expect in a chelicerate arthropod, but it also lacked chelicerac (Briggs &
Collins 1988). This is a problem, since chelicerate mouthparts are the defining
character of the Chelicerata. Although Sancrararis approaches a cheliccrate grade
of organisation, the mysterious Aglaspidida (Hesselbo 1992) and a number of the
enigmatic Burgess Shale arthropods (e.6 Sapmtoccm, Yohoia) appear to be more
dosely related to what we today consider the Chclicerata (Briggs & Forrey 1989,
Dunlop & Seldon 1997).
THE MARINE MEROSTOMES
Traditionally, the Chelicerata has becn subdivided into three major groupings: the
Xiphosurida (horseshoe crabs), the Eurypterida (marine scorpions) and the
Arachnida (terrestrial scorpions and arachnids). T h e first two groups, together
termed the Merostomata, are entirely marine and are almost entirely extinct; only
four species of horseshoe crabs are alive today. Some tantalising fossils from the
Cambrian (550 mya) may represent the beginnings of the Xiphosurida but the car-
liest confirmed horseshoe crabs are from about 400 mya during the Silurian pcri-
od (Ward 1992). Perhaps the most intriguing of the fossil horseshoe crabs is
Euproops dame, small animals, 2 cm long, from the Mazon Creek beds (300 mya)
that are commonly found in association with the fossils of terrestrial and freshwa-
ter animals and once on the trunk of a fossiliscd tree (Fisher 1979). Nthough mod-
ern horseshoe crabs are marine, there is no reason to dismiss the possibility that,
during the time of their greatest diversity and abundance, some xiphosurans
coloniscd the land.
The giant marine scorpions that sometimes grew to ovcr 2 m in length, the
Eurypterida (Figure 2.01, also have enigmatic beginnings and thrived in the occans
during the Ordovician, Silurian and Devonian periods (Bergstrom 1979). Many
species inhabited shallow aquatic environments and appcar to havc been adapted for
walking on land and possibly for gas exchange, both in water and in air (Manning
& Dunlop 1995). About two dozen Families of eurypterids are known and within
this diversity may lie the origin of the arachnids, including the group that has tradi-
donally been considered the earliest derivative Arachnida, the scorpions.
True scorpions have a subdivision of the opisthosoma that is unique in arach-
nids: the tail-like metasoma This consists of five ring-like segments that terminate
in the anus and is followed by a tail-spine modified into a sting with venom glands.
Although the memsoma is not present in other extant chclicerates, it is characteris-
tic of eurypterids (Dunlop 1997). One such is M*optrrus, which has been recon-
structed in a very scorpion-like pose that suggcsu that the tail-spine in t h e animals
may havc been used as a sting (Hanken & Stermcr 1975). Such striking shared
characters as the metasoma and sung cannot easily be explained away as primitive
or convergent morphologies and other characters support a scorpion-curypterid sis-
ter grouping (e.g. Dunlop 1998). However, not all agree. For example, van dcr
Hammen (1989) and Shule (1990) boch have proposed a dose relationship
- -
between harvestmen (Opiliones) and scorpions.
The first scorpions were marine and sccm to have made the transition to ter-
restrial existence later than other terrestrial chelicerates. Fossils of aauatic scomi-
ons arc known from the Lower Silurian (439 mya) and appear to havc persisted
well into the Carbonifkrous (362-290 my& and perhaps later (Kjellesvig-Waering
1986. Sissom 1990. Selden 1993). Recently discovered fragments from the lower
Devonian (390 mya) include lamellate structures that may represent scorpion
book lungs (Shear et rrL 1996). If so, then terrestrial scorpions may have colonised
land long behre their aquatic ancestors disappeared in either case, scorpions seem
to have invaded the land as relatively large predators after a Fairly complex terres-
trial ecosystem had evolved and othcr land animals were well established.
Modem terrestrial scorpions are a monophyletic group (see Box 1.1 in
Chapter 1 fbr a summary of relevant tums) and shared a common ancestor
among the aquatic scorpions (Sissom 1990). The major differences between
aquatic and t e r r e s d scorpions are largely due to adaptations to the terrestrial
environment. For example, book lungs replaced book gills, vichobothria evolved
to sense the movement of air currents and the lateral compound eyes of fossil
scorpions gave way to fivc or fewer separate ocelli, possibly because the chelicer-
ate compound eye required a film of water to function (Lcvi-Setti 1975). So, a
scenario in which a single species of scorpion became terresmal and h e n went on
to become the common ancestor of modem scorpions is not unreasonable.
Relating scorpions to othcr terrestrial chelicerates, however, is problematic,
since shared characters seem to bc primarily plesiomorphies or probable conver-
gent adaptations to the terratrial habitat ( S i o m 1990). None of the major char-
acters of scorpions, such as pectines, body tagrnata, embryonic development and
formation of the buccal region, are present in arachnids and it is diicult to imag-
ine a hypothetical ancestor of both (Snodgrass 1952, Weygoldt 1998). Therefore.
despite the textbook dogma that places scorpions at the base of the arachnids, the
idea that a monophyletic Arachnida was founded by some hopeful scorpion is
poorly supported (Kjelldg-Waering 1986. Polis 1990, Shula 1990). Of greater
relevance to our quest b r the ancestor of the MIis that neither modem nor
ancient scorpions have characters suggesting that they have a close relationship to
mites. So, we must search for an acarine origin among some lineage of other
eurypterids, xiphosurans with terrestrid indinations or perhaps evenmore enig-
matic cheliceratcs that lived in the Ordovician and Silurian (Bergstr6m 1979.
Dunlop 1998). A single, intrepid founder of the non-scorpion Arachnida would
be an inspiring way to smrt the story of the successful rise of the mites but is it a
reasonable hypothesis?
THE ORIGIN OF THE ARACHNIDS -
A PALAEOFANTASY
'Arachnid' is the name we give to terrestrial chelicerate animals and to their
descendana that have secondarily colonised fresh, salt or interstitial waters.
Traditionally, the Arachnida has been treated as a class of equal rank to the
Xiphosurida and Eurypterida. Although the Xiphosurida may bc monophylctic
and hence a natural taxon under the rules of phylogenetic systematics, neither
the Euryptcrida nor the Arachnida are clearly so. However, traditions die hard
and arachnologists havc the added burden that the original colonists of land may
haw been very small and lightly sderodsed, and therefore unlikely to form
prominent kssils, and that all of their close relatives have long been mtinm
Is being a terrestrial chelicerate a sufficient synapomorphy for the
Arachnida? By way of analogy, it is usem to consider the terrestrial crustaceans
that inhabit rainforests in Queensland, Auscrali. Isopods (Class h4alacostraca,
Ordcr Isopoda) are well known litter inhabitants throughout the world. In
Queensland, however, isopods are usually outnumbered by other crustaceans,
the calicrid amphipods (Class Malacostraca, Order Arnphipoda, Family
Talitridae), which are major processors of leaf litter (Friend & Richardson 1986).
including suspended humus many metres up in the rainforest canopy. Other
unexpected cruscaccans also inhabit the rainforest floor, ofcen in large numbers.
For someone used to the litter huna of the Northern ~cmis~here,-the sight of
hundreds of small, white, bivalved shells crawling across the floor of a live-
extraction vial is dis&ncerting. T h a e animals are ostracods (Class Ostracoda).
well known for the several thousand species that can be found in virtually any
aquatic habitat (McLaughlin 1980) but, in this case, adapted to life on land. Less
well adapted to terrestrial existence and by far the smallest of the rainforest crus-
taceans are the copepods (Class Copepoda). Although common in leaf litter,
these animais are not truly terrestrial and arc active only in films of water on leaf
liner, decaying fungi and other wet organic remains. In contrast are the largest
(15 cm long) and most vividly coloured of rainhrest crustaceans, the blue and
yellow crayfish or yabbics (Class Malacostraca. Order Decapoda, Family
Parastacidae, Genus Euas~cus).Although these animals are primarily stream
inhabitants, they often forage on land and can bc found well away from water
(Jones & Morgan 1994).
The terrestrial cruscaccan fiuna in Queensland has been derived from at least
fivc independent colonisations of land and probably by three independent
routes. Isopods and amphipods are believed to have colonised land direcdy
fiom the ocean via beach wrack (Labandeira & Beall 1990). Ostracods and
copepods probably started out in fresh water and then colonised land via soil
interstices (Gordon 8r Olson 1995), while yabbies are in the process of mov-
ing direcdy to Land fiom fresh water, perhaps much like scorpions did long
ago. Because all of these animals have living aquatic relatives and because the
Crustacea has a long and rich fossil history, no one is likely to suggest that cer-
restrial Crustacea represent a monophyletic taxon. Terrestrialisation is clearly a
grade of evolution that has been achieved a number of times (with varying
degrees of success) and it would be meaningless to erect a 'Class Geocruscacea'.
Why then d o we recognise a class called the Arachnida fbr what seems an even
more diverse array of terrestrial chelicerates?
Unlike crustaceans, chelicerates have neither a rich fossil history nor
many living marine relatives. The sparse array of known fossils may relate to
the basic mode of earning a living in the Chelicerata: eating other animals.
Behaviours often correlated with high population densities, such as scaveng-
ing, filter-feeding and detritus feeding, seem to be the dominant ways of
earning a living in the Cruscacea, but marine chelicerates were always prima-
rily predators and existed in relatively low numbers. Although comparatively
M l f ES: ECOLOGY,EVOLUTION
A N D BEHAVIOUR
few fossils of these marine predators have been found, they indude a &r
diversity of lineages that were alive when chelicerates first colonised land. For
example, at least 54 genera of Eurypterida (Tollerron 1989), 13 genera of
aquatic scorpions (Sissom 1990) and several enigmatic chelicerates
(Bergstrom 1979) arc known from the Ordovician through to the Lower
Devonian periods (ca 500-400 mya), when the colonisation of land by che-
licerates must have occurred (Gordon & Olson 1995). In the late Siwian
done, 70 species of eurypterids representing 28 genera are known (Plotnick
1996). Did one and only one of this @eat diversity of forms make the suc-
cessful transition to land?
Given the distinctive primitive character states that differentiatearachnids
fiom other terrestrial arthropods, such as chclicerae and prosoma with six pairs
of limbs, the lack of any informative data fiorn the fossil record and the few
surviving merostomes, it is little wonder chat many arachnologists tend to
cram d l terrestrial cheliccrarcs into a single lineage. Unfortunately, these
&m have not resulted in agreement that the Arachnids i s monophylctic, nor
have they established a likely sister group of the arachnids ( B e 4 8r Labandeira
1990. Selden 1993). Although most arachnologists would prefix a mono-
phyleuc Arachnids, none has made a convincing case that this is me.
ARACHNIDS AND THE COLONISATION OF
LAND
The Pridoli Epoch in the lace Silurian (414 rnya) provides our first dear records
of terrestrial animals, induding a tiny (1.3 mm long) arachnid in rhe order
Trigonitarbida &ram et aL 1990). Trigonotarbids are the earliest known pul-
monate arachnids and they had welldcveloped book lungs f$r breathing air
(Gordon & Olson 1935). Trigonotarbids show up spin in thc Devonian
Rhynie Chur of Scotland (ca 400 mya), the black shale of Alken der Mosel of
Germany (390 mya) and the black shales of Gilboa in New York (380 rnya),
where nine species are present (Shear & Kukalovd-Pedc 1990). Trigonotarbids
persisted into the late Carboniferous before disappearingfiom the fossil record,
not long after ricinuleid hssils began ro appear (Selden 1993). Ricinulcids havc
survived until today and are one of the arachnid groups that have been pro-
posed as dose relatives of the mites (see Lidquist 1984, Schultz 1990, Wheeler
& Hayashi 1998). However, Dunlop (1996) has rccendy proposed that ricin-
uleids-and trigonorarbids together 6rrn a sister group of &e &nonate arach-
nids and are only distantly related to the mites.
The early mgonorarbids appear to havc been quite small (1-14 mm long).
Lightly arrnoured and to have retained remnant compound eyes. Later speci-
mens were much iarger, up to 5 cm in length, heavily m o d and most had
lost all vestiges of the lateral eyes (Shear & Kukaod-Pedc 1990).This may rep-
resent an example of Cope's rule i.c new taxa tend to originate small reladw to
their potential size range (Stanley 1973). If so, then mites seem to flout this
rule, as they do so many others. Although the earliest known mites were,
indeed, very small (hall a millimecre or less in length), b r the most part they
havc stayed small or become even smaller. In fict, miniaturisation may havc
been the key to their invasion of land thiough beach sands and soil pores.
FOSSIL MITES
Mites are among the earliesc of the f$ssil arachnids and are known fPxn both the
Gifboa shahs and the Rhynie Chert (380-400 mya). At least 1 1 species of mites
are present at these cwo sires (Kethley ct aL 1989; Shear & Kukalovd-Peck 1990;
Bemini 1991). Four species of the early derivative oribatid mite taxon,
Enarchronora, are known from Gilboa (Norton ctaL 1988). The two species that
have been described, L k u o m s c h i c k i Norton and Roochkboniw &a
-
Norton, are both small, ranging fiom 323-512 in length. S-&ly, the
endaostigmacid mite, A*chaeacarus riubinini K d e y and Norton from Giboa, is
less than 400 p in length (Kethley ct aL 1989) and the Rhynie Chert endeostig-
matid, h * I M i r Him,is less than 500 p n long (Gordon & Olson 1995).
How does one distinguish fossil mites from other arachnids? Aside fiom
being g e d y tiny cheliceratc arthropods with an anterior body q i o n called
either the capitulum ('little head') or gnathosoma ('jaw body'), the absence of
dear opistho&naI segmcncation and a-kv distinctivevesau&, such as a rurcl-
lum (a shd-shaped sera on the gnathosorna of primitive mites), this question is
difficult to answu (seeChapter 3). Thm distina lineages of mites arc ret~gnisad:
the Acxrifbrmes. Opilioacariformes and Parasitifbmes (Grandjean 1936). All
-
share the eeneral characvristicsof mites but, as Lindauist (1984)- has ~ointedour,
many of &c chamaers used to define mites are aIso-pr&nt in other chelicerate
orders. For example, most spiders have lost all sign of opisthosomal segmentation,
while'ridnuleids have both a h 4 larva and a gnathosoma. O h ,it seems,
mites are most easily mx+sed by what they are not - o h dds.
Fossil Acari formes
About 80 species of fossil acarifbrm mites have been formally described, indud-
ing a few relatively recent spccies of predators and plant parasites fiom Tertiary
amber (Selden 1993). All of the Devonian fossil mites belong to the
Acarihrrnes, as do all of the Paleozoic and Mesozoic fossils, and most can bc
placed in families with living members. Most ancient mites, induding the earli-
est plant associates, belong to taw whose descendants today fkcd on fimgi, seav-
enge dcad plant matter and graze on green algae. Based on extensive fecal
remains, it appears that these d m mites were major components of the
deaitivore system in Paleozoic coal swamps (Labandcira ct rrL 1997), just as they
are in modern soil-litter systems.
Fossil Opilioacariformes
Fossil opilioacarans are unknown (Selden 1993), although DunIop (1995) has
raised the possibility that they may be related to a curious group of
Carboniferous fossil arachnids, the Phalangiotarbida. Modern'opilioacaransarc
rather large (2-3 mm long), active animals, widely considered ro be the most
primitive of living mites. Ancestral characters retained by opilioacarans indudc
retention of the full developmental sequence of the Acari (i-e. a prelarva, larva,
pmmnymph, deumnymph, tritonymph and adult), parciculace ficding, up to
rhrcc pairs of lateral eyes, remnants of opisthosomal segmentation and large
numbers of serae and lyriftsures. Today, opilioacarans arc bund in warrn-tem-
perate to tropical areas, especially in seasonally dry habitats.
MITES: ECOLOGY.E V O L U T I O N
AND BEMAVIOUR
Fossil Parasitiformes
No fossil parasitiform mites are known from the Paleozoic and even their recent
fossil history is poor. A tick. Ixodcs trrtiarius, is known from early Terriary amber,
while two other species - a phytoseiid mite, Sciu bdcbidez, and a digamasel-
lid mite, DendroCacLpsfissiIis- have been described from mid-Tertiary amber
(Selden 1993).
ARACHNID RELATIVES OF MITES
The possibiliry that mites have no close relatives among terrestrial chelicerates
has rarely been considered and arachnologists have tended to assume that mites
are (a) monophyletic and (b) relatively derived within the Arachnids. However,
acarologists are divided on the monophyly of mites, and belie& about mono-
phyly and diphyly of the Acari have influenced hypotheses about mites' closest
arachnid relatives (Evans 1992). At various times, pseudoscorpions and solfugids
have been thought to share some characters with the mites (see Figure 2.3) bur
more recent discussions of arachnid phylogeny have singled out three orders as
potential mite relatives: Palpigradi, Opiliones and Ricinulei. Morphology and
biology of the main contenders are discussed below.
Figure 2.3
Both pseudarcorpmns (right) and acariform mires (left) are known from Devonian fosslls
and were among the earlien tenemlal sdi anirnalrThese modem animals (the mite
betongs to the family Cheyletidae) coinhabk leaf liaer in an Australian rainforest
T H EO R I G I NO F MITES
Palpigradi
Palpigrades are minute, enigmatic arachnids with a rather generalised mor-
phology and numerous, seemingly ancestral, character states, e.g. chelicerae
three segmented, palps leg-like, book lungs absent, first pair of legs antenni-
form and telson (flagellum) present (Kaesrner 1968; Savory 1977; van der
Hammen 1989).They have ofren been considered the most primitive of arach-
nids (Cond.6 1996) &id some authors have suggested that-that they are not
completely terrestrial. For example, species of Leptokommia from littoral sand
are able to swim easily in sea water (Monniot 1966). However, this genus
appears to be recently derived and mosr palpigrades are clearly terrestrial. Also,
palpigrades have numerous well-developed trichobothria (sensory hairs that
function only in air). h k o m m i a whccIrri has paired invaginations on segments
X-XI1 (lung sacs) and a pair of papilla-like bumps (vetrucae) o n the underside
(venter) of segment IX These may be remnants of ancestral book lungs: mod-
ern palpigrades, like many acariform mites, are thought to respire cutaneously
(van der Hammen 1989).
Based on his concepts of the origin of feeding snuctures in Cheliceraca, van
der Hammen (1989) considered the Acari to be diphyletic and contended that
the two lineages are only distantly related. Van der Hammen's phylogeny can
be interprered as implying that at. least three independent colonisations of land
by arachnids occurred: by ancestral Opilionida, by Scorpionida and by an
ancestor of the rest of the arachnids. According to van der Harnmen, the
Acariformes and Palpigradi are sister groups that form the taxon Epimeraca.
However, the characters that he presents to support this taxon are a mixture of
plesiomorphies (e.g. tridactyl claws) and interpretations of development or
morphology that are not generally accepted. In fact, there seem to be few if any
basic character states that the Acariformes and Palpigradida share that are not
found in other arachnids.
One general point chat favours a palpigrade-mite relationship is that both
are small, soil-dwelling animals whose first terrestrial ancestors may have invad-
ed the land through soil interstices (CondC 1996). Both early derivative acari-
form mites and most palpigrades appear to rely on cutaneous gas exchange for
respiration. Adult acariform mites have three pairs of genital papillae that rep-
resent remnants of rhe limbs of three opisthosomal segments (Grandjean
1946). These papillae appear to be homologous in position and origin with
book lungs or book gills and spider spinnerets. Although genital papillae have
no respiratory flnction, they are used for osmoregulation (water uptake and
ion balance) (Evans 1992).
Generally, genital papillae are added sequenrially during postembryonic
ontogeny in acariform mites: larvae have no papillae, protonymphs have one
pair, deutonymphs two pairs and trironymphs usually have the full three pairs
(see Chapter 4). Van der Hammen (1989) has pointed our that the lung sacs in
Z? whcelrri appear to be similarly added in sequential moults. However, there is
good reason not to accept this similarity as a shared derived condition. The
trilobite larva of the horseshoe crab has only wo pairs of book gills. Additional
pairs of book gills are added sequentially with moults, until the adult a m p l e -
ment of five pairs is reached (Kaestner 1968). Presumably this sequential addi-
tion represents an ancestral chelicerate ontogeny. If the ancestor OF acariform
T
o work with mites, one must first understand their morphology and
classification. The major hurdle to mite identification, other than the need
for a good microscope, is the scattered nature of the literature. This
disarray includes both the variety of languages and locations of the rele-
vant papers and the babel of jargon used to describe mite morphology. Fortunately,
in recent years mite morpho-speak has become more homogeneous and several
excellent texts exist that provide clear and comprehensive discussions of mite mor-
phology (e.g. Kcantz 1978; Evans 1992). For those interested in learning to iden-
tify mites, we recommend the 'bible' of acarologists, Jerry Krantz's A Manual of
Acarology. A revised version of this text is in preparation. For those who speak
English and who wish to learn to become proficient in the identification of mites,
The Acarology Laboratory at The Ohio State University runs a series of short
courses in the Northern Hemisphere summer. The Acarology Summer Program
has been in existence for nearly 50 years and both authors learned much of what
they know about mite taxonomy there. A similar program in Europe, The
International Course in Acarology, has been running for more than a decade.
Major sources of information on mite biology and taxonomy are given in
Appendix 1 and anyone interested in acarology should begin searching the inrer-
net for some of the increasing amount of information available. This book is not
intended as an identification manual but anyone who works with mites needs to
know something about their taxonomy and morphology. In this chapter we briefly
review the major orders of mites and their Functional morphology.

OPILIOACARIFORMES
- THE MISSING LINK?
The Opilioacariformes (Figure 3.1). as
their name implies, resemble small opil-
ionids (harvestmen, daddy-long-legs)
and are widely thought to be the most
primitive of living mites. To date fewer
than 20 species have been discovered
and all nine described genera have been
placed in a single order (Opilioacarida)
and Family (Opilioacaridae). Most opil-
ioacarans have been found under rocks
in Mediterranean, monsoonal or other
seasonally dry climates in Europe,
Africa, Asia and Australia, but some are
known from rainforest litter in Central
America. Figure 3.1
Opilioa- adults are usually 2-3 Dorsal view of an @liicarifonn mire.
mm in length with purple-striped, L
brownish grey bodies and long legs banded with white. The cuticle is leathery
and lacks the sclerotised plates that are found in most other groups of mites. Two
or three pairs of lateral eyes are present but median eyes are not. No cri-
chobothria are present on the prodorsum or other locations on the body; how-
ever, femoral trichobothria have been reported for one species. These structures
MITES: ECOLOGY. E V O L U T I O N AND BEHAVIOUR

may be homologous with the rrichobothria of other arachnids or may be con-
vergcndy derived (as in some Mesortigmata). T h e opisthosoma has four pain of
antero-lateral tracheal openings -a unique condition in arachnids. The almost
dorsal placement of the spiracles is rcfleaed in another name somctima used for
this group: Notostigmaa
Opilioacarans feed on pollen, fungi and small arthropods. Large, &re-scg-
mcnted cheliceae are used to grasp food and large, scrrared rutella (hyperrro-
phicd sctac on either side of the buccal opening) saw it off into bitc-sized
chunks. Ingated food forms boluses in the g u of ~ the mites. Neacom t - n u
from Big Bend National Park in Texas lay one large egg at a rime bur the repro-
ductive biology of these animals is otherwise unknown.
, completely cncascd in armour but the larva and three nymphal stages are
I : .. . . .6. &... .&. . 3. .3 . , : , : : - '
possibly homologous to the c o d apophyses in Opilioncs.
A crucial aspea of the biology of opilioacarans that is still unknown is how
they transfer sperm. If the males produce a stalkless sperm sac that thcy transfer
to the female genital opening with their chclicerae, then opilioacariformans may
be closely rclared to the Parasitiformes. If they produce a stalked spcrmatophore
that is placed on the subsrratc, then this would suggest a closer rclationship to
the Acariformes (see Chapter 5).
PARASITIFORMES
- TICKS AND THEIR RELATIVES
T h e origin of the name Parasitiformcs is casy to understand -many species are
imporrant pararites of vertebrates. The three suborders of parasitiformans arc:
Mesostigmata, Holothyrida and I r o d i d a Ixodids are ticks perhaps the -
most familiar of all mites because of their large size and bloodthirsty habits.
Three (sometimes five) families of ticks are currcndy rccognised and about 850
species have bcen described All are vcztebrate haematophages. Thcy have spe-
cialised cheliccrac modified for curcing into the skin of vertebra- and a well-
developed anterior hypostomal process that is covered in teeth that helps them
anchor their mouthpam during feeding. A rritosternum is not present. Males
usc their chelicerac to transfer sperm in a sac-like spcrmatopbore directly to the
female's genital opening (sce Chapter 5). Sonenshine (1991) provides an ucel-
lent modern revicw of tick morphology and biology.
The Holochyrida also contains thrcc families but fewer than 30 described
species. Adult holothyrans are l q c (2-7 mm long), reddish to purplish mites
~

. ' . ".
"
. . . . .. . .. . . ...>... . . . . . . .. . . 6
1 . . Fovr.merbrrigm&s fmm nirdoreniktkln ~"ecnrland: a rn&b&&e (a)
SeiinrUrnpodim lineage (HEmhmXam1hmh.s).@) an vndesuibed p n u s o f . . . . .
. "', :
. . . . . . . . .
.
',..'
.
.
,

.
.
f
, .
. C-ornegirrins and n*o Dennan@m (=) a laelapid (Hy@&r .p).. . . . . . . . ... . . . . .
8

\
,
.
. :.. a n d (d) a male d + m i d (EugMur rp.):
, .
. . . . .
. . . .. . . .. ., . ... . . .. , . ~. . . . ... ... ... .
. .:(

Opilioacarans look primitive to acarologisrs and they have a number of

morphological and behavioural charaacrs that may indicate relationships to
both Acariformes and Parasitiformes. Like early d e r i ~ t i v eamiform mites,
opilioacarans ingest solid foods and have welldevclopcd rutella. Howcver,
other characters suggest a closer relationship to parasitiform mites. These
include the loss ofthe median eyes, the retention of the basal chelicenl segment
and the lack of prodorsal trichobothria. Such losses and plesiomomhics are not
strong inferen& but the presence of a rritosternum L usually Ansidered a
-. .
strone a~omorvhv. , Unfomnatelv. ,. a rritosternum fliterallv.
,. the sternum of the
third segment) is present in most arachnids. Usually it is platc-lie and is some-
times called the labium (Figure 3.2). The rritostcrnum oficn has scral proms-
er that extend under the palpcoxa (Figure 3.2b. c) bur in opilioamans the
rritosternum consists of two. separate finger-like p r o m s (Figure 3.2d) and is
 MITES:
ECOLOGY, E V O L U T I O NAND B E H A V I O U R

soft-bodied. As in ticks, a maximum of one pair of lateal eyes is present on the
idiosoma. Holothyrans are rare, poorly studied mites, known only from
Australia and New Zealand (Allothyridae), the Neotropics (Neothyridae) and
islands in the Indian and Pacific Oceans (Holothyridae). Allothyrids scavenge on
dead arthropods and, like ticks, feed only on fluids - haemolymph and exter-
nally digested tissues (Walter & Proctor 1998a). Species ofAllothymhave a pair
of elongate, seta-like tritosternal laciniae originating from a common base.
Sperm transfer is thought to be similar to that in ti&.
The Mesostigmata (Figure 3.3) is the most diverse and broadly distributed
i suborder of Parasitiformes with about 70 families divided into 12 lineages.
About 10 000 species have been described, of which half are free-living preda-
tors in soil-litter, rotting wood, compost, herbivores' dung, carrion, nests, house
dust or similar detriw-based systems. These predators are usually abundant and
voracious enough to regulate the populations of other small invertebrates. No
swimming mesostigmatans are known but some species live in the intertidal
zone or the margins of freshwater streams and lakes and may spend a consider-
able time submerged (see Chapter 7).
A fav species of mesostigmatans, in several families, have switched from
predation to grazing on fungi and some species ingest fungal spores and hyphae.
Some feed on pollen (digesting the exine externally and ingesting only fluids),
nectar and other plant fluids. Pollen feeding is common in the Phytoseiidae, a
family that has successfully colonised the Ieaf-surkce habitat and accounts for
about 15% of described species of Mesostigmata. Phytoseiid mites are used with
great success as classical biological control agents and are the dominant family of
predatory mites on plants in most terrestrial ecosystems (see Chapter 8). The
remainder of the described mesostigmatans are parasites. Sixteen of the 17 fam-
ilies in the superfamily Dermanyssoidea are composed entirely of para~itesof
mammals, birds, reptiles and arthropods. Dermanyssoids range from facultative
ectoparasites, to obligate enoparasites, to obligate internal parasites of vertebrate
eat canals and respiratory passages (see Chapter 9).
Mesostigmatams have three-segmented chelicerae and most are fluid-feeders with
membranous processes that filter out particulate matter. As in ticks,the gnathosoma
resembles a small head (capitulum) with a basal, sderoused ring brmed tiom the
L i o n of the palp coxac and gnathosomal tecrum. The body t o h dorso-vend-
ly flattened, oval to sub- in shape and protected by dorsal and ventral sde-
rotised shields, at least in the adults. Mesostigmatans lack any indication of eye
lenses; however, pigment spots can be seen on the antemlacecal margins of the idio-
soma in some lightly sderotiscd, plant-inhabiting species. The distal part of the first
pair of legs has a welldeveloped field of sensory setae that is sometimes within a
pocket-like depression (reminiscent of Haller's organ in ticks) and may or may not
have paired daws and an ambulacrum. No mchobothria are present but a fkw species
of K-~gaia(Veigajidae) have what appear to be h a i o n a l l y similar modified setae on
the legs. Sperm nanstk is by means of the chelicerae. Males of m l y derivativegroups
of M d g m a r a tclnsfiir sperm directly to the female genital opening with unmod-
ified chelicerae; however, a more elaborate system has devdoped in some groups (see
Chapter 5). Eggs are produced singly in the Dermanyssina but one, nvo, four or a
few dozen eggs are rnarured concurrently in other less derived lineages.
ACARIFORMES
- THE MITE-LIKE MITES
The Acariformes (Figure 3.4) are by far the most diverse of the three orders of
mites, with over 30 thousand described species contained within two suborders,
the Sarcoptiformes and the Trombidiformes, and a paraphyletic trashbin of
primitive forms - the Endeostigmata - composed of about 10 families of
minute, soft-bodied mites. Most endeostigmatan genera are found worldwide
and often in exrreme habitats, especially deserts (cold and hot) and deep soils.
One or two pairs of trichobothria occur o n rhe prodorsum, and one or two pairs
of simple ocelli (the remnants of ancestral compound eyes) may be present.
Some species also have a median ocellus under a projection of the anterior
prodorsum (the naso). Chemosensory secae (solenidia) and often trichobothria
are present on the legs.
- Most of the setae and other cuticular structures have a
core of material that glows under polarised light (actinopilin, and hence an
alternative name for the order, Actinotrichida). The chelicerae are cwo-segment-
"
ed and most species have well-developed rutella that act as shears to clip offseg-
ments of food for swallowing.
The Endeostigmata can be divided into two groups based on the presence or
absence of rutella Endeostigmata with rutella, such as the h i l i e s Alicorhagiidae
and Terpnacaridae, are certainly sarcopriformans. However, those that have lost
the rutellum may be related to the Trombidiformes (OConnor 1984). The fav
endeostigmatans that have been studied ingest solid foods such as hngi, algae and
sofc-bodied microinvertebrates like nematodes, rotifers and tardigrades.
Most Sarcoptiformes ingest solid foods, primarily microbes, microinvertc-
braces and bits of decomposing vegetation. Soil, leaf litter, lichens, mosses and
Figure 3.4
Four aarifomuns from rainforest liaer In Queensland: (a) a prirnlcive oribatid mire
(5- sp.). (b) a sobbodied prusdgmam (Cunaxidae), (c) v e d view of an oribarid
mite (WM sp),and (d) dorsal view of an armoured prostigmacan (Labidonomaridae). .
 forest canopies are home to more than ten thousand known species of oribatid
mites (Oribatida, a k a . Oribatei, Cryptostigrnata). Many of these mites are
encased in a sclerotised cuticle as adults and, along with other xlerotised acari-
formans and uropodine mesostigmatans, are called beetle or armoured mites.
Most species are microhcrbivores, fungivores and detritivores (see Chapter 6). A
monophyletic lineage, the ~ s t i ~ m a appears
i, ro have arisen within the
Oribatida (Norton 1998). Early derivative asrigmatans somewhat resemble the
immature stages of oribatid mites and have similar feeding habits. However, a
derived lineage of astigrnatans, the Psoroptida, are primaril;assodated with ver-
1
tebrates and nesr-building insects. Scab and mange mites, as well as house dust
mites, stored product mites, feather mites and some fur mites belong to the
Psorootida Gee Chaoter
' 9).
-,
T h e Trombidiformes also contains a number of mites parasitic or cctocom-
mensal on vertebrates and invertebrates; however, it is the plant-parasitic trom-
bidiformans that cause the most economic damage. All of the major acarine
plant parasites bdong to the Trombidiformes, including spider mites, flat mites.
car& mites, gall mites, erinose mites and bud mites (see Chapter 8). These plant-
parasitic mites are found in 10 families in three trombidiform lineages. T h e
remaining 110 families contain predators, fungivores and animal parasites. T h e
largest and most spectacular lineage, the Parasitengona, includes more than
7000 described species of t e m m a l and aquatic mites. The parasitengone life
cycle is complex, involving a parasitic larva, two pupa-like resting stages and two
active predatory staga (see Chapter 4). Within this group, velvet mites and
water mites are conspicuous because of their size (some > 1 un long) and often
brilliant colours. At the opposite end of the size scale, larval chiggers (or scrub
itch mites) are pesky inhabitants of meadows and grasslands whose bite can
result in welts and a maddening itch, or worse, transmit microorganisms that
cause scrub typhus.

HOW DO MITES DO THE THINGS THEY DO?

Morphology and behaviour are the costumes and scripts in 'the ecological theatre
and the evolutionary play' (apologies to G.E. Hutchinson), so some understand-
ing of mite morphology is a prerequisite for any discussion of their behaviour.
Mites are arthropods with ccternal skeletons and a maximum of six pairs of
jointed limbs and, as with all arthropods, the limbs are the key to understand-
ing behaviour. Below we review the morphology of mites in terms of how acter-
nal structures are used to get through life.

Feeding, sensing and silk - the gnathosoma

At the front end of the mite body, the chelicerae and palps are used primarily in
capturing, tasting and ingesting food (Figure 3.5). T h e earliest mite probably
had chelatdentatc chelicerae, i.e. shaped like pincers with toothed digits
(Figures 3.5d. 3.6e). T h e pincer is formed from a distal segment, called the mov-
able digit, that articulates against a dorsal extension of the second chcliceral scg-
ment (the fired digit). As might be expected, chelate-dentate mouthparts are
useful for cutting things into pieces small enough to cat (Figure 3.5d, e) but they
are also useful for ripping holes in the bodies of prey (Figure 3.Ge).
MITES: ECOLOGY.E V O L U T I O N
AND BEHAVIOUR
Because most arachnids are predators chat feed only on the fluids of their
prey, it is thought that predation and fluid-feeding are the ancestral behaviours in
this group (Krantz 1978). However, it is possible that the earliest mites were more
i n c l i k l ;o scavenge and ingest solid fodd. The earliest known fossil mites from
the early to mid-Devonian are primarily from groups whose modem descendants
swallow microbes, bits of decomposing organic matter and minute, sofi-bodied
invertebrates, such as nematodes (Walter 1988a, Walter & Proctor 1998a). Their
chelicerae are two-segmented and generally fairly stout - useful organs for cut-
ting organic matter into small bits before swallowing. In contrast, mites with
three-segmented, relatively slender, chelate-denrate chelicerae can rip holes in the
sides of animals and exrend the chelicerae into the body of their prey to macerate
the internal tissues. For example, many mesostigmarans and allothyrid mites are
fluid-feeders that use their chelicerae to hold, mash and chew small arthropod
bodies but they can also extend their chelicerae into the wounds of larger animals
and move them rapidly back and forth as they shred internal tissue.
Among modern mites, all known Opilioacariformes, mosr Parasitiformes
and many Acariformes retain the chelate-dentate condition. However, all ticks
Figure 3.6
Useful structures from various mites: (aj ventral view of the hypostome and -&wsrernum
of a mesostigmarao. (b) the stalked eyes of a wmbidioid mtte. (c) an adult female oribatid
mite with hcr onpostwr extended. (d) the bothridla1 sensillus of an oribatid mire
(Brnchychhonius sp.). (e) Imeral view of zhe chehcerae of a predatory mesosdgmatan
fGamosellus sp.).
and mosr of the other parasitic lineages within the Parasiriformes have modified
cheliceral digits chat pierce or slash tissue. In the Acariformes, mites that are par-
asites of vertebrates, arthropods and plants tend to have stylet-like mouthparts
(Figure 3.54. Plant parasites, such as spider mites, have long, whiplike srylets
capable of probing beneath the epidermis of a leaf and stabbing individual celh.
Many succasfi~llineages of predators and hngivores also have piercing-sucking
mouthparts. Predators and hngivores often have movable digits modified into
stout, sharp spines capable of penetrating arthropod cuticle or hyphal walls.
Many of these modified cheliccral forms are distinctive and can provide a good
indication of how their owners earn a living.
Chelicerae are also used in non-feeding roles. In agoniscic (or cannibalistic)
encounters, the chelicerae of mesostigmatic mites can be used to thrust and
parry (Lindquist & Walter 1989). Male spider mites attack and even kill preda-
tory mites by stabbing with their cheliceral srylets (Saito 1986a, b). Males of rwo
derived lineages of mesostigmatic mites have modifications of the movable digit
used in sperm transfer (see Chapter 5). The finger-like projection is called a
spermatodaayl ('sperm finger') in the Dermanyssina and a spermatotreme in
the Parasitina Chelicerae can also be used to hold onto a host during phoretic
migration.
The palps are used to sense food and handle prey during feeding. They rypi-
cally resemble small legs but may be antenniform (e.g. Bdellidae), raptorial (e.g.
Cunaxidae [Figure 3.4b], many water mites), armed with a daw-like suuccure (e.g.
spider mites, Trombidiodea) or reduced to stubs (e.g. Tarsonemidae). They are
usually well supplied with mechanoreceptory setae, and clusters of sensory secae at
the tips of the palps presumably allow mites to caste their food before and during
feeding. Many mesostigmatans tap the substrate with their palps as they walk.
The production of silk from the gnathosoma appears to be a basic abiliry of
acariform mires, although silk production has been lost among sarcoptiformans
(except, perhaps, for signal threads leading to spermatophores produced by some
oribatid mites - see Chapter 5). Primitively, silk seems to have been used pri-
marily for protecung eggs and quiescent immature stages. For example, adult
females of the endeostigmatan A f i ~ o r h a g i a ~ f (Alicorhagiidae)
is weave a silken
platform on which the eggs are laid, and larvae and nymphs spin a protective
cocoon around themselves before becoming quiescent and undergoing a moult
(Walter 1988a). The use of silken cocoons for protection of eggs andlor imma-
ture mites also is known to occur in several prostigmatan lineages: Eupodina
(Eupodidae, Bdellidae, Cunaxidae, Tydeidae, Eriophyidae), Anystina
(~d-ystidae, Anystidae) and hphignathina (~heyletidak,~ a r p b h ~ n c k i d a e ,
Camerobiidae, Teuanychidae). In most of these mites the fine silken strands
originate within the buccal opening From modified salivary gland secretions
(Gerson 1985). However, some spider mites have a large unicellular gland that
extends from within the body ro the spinneret -a hollow sera at the tip of each
palp. Early derivative spider mites use silk primarily for protection of eggs and
moulting immature mites but, among the true spider mites, silk is used through-
out the life cycle: egg and moulting covers are spun, active stages live in or under
silken webs, males sequester quiescent female deutonyrnphs under a silken mat
and silken strands may be used as droplines and to hcilitate aerial dispersal.
Some predatory prostigmatans also use silk in prey capture (see Chapter 6).
MITES:
ECOLOGY,EVOLUTIONA N D BEHAVIOUR
Moving, sensing and interacting - the legs
In the Opilioacatifbrmes, Parasidforma and in many Pmstigmaca, the fim pair
of legs arc used like antennae and are o h slender, elongate and lack welldevel-
oped claws Figures 3.3,3.4). Like the palps, the first pair of legs usually have
dusters of sensory sene near their tips. When walking, many mites paform
characteristic leg-waving mwcments. Sometimes these movements arc stens-
typic enough to be diagnostic For example, the oribacid mites Oppicb nwaand
Oppia n i m that are commonly sympauic in mesic soils are easily distinguished
by the characteristic leg-waving behaviour of 0.nitem that is absent in 0. n o ~ a
(Scniaak 1975).
The first pair of legs are o h used to size up a potential sexual partner or
prey item through tentative capping movements. Legs may also be used in prey
capture. In some predatory mites, the first two pairs of legs are used in con-
junction with the palps and chelicerae to hrm a basket-like amangemat of
limbs to entrap small arthropods (Coineau 1973, Lindquist & Walter 1989,
Proctor & Pritchard 1990). In some mites the first pair of legs arc modified for
clinging to a host during phoretic dispersal. The second, third and hurth pair
of legs are the primary organs of locomotion in mites and,when the first pair are
primarily sensory in h c t i o n , mites arc functionally hexapod. H~wcvet,in
many acarifbrm and some parasidform mites the first pair are also used in walk-
ing.Most water mites use all bur pairs of legs fbr crawling but the last pair may
be trailed Like stabilisers during swimming.
The first two mite instars ( p h larva) are morphologically hexapods, i.e.
their bur& pair of legs is not expressed, but h e are fLnctionally quadripod
when the first pair of legs are used exclusively fbr sensing. In a fkv groups of plant-
parasitic mitts, some legs are absent in all stages (eg. the fourth pair in LatYacanrs,
Tenuipalpidae; the third and f o u d pair in the Eriophyoidea). The most a m u n e
reduaion in legs known occurs in some insect-parasitic Podopolipidae. Larvae and
adult rn& in this M y are o h n hcxapods and adult h a l e s can be reduced to
sac-like bodies with only remnants of the first pair of legs.
Reproduction
Mites have a bewildering diversity of sperm transfer methods (see Chapter 5). In
males, every appendage that can be modified for reproduction has been. D i
uansfkr of sperm via apposition of genital openings has evolved independently
several times in the Acari but this type of direa transfix is relatively uncommon
in mites, most of which use a more indirect route. As previously mentioned,
many parasitiCbrm d e s have spmnatodaceyts on their chelicefae to channel
sperm into the W e ' s genital opening. In other parasitibrm species, the mak
simply pick up a spurn packet (spennstophore) from his genital opening with
unmodified chelicerae and places it in the M e ' s reproductiveopening. In water
mites there arc examples of species that have the first, second, third or burth pair
of legs modified fbr holding and d m h g sperm packets (Proctor 1992). In
the Hydracarina and many Mesostigmata, males have legs modified for holding
h a l e s during mating, or fbr attacking rival males. Tarsonemid mites capture
quiescent prc-adult f d e s and carry them on a suctioncup process on their pos-
terior, although over-enthusiastic suitors ofien sequester developing males, rather
than females (Gargact aL 1997). Finally, there a n a Iargc number of terrestrial
and aquatic mites in which mdcs and f d e s never come into contact during
sperm ffaflSfir; rather, males leave sperrnatophores on a substrate and these are
picked up later by &males. Even stranger than comp1etely dissociated sperm
eransk are the many cases in which mites avoid sperm altogether. reproduction
by virgin females @ardrmogcnesis)is very common in mites.
-
Female mites have fewer modifications fbr gamete or rather zygote -
amusion. Most mites lay eggs on a substrate without having special genital
structures b r oviposition. However, many oribatid females have cxavsible
ovipositors (Figure 3.6~)for probing into safk soil and litter niches (Kranrz
1978), and fkmales of the water mite genus Hydnzchna use their ovipositors to
push eggs into the air spaces of aquatic plant tissues. Funaes of another water
mite, Unionicola, have long spines on their genital valves that prise apart tissues
of the sponges and mussels in which these mitcs lay their eggs.
Digestion and excretion
The basic organisadon of the chelicerate digestive system is strikingly different
h m that of mandibulate arthropods (Snodgrass 1948, Manton 1977).
Cheliccrates do not have grinding jaws and the pincer-like chelicezae lie above a
mouth opening that is rooflsd by a small plate, the qistome ('above the mouth'),
that has a projecting lip (the labrum). In horseshoe crabs, the mouth opens
badcwards - towards a pocket formed by the s p i n d come of the pedi-
paps and the second and t h ' i pair of legs @dobases). Sh&h, worms and
other creatures captured by the pincers on the limbs of horseshoe crabs are
crushed and killed by the spiny coxae. The strongest pair of crushing coxae are
chose on the fourth pair of legs, at the posterior end of the prosoma; these are
capable of cracking open relatively large dams (Manton 1977). As the coxae sub-
due and shred the M, pieces are moved into the mouth by the pincer-likc chc
liceme. A muscular &mad completes the masticatory process and the hod
passes down the oesophagus into the midgut where it is finher d i g d &re
being forced into the radiating branches of the gut (diverticula or caeca) where
epithelia cells engulf the food particles and complete the digestion.
In most arachnid orders, the coxac are not gnathobasic and the mouth
points forward into a pre-oral opening hrmed by the padipalpal coxae, epistome
and labrum The gizzard is replaced by a pharynx and only fluids enter the
midgut - sucked through filtering structures around the preoral opening by
the dilation and constriaion of pharyngeal muscles. In this + parasititbrm
and trombidifbrm mites arc typical arachnids. Digestion begins externally as
enzymes arc pumped into the mangled body of a prey or a plant d l and con-
cinues in the midgut and gastric caeca. The branching pamrn of gasaic caeca is
o k n visible in mites as digestive products accumulate in them.
Sarcopabnn and opilioa&rm mites, however, havc a very different
fixding mode. Chelicerac, assisted by rutella on the hypostome (which are at
least analogous to the spiny gnathobases in hofseshoe crabs), cut off pieces of
food and move them into the mouth. No gizzard is present, so additional com-
minution of the food does not occur. In fia,food W e n t s can ofien be
identified in the gut contents of these mites. A ball of food accumulates at the
base of the oesophagus and is compacted into a food bolus that gradually
makes the transit of the midgut to the anal opening. T h e gastric caeca in these
mites are generally lobe-like and simple in structure. Pigments or other diges-
tive products may accumulate in these gastric lobes but the bulk of the ingest-
ed material remains in the bolus (covered by a peritrophic membrane). Up to
three boli in various stages of digestion are commonly present in actively feed-
ing oribatid mites. At the end o f its journey, the bolus is expelled as a fecal pel-
let through a relatively large anal opening covered by a pair of trapdoor-like
valves. T h e few parasiriform mites that have secondarily evolved feeding o n
particulate foods also have relatively large a n d openings, e.g. some species of
Proctolaeikps ('anus hurricane').

SUMMARY
Mites representing three major lineages are alive today and the basic differences
among these orders are often more strikjng than the similarities. However, nll
mites have an anterior section resembling a tiny head (the gnathosoma or capit-
ulum) that contains the two pairs of limbs devoted to feeding: the chelicerae that
lie above the oral opening and the pedipalps, whose Fused come form thc floor
and sides to the opening to the digestive system. T h e remainder of the body is
more or less fused into a sac-like idiosoma that contains organs of digestion,
excretion and reproduction. Except in the Sarcoptiformes, movement is usually
hexapod, with the first pair of legs being used as feelers. Parasitiform and trom-
bidiform mites resemble other arachnids in that they feed primarily on fluids:
blood, sap or externally digested tissues. Sarcopriform and opilioacariform mites.
however, bite off bits of food and swallow them. T h e great variety of feeding and
reproductive habits exhibited by the Awri will be discussed in detail in the fol-
lowing chapters.

M
atcrnal care is widespread among cheliccrates and mothers ofien
carry eggs and developing young. Even some horseshoe d fkmats
carry their eggs until they hatch (Shipley 1909). On land, arachnid
mothers o h build a burrow, a sillr-lined chamber or a silken egg
sac (spiders) in which eggs or broods are protected. Many scorpions, whipreorpi-
om, sun scorpions, s p i d a ~and pscud~~~)rpions guard their young until they arc
M y aaive and mdy to begin hunting. Paternal care appears to be much rarer but
males in the neompid opilionid genus ZygopadyW construct a nat into which
fkmales place their eggs &er mating. The malts dean the eggs of &gal parasites
and ward off potential predators, espedally other opilionids (Mora 1990). Other
cases of paternal cue have been reported ( M a n a s 1993) and some fkmale opil-
ionids are known to guard their eggs and young j u d e s (Mitchell 1971, Ramires
& Giaretta 1994); ~ O W C V ~most ~, opilionids limit parental care to the use of
ovipositors to seucte eggs in atvices or in the soil (Preston-- & Preston-
Mafham 1993).
From what we know of mites, they tend to be less caring parents than most
arachnids. When it comes m overall rcproduccive &rt, speed of development
and modifications of ontogeny, however, mim arc without peer. In this chapter
m review the lifk cycles of mites and end with a dtarssion of the relationships
between lifE:history parameters, generation times and size.
OVIPOSITION
Almost all mires begin their lives as eggs, laid singly or en mase. Occasion*,
mite eggs have the shape and aspea of minivurc hen's eggs but more o h h e y
are spherical, bamquely ornamented or bizarrely formed. For example, the eggs
of ornate f i k spider mites (Tudcuellidae) are dc-like red flecks covered with
waxy ribs and horns. Variations of shape, colour and ornamentation arc com-
mon enough for it to be ofan possible to diffacntiate the eggs of symporric
species. Whatever their appearance, howc~er,mites arc usually very particular
about whue they lay their eggs.
Parental care
Maternal cue in mites is usually limited to hiding eggs in crevices, laying them
within silken webs, sovering them with detritus parcides or a jelly-& sheath,
or conveniently dying with them protected inside the mother's body. For exam-
ple, red-legged earth mites, HaCotythw ubwctvr, &al on pasture plants during
the autumn and win% As spring approaches, the firnales die, their bodies filled
with diapausing eggs. The eggs rrmainwithin the f;emae's body until they hatch
the next autumn (W!allace 1970). What appears to be a similar behaviour occurs .
in some mites with well-sclerotisad cud&. For example, egg-filled shells of
dead armourcd miter can be found and larvae sometimes hatch fiom these eggs
but it is not dear how easy it is for than m escape fmm what is probably a
rnacefnal tomb (Norton 1994).
Howewer, most mites oviposit and show considerable care in the choice of
sires where eggs are laid Oribatid mites usually use an emurible ovipositor,
sometimes as long as the f;unale'sbod5 to place their eggs within crevices. Some
water mites prepare oviposition sites in .the stuns of aquatic plants with their
chelicerac (see Chapter 7).Female dermanyssine Mesostigmata develop a single
large egg at a time. Each egg fills the opisthosoma, causes considerable disten-
sion and may weigh as much as 40% of the non-gravid fkmale's body mass (thus
r i d i n g the kiwi fbr m a t d investment in a single egg). Under fivourable lab-
oratory conditions, fkmales may lay 4-8 eggs, or 2-3 times their body mass, per
day. Wore oviporiaon, the W e may spend several minutes investigating
ctacks and cfevices.The egg exits fiom the genital openiw which usually resem-
bles a trapdoor hinged posteriorly at about the level of the burrh pair of come
and covering the entire intercod width. As the egg is amuded anteriorly into
the dregion, the gnathosoma is bent to receive it and the egg is grasped
between the palps and the dorsum of the gnathosoma. The egg is so large that
f d e s often need to stand on M y extended legs to allow its passage. Using the
chelicuac, paps and first pair of legs, the f e d e cardidy places each egg in a
d c e or other recess and may spend several minutes capping it into place.
Parddes of soil may be scraped onto the egg and patted into place but soon the
M e loses interest and wandus 06possibly because the pressure of the next
swelling egg ~ c i a t e ssearch for a new oviposition site.
Another case of possible parental care in mites is the oribaud Dama~uuer-
tin'CltPes (Oribatida). In this species oviposidng females may lay their eggs on the
backs of conspecific males (Canceb. da Fonseca 1975). A few species of
halacarids arc known to carry qgp attached to their posterior legs until they
hatch but they have no known interactions with juveniles (Harvey1990, Bartsch
1996). Camying or guadng eggs h r longer than described above is rarely
reported among acarines. Occasionally, mites and ticks have been observed
tunaining near a clutch of eggs and sometimes they appear to help larvae escape
the egg shell (Walter 1988b). The predatory cheykad mite Chgukzu enu&tw is
reported to guard eggs against intruders (Summers & Win 1972, Preston-
Mafham & P r e s t o n - M b 1993). This is probably a general behaviour in this
M y because in A u s t d a n forests cheyletid mites in two other genera,
0 ~ n t ~ ' c h y lcopmsomac
iz and Hmichcykctict wcIlsi also actively detind their
eggs. The &male lies in ambush at the base of a leaf, usually along the main vein,
and attacks mites and small inseas that attempt to enter the I d . Usually, 3 4
eggs arc brooded at a time, each within a silken covering. Funales stand their
ground when disturbed and repeatedly snap their palps and stab with their chc-
licesac when probed Hatchling larvae and protonyrnpk can oftcn be found
near the mother but they soon disperse out onto the leaf surface (Walter, unpub- .
lishcd). These and other chcyletid mites may be showing the first indications of
sociality (Saito 1997). Some subsocial spider mites in the genus Schiao~n~~nychuz
carry this protective bchaviour one step fiuther. Both males and f k d e s active-
ly deknd their young within silken nests f k m marauding phytoseiid mites
(Saito 1986a, b, 1997).
Egg number and egg size
The complete gamut of rcproduaivc strategies can be fbund in the Acari, from
the repeated production of s+e eggs or egg clutches (iteroparity) to a single
burst of reproduction (semdparity), and ofien extremes of &rt can be hund
within a single lineage. For example, adult f k a l e argasid ticks r y p i d y produce
about a hundred eggs aftu each fixding event but ixodid ticks have a single mass
 Devclopmcnr is usually gradual, wirh immarurc mircs morc or lcss resembling
the adults (homeomorphic). In a few mire lineages onc insrar differs dmmariwl-
ly from the othen and is said robe heteromorphic. For example, Astigmata have
hercromorphic deutonymphs referred ro as hypopi (or hypopodes) and
Pamitengona have hcreromorphic larvae. In 1 sense, mosr awrine 1-e are her-
emmorplic because they are usually six-legged (hexapod), rarher than eight-legged
(octopod) as arc nymplw and adulrr. P r c l m e , when prcsenr and well formed, arc
also howpod, and are invariably scmngly kreromorphic. Immamre swga and
adults of Inany orihacid mires are quire different in form and can be difficult ro
associate widlout rearing. L ? m c and nymphs are evily confused with astigmauns
by novices. Both =are whirish, lighrly sclerorised snrwptiform mires with sac-like
bodies and single claws. Adults of higher oribadds (bcerle mitcs), in contnst, are
srrondy
- . sderotised, typically
.. . a shiny brown o r deep black in colour, and ofren have
wing-like lateral processes (pteromorphs) and thrcc claws.
Cuticular growth within an insrar (neosomy) is known for chiggers, hard
cicks and some pamitic Mesostigmata (Radovsky 1994) but, in general, intra-
moult increase in s i x is restricted ro swelling or unfolding of previously deposit-
ed cuticle. Post-adult moulc; have been reported from a few pamitengone mites
and some soft ricks have brtra' nymphal moults (Evans 1992) but these seem to
be clear additions to the basic dcvclopmental parrern. Alrhough such ancillary
moulting is rare in the Acari, the loss, suppression and reduction of instars is an
awrine lcirmotiv.
Larva and prelarva
in mosr arachnids rhe firsr acrive instar is an eight-le~edcrexure wirh imper-
fecrly formed limbs and little or no retarion (Kacsmer 1968, Foelix 1982, Polis
& Sissom 1990, G n a r d & Stockmann 1993). This 'larva' (Foeli 1982),
'incomplrte juvenile' Ui. JiI or JP of Canard & Stockmann 1993) or '11 Lrva'
(as we will d l iO usually can move bur docs not fecd. In some of h e larver
~
o - ~
arachnids (scorpions, spiders, whipscorpions), the J l larvae climb onto the back
of their mother and undergo further dcvelopment Fuelled by yolk reservcs unril
moulting into rhc 'nymph' or second insrar juvenile 02). Thc J2 nymph usual-
39
ly has functional mouthpnrrs and actively hunu and fced~.In rhe opilionid
E p ' n u l u ~(auotibiali~,
a J1 larva wirh vestigial mouthparts, cyes, setation and
limb segmentation emerges from the egg and moults almost immediately inru
an active 12 nymph (Goodnighr & Goodnighr 1976).
Many spiders and whipscorpionn have 1-3 moults char occur afccr the end
of embryonic dcvelopment bur prcccde rhe formation of d ~ 11 e larva Thesc
prelarval or foetal inscars arc only partidly dcvelopcd and may bc retained wirh-
in thc egg. Thosc that burst from rhe chorion are immobile, have eight legs with
incornplcre segmcnrarion, and lack cyes, claws and setac (Canard 81 Stockn~ann
1993). Modern xiphosuran eggs hatch into ='blastodermic cuticlc' char gives rise
to the trilobite larva (Shiplcy 1909). Possibly the prelarval curicles in spiders and
whipscorpions arc rcmnanrs of planktonic stages in their marine ancestors.
In mosr rnircs, d ~ fci r s sctivc insrar is a hexapod feeding scagc cdlcd rhe
larva. Buds for the fourth pair of legs appear early in embryonic development
bur then rcgress. In some mites, another heupod stage, rhe prelana, precedes
the larva. The prclarva of the opilioacann P/dmyiacnnrr- bromri hzs three airs
ofrcgmmrcd legs and only bumps wherc the fourth pair of lcgs would arise. Thc
gnathoroma is nor much reduced but no body serae are cx~resscd(Coincnu 81
van der Hammen 1979). Ac with the ocropod J1 larva in spiders, wl~ipscorpionr
and opilionids, rhe hcxapod prelarva of mites does not fced.
In acarology, stages of ontogcnecic dcvelopmcnr arc often wllcd s t a u s
(Grandjean 1969). In the Awriformes, the prclana is usually considered ro be a
regressive srase, i.e. reduced from n previously more fully dcveloped form and, in
a sense, dc~cnerare.At best, the limbs and their seration are rudimentary and
prelarvae of many species are 'reduced' ro a featurelas laycr of cuticle or are entire-
ly absent. Most early derivative acariformans have inactive, non-feeding prel-e.
In mire jargon, presumed regressive swses arc referred to as elanostaser ('reduced
swes') if they w move bur nor fced and as d y p t o s t a r n ('veiled sager') if they
can neither move nor fecd. Calypxraso often consisr of lirde more than a layer
of cuticle (apoderm) within the skin of the previous sese. In most oribarid mites
and in tllc cndeostigmatid mites Tkpnurano ghbulcnm and Abns roscu, the
prdana is a leglw blob within the egg Walter 1988a, Kcrhley 1992). Other early
derimdve aeriformans have a dyptosecic prelana that banrly procruder from the
egg afrer it splits, although ir may have some hypertrophied setae that protect the
protruding dorsum (e.g. Hybalim). In Alimrha+f.agrgr& thc adult Female spins a
small sheer web on which she lays her cggs. When d ~ e cm hatch, the legs of the
prdarva expand away from d ~ body, e pushing rhe egg shell remnants away Walrer
1988~). Ocher than the, presumably, hydrosraric expansion of the lcgs, the exposed
 MITES: ECOI.OGY,E V O I . U T I O N
AND BEHAVIOLJR
prelarva of this species is completely inactive, with rudimentary cheliccrae, leg seg-
ments and setation, and resembles the immobile octopod first inscar of solfugids
(Grandjean 1738; Cloudsley-Thompson 1792).
A few acariformans, however, have an active, ellatostatic prelarva similar to
the J l larva in opilionids. In the anystid mite Chaursimir vmusrirsitna, the prelar-
va emerges from the egg shell and wanders around for 2-5 hours before becom-
ing quiescent and moulting to the larva (Otto 1777). Elattostatic prclarvae are
known in three other species: an undescribed anystid mite (Otto 1777) and the
adamystid Saxidrornus dclamani (Coineau 1776). both in the Anystina, and in
40 the endeostigmatid Spekorchest~podt~r0ides (Nanorchestidae) (Schuster & Potsch
1787). All of these mites seem to be members of relatively derived taxa within
their lineages and certainly are not the most primitive of acariform mites. Other
known acariform prelarvae are calyptostatic and most are partially or fully
retained within the egg.
In contrast to prelanrae, mite larvae tend to approach life with open mouths.
For example, larval Mesostigmata from soils in Colorado typically have chelicer-
ae that arc well developed enough to capture, puncture and feed on smaller inver-
tebrates. Larval Lasioscius, Gamasellodcs (Ascidae), Dcndrolaclaps
(Digamasellidae), Rhodncdrus and Rhoakarellw (Rhodacaridae) will starve with-
in a week if food is not available. In contmt, larval feeding is Facultative in species
of Protogarnasellus (Ascidae) and absent in species of Laelapidac and
Macrochelidae (Walter & Lindquist 1787, Walter, unpublished). Phytoseiid
mites living on the leaves of plants also vary from obligate to facultative to non-
feeding larvae, with only a few derived taxa being the latter (Zhang & Croft
1774). Larval feeding also appears to be the norm in the Auriformes.
Endeostigmata (Walter 1788a) and, as far as is known, Oribatida (Walter &
Proctor 1778a) have larvae that actively feed. Most Prostigmata have feeding lar-
vae, although some Labidostommatidae and Rhagidiidae (Eupodina) are report-
ed to be non-feeding (Evans 1772). As in ticks, the parasitic larvae of
Parasitengona actively seek their hosts and some, such as Vatmarus ipoides, a
trombiculid mite that lives in the nostrils of sea snakes, feed only as larvae.
Determining the homologics of instars or stages within a group as diverse
and ancient as the arachnids may not be possible bur we believe chat develop-
ment in mites will be best understood when their relationships to other che-
licerates havc been fully explored. To date, the only coherent approach to this
problem within acarology has been the school of thought founded by Franqois
Grandjean that considered regressive evolution to be the dominant forcc in the
phylogenctic history of the Acari. For example, in this tradition Kcthley (1970)
hypothesised that the prelarvae of ancestral mites were fully formed and fully
functional and that the few known ellatostatic prelarvae are closest to this ances-
tral condition. However, Otto (1777) argues that modern prelarvae that are
capable of movement were derived several times from immobile prelarvae in tam
that inhabited dry habitats, probably because movement increases the ability of
the prelarva to secure a humid microsite for moulting or to avoid cannibalism
by siblings.
Are mite prelarvae a regressive remnant of a formerly more perfect scxge?The
overall behavioural and ontogcnetic trends discussed above suggest the following
hypothesis. A non-feeding instar subsisting on yolk reserves and cared for by the
mother is charactcristic of most arachnid orders. Because both this stage and the
associated maternal behaviour are present in both pulmonate arachnid and scor-
pion lineages, we consider it plcsiotypic and probably inherited from marine
ancestors. The non-feeding aurine prclarva, therefore, is homologous to the non-
feeding arachnid J1 larva (Table 4.1). The loss of extended maternal parding of
prelarvae may be an apomorphy of the Acari, perhaps accompanied by the repeat-
ed production of a few, relatively large eggs that were laid and then abandoned.
With no mother to seek out and crawl upon, mobility in the mite prclarva no
longer provided a selective advantage (except in some modern forms characteristic
of dry habitats). Unlike the arachnid J 1, acarine prelarvac do not express a fourth
pair of legs; however, as in the larva, we believe that this is most simply interprct-
ed as a derived character state within the normal dcvelopmcnd sequence, i.e. an
apomorphy of the Acarinomorpha, and not an indication of a stage lost in othcr
arachnids. Suppression of a fourth pair of legs may allow the redirection of
resources to other, more essential, parts of the developing embryo. Similar devel-
opmental constraints may explain the loss or retarded expression of the posterior
pairs of legs in very small mites in the Eriophyoidea and Demodecidae.
M y the prclarval or othcr stages (or at least their apoderms) arc retained
where they now havc no obvious function may have to do with the canalisation
of development: particular developmental steps or additions of structures require
the formation of che apoderm of the previous stage. This seems to be the sim-
plest explanation for the formation of calyptostatic protonyn~phs and
tritonymphs (see page 44). However, in some mite lineages the prelarva and
other stages arc apparently lost.
The first feeding stage in mitcs is the hexapod larva, while in other arach-
nids i t is the octopod J2 nymph. Assuming these two stages are homologous, the
three nymphal stages of mites may then be homologous to the succeeding
nymphal stages in other arachnids (i.e. J3,J4, J5), provided no instars havc been
added to or subtracted from these developmental sequences. In mites, addition-
al moults are known only in a few seemingly derived mite taxa; therefore, these
are most likely to represent evolurioriary innovations and not retained or re-
expressed ancestral arachnid stages.
 Suppression and skipping of nymphal stages
Rcdoccion in the number and degree of cxpression of free-living onrogrnetic
stages has been a recurring motif in acarinc evolurion. Indeed, the reducrion
in stages ro a maximum of five juveniles is a possible synapomorphy of thc
Acarinomorpha. Howcver, onc major radiation of mitcs, the Sarcopriformes,
has found the expression o f a full developmenrnl scqucnce no impedimenr ro
success. In all known oribatid mires, a full developmental sequence is present,
although prelarvae are reduccd to a minimum cxpression.
Thc Astigmara (a derived lineage of oribatid mites) are a special casc.
Asrigmatans often have an unusual deuronymph modified for dispersal - a n
elattostatic heteromorph or hypopus in mire speak. iHypopi d o nor have func-
rional nmurhparrs and usually haw incomplete guts (I-louck 1994). In mosr
taxa rhe formation of the dcuronymph is facultative. When ir is nor formed or
when it is entirely suppressed, as in parasitic and cctocomrncnsal rpecia, rhe
protonymph moulcs directly to rhe rritonymph, skipping the deutonymphal
instar cnrirely.
Snrcoptiform mires are dcvclnpmentally conservariw and unusually so for
mircs. For mosr lineages of Awri, the evolutionary rrcnd has been the rermi-
nal truncation of ontogenetic sragcr. For examplc, a synapomorphy of rhc
Mesosrigmara is rhe reduction of rheir onrogcny ro a larva and nuo nymphal
insrars, sselningly by suppression of rbe rrironymph. Pharate srages form
directly under rhe curiclc of rhc previous srage ( m e n bcing able ro move unril
just before rhe old cuticle is shed), with no indication of the apoderm of a
missing stage present. Deutonymphs and adult mesortigmatans rypidly have
rlx same serarion, with differences confined ro changes in exrent of sclerorised
plates and chc development of scxual characters. 'Therefore, mcsortigmnran
ontogcny probably results from rhe suppression of rhc rritonymphal srage ibar
Life cycle o f the Parasitengona
The prosrigmaric suborder I'amsitengona includes marc than 50 families and
7000 described species of rerresrrial and aquatic mires. One unifying character-
istic of this morphologically and behaviourally diverse group is rheir vcr). com-
plicated life cycle - perhaps the most complex of all awrine developmenral
patrerlis (Figurc 4.3). Although a prelarva has been dcscribcd for only a few
species af water mires (Hydraurina) (e.g. Meyer 1985) and terrestrial pansiren-
gonrs (c.g. Johnston & Wacker 1967). it is likely ro be a universal srage in this
group. Thc prelam bursts d~roughthe eggshell bur is orhenvise inactive (Mcyer
1985) and rhe larva emerges from rhe thin prelmal curicle.
Most Larval Parasirengona seek out and parasitise an arthropod or verrchrate
host. However, a few rerrcrtrial species and scveral do701 aquatic ones have
dispensed wirh the parasiric *rage, with rather drasric repcrcu~sionson orher
aspects of rheir life hisrory and ecology (see Chapter 9). Depending on rhc
species, thc larva spends from days to monrhs on the host and may be moved a
costaric praronymph. Terrestrial species usually seek a humid site or bury rhern-
,.
selves i n soil, whereas warer mites attach to aquatic vegcr:erarionor seek shelrcr in
the tissues of freshwarer sponges and bivalves (Hevers 1980).
The dcutonymph develops wirhin rhc skin of rhe proronymph, which in
rum is enclosed in the larval curiclc. The deutonympb rhar emerges is a very
diffcrcnr crcarurc from rhc larva. Morphologidly, rhesc nuo stages bear no
I
I Figure 4.3

is present in Holothyridn and argasid ricks. Similarly, convergent suppressions

of rhe rritonymph are charncrcristic of the divcrrr prostigmatic group
Eleurherengona and the endcosrigmatic raxa Alicorhagia and Nanorchesridae.
Ocher mire lineages carry this trend even farther: both ixodid ricks and erio-
phyoid rnircs have a single nymph benvecn the larva and adult. Presumably,
t l ~ cixodid nymph is the protonymphal srage, although chis is not necessarily
true. Derermining homologies of stages among eriophyoid mites is especially
difticolt sincc so many normal characters have been lost (e.g. the third and
fourth pair of legs are lost in all Eriophyoidca). Mowcver, rhe characrers that
remain suggest rhar ir is the larval and protonymphal sragcs rhat are exprcrscd
(Lindquist 1996b).
The mosr extreme truncations in life cycle among any animal species occur
in rhe Hcrerosrigmara. Early d e r i ~ r i v ehererosrigmarans in rheTarxlchcylidac
and Hcrcrocheylidae have a rclativcly complcrc life cycle wirh only thc prclar-
va and rritonymph suppressed (Lindquist 1986). Howevcr, most heterosrig-
matans have only a single active preadult stage, the hexapod larva, This rrcnd
towards reduccd active stages reaches its most cxtrcme possible condition in
gencrn such as Doiichorybc, Sirtrepter, Pycmotes and Arnrophcnax where devel-
opment, and ofren mating, occur within the physogasrric body of the mother
(?&liszrwski er al. 1995).
 resernblanct to each other in the structure of palps, legs or body. This radical
uansfbrmation is similar to the scruaural rearrangement that occurs in insect
pupae, which has led some water mite biologists to call rhc lifk cycle of para-
sitengones 'essentially holomecabolous' (Smith & Cook 1991). As well as look-
ing difhent fiom the larva, the deutonymph behaves diihently. It is an active
predator of &e eggs, larvae and pupae of insects, soft-skinned rnites and (in
water mites) small crustaceans (see Chapter 7). The deutonymph k d s until it
is bloated and then enters a second calyptostase, the aitonymph. In this case the
uansfbnnation is less amcme and thc d o s e d adult is usually morphologically
44 similar to the deutonymph. However, in water mites the adults arc often more
highly sderotised than the deutonymphs and in sexually dimorphic species the
W e resembles the deutonymph more closely than the often bizarrely modi-
fied male. Adult parasitengones are predatory and have diets similar to their deu-
tonymphal stages, although they may feed on larger prey. Only the first active
stage of parasicengone mites is parasitic; the other stages are free-living.Animals
that arc parasitic only as immatures are called protelean parasites (Treat 1975).
This dewlopmend pattern is rare outside the Parazitengona but some astig-
matans have deutonymphs that are protelean parasits in mammalian hair bUi-
des or under the skin of birds (Athias-Binche 1991).
Parasitengones are among the longest-lived of aca&rm mites. Species of giant
&t mites found in desar regions of Afiica and Norrh America are thought to
live several years as an adult. This long life may be due in part to these mites being
a& only immediatelya f k rainfgll: the interveningperiods are spent buried and
inactiw (Cnwfbrd 1990). Adults of the water mite Limnocbam a p d a z live fbr
more than two years in captivity (B6-r 1972). Badcr (1980) repons that adult
&pans of 1-2 years are common b r water mites that d d in cold saeams; how-
ever, mites in warm water may live only 2-6 months as adults and have no more
than one generation per ice-free season. One problem with living for a long time
is wear and tear on the cuticle. Old water mites are often wvered with e n d
din, algae and phoredc p r o m a n s and may bear scars from predator attacks
(Proctor, unpublished dam). Perhaps as a result of selection to renew the cuticle,
Limnochmer aguluica is able to undergo supernumemy moults up to a year afier
laying eggs (B6tegcr 1972). Some individuals moulted twia during Biirrger's study
and in every case the adult entered a caiyptostatic state prior to moulting. Post-
adult moults and calyptostases also have been observed in tccrestria pansitcn-
go= hkhener (1946) s ~ a a sthat -M . . tnawkmm (Miaouombidiidae)
may moult up m seven times as an adult. The amount of growth bcrwetn such
moults varied greatly (cg. the increase in length of the cusi on the first pair of legs
ranged h m 0.02-0.19 mm).
Paedomorphosis, ptogenesis and neoteny
Ekdogmesisor reproduction by immature individuals has been qorted f$r a
plant-parasites on citrus (Baler 1979, Ochoa 1989), but appears m be ntrrmely
rare in mites. Paedomorphosis ('child shape'), however, &rs to the prsence of
a n d juvenile chanaers in later developmental stages ( o h the adult). Sevrral
authoa haw applied this wnccpt to mites (Kethley 1974, Atyeo et aL 1984;
OComor 1984). For example, the adult k d e s of MdyLtia, cheyletid mites
living in the kachers of parrots, are hcxapod and rcsemble 'a large, globubr larva
with funmonal genitalia' (Atyeo et al. 1984). Gould (1977') proposed that paedo-
morphosis resulted from two e ~ l o g i d disdna
y seleaive regimes. h r d i n g to
God& hypodus'is, progenesis ( ' b d produdon') rentla &om amlcrated
maturity in species exploiting ephuneral rcsoutws; in wncrast, retardd m a d o n
in species compering for stable resouroes d t s in neoteny ('extended youth'). In
both cases the d t is a later developmend stage that in some sense rrsunbles an
earlier developmental stage of a presumed ancestor.
Several groups of sarcoptiform mites have adults that arc poorly sdcrotised
and resemble the immanms of related taxa. However, there is no indication that
these 'larvifbrm' adults result from extended developmental periods (neoteny).
Rather, evolutionary change in the Acari is characcerised by the loss of segmenrs,
structures and stages and by the acquisition of smaller body sizes and b r devel-
opmenral rates. Gould proposed Simptes graminurn (Figure 4.4) as an acarine
example of progenesis. Development is h e r in offspring produced physogasui-
cally and they have fewer l a d cuticular structures than those that develop from
eggs laid outside the mother (Rack 1972). On a broader scale, the entire
~-esosti~maracould be interpreted as an exam-
ple of progenesis. Mesosagmatans arc sexually
mature afcu three moults, compared to bur in
holothyrans and most argasid ti&, and they arc
generally smaller, less hirsute, less w d armed
and develop much faster than holothyrans
(Walter & Proctor 1998a). However, adult
mesostigmatans do not resemble immature
holothyrans or ticks.
Many rnites that exploit ephemeral re-
sources have very rapid developmental rates but
main the M I developmental sequencc of more
slowly developing relatives. In some of these
caxa, the adults lack ontogenetically added cutic-
ular mctures normally characteristic of adults.
Chant (1993) has proposed that faster develop
ment within existing stages that results in pae-
domorphic adults be called sequential
progenesis. For example, adult phyrosciid mites
are considered to be hypouichous ('under
hairy'), i.e. setal complement is less than what is
considered the primitive condition (holorrichy
- 'complete hair') in the Mcsosdgmata Chant
(1993) argued that phytoseiid mites tend to be
smaller and to develop h t e r than many of their
more setose relatives and that within the
Phytoseiidae less hairy species tended to develop
fssrer than more hairy species.
Chant (1993) has convincingly demon-
strated that the setae present in adult phytosei-
id mites are primarily those first added in the
larval stage and that setae added in later stages
ofrelared mitcb are rhosc rhar rend to be ahrerrt in Phyrosciidae. As a result, adulr group wirh nearly 3000 described specia of tiny, worm-likc plant-parasits, irc
phytosciid mites rcscmble immature srages of rheir existing relatives. Other typically abour 200 prn in lmgch and 30-50 p n in diameter, with some species
mesostigmarans, however, mature even mom rapidly than phytoseiid mites (see being as small as 80 pm long (Lindquisr rt aL 1996).
page 48) bur show litde or no indication of rcquenrial progenesis and even phy- Parasitiformans also can be very small. Phytoseiid mircs, those mosr useful
tosciid mites mature at thc normal adulr stage. So, neither neoteny nor progen- of biological control agents, rarely exceed 500 p m in lcngrh and some efficient
esis appears to apply to thesc mites. Perhaps post-displacement (R& 1996), i.e. predators of spider mircs (e.g. Gukdmmur ocridmralir) are less than a quarter of
a form of paedogeneris unrelared m maturation rarcs whrrc the expression of fcn- - .. to be the lower
a millimetrc lona. An adult lenzth of about 200-250 .pm appears
limir in the Mesostigmara bur this is a characteristic size for many cosmopoliran
tures (e.g. addition of setac) is delayed, is a simpler way to account for the loss
of setae in some mesostigmatans. -
soil-liner inhabitanrs such as Rhohcdrur rorrur and I+orouumasell~rnirn. The
latter has been collected at depths of up to 8 m along mesquite roors (Walter &
Ikonen 1989) and, in general, the deeper one samplcs in the mineral soil, the
SIZE, DEVELOPMENTAL KATE A N D smaller and narrowcr the size of the mires thar live there. In hcr, many habitars
GENERATION TIMES will have acarine size ranges char are distinctive.
Although we think of mites as small, size is relativc and the largest mire is more Firmre 4.5 shows rhe body size distribution for 180 species of puasiriform
than one million times the mass o f t h e smallcsr. Mass, metabolism and growth mites from subtropical rainroresr in the Green Mountains section of Lamingron
rate are oFren strongly inter-relared among rhe animals with which we are most National Park in Queenslxnd. Australia. The body lengrh of d ~ smallest
e species,
Familiar (c.g. rhe mouse to elephant curve). In mircs, however, rhese interrela- a phyroseiid mite (240 pm), was used to ser the f~isrograminterval. The num-
rionships are not so simple
in lengrh or greater were rare and consisted
-
. , with increasing size. Mites 2 mm
ber of s~eciesin each inrcrval declines stecplv
of holothyrans (2000 wm),
Overview of mite size patterns three species of ricks (2500-5000 pm) and a numbcr of rrigynaspid mires (to
2866 pm), associared wirh large arrhropods living in logs. Mires collccrcd from
Although smallness is the very essence of being n mire. some mires are noncon- leaves averaged only abour half the length (mean = 349 * 9, range = 240-400
formists. Engorgcd adult female ricks may be thc ri;?e of cherries (2-3 cm). pm) of mires collecred from foresr floor habirats (mean = 709 * 46, range =
Adulw of rhe African gianr red velvcr mires Dinorlmmzbium tincrorum reach
13-16 mm in length (Thor & Wfillmann 1947, Ncwell &Tcvis 1960) andorhcr
velvet, watcr and holorhyrid mites excccd 5 mm. Opilioacariform and early
derivative parasiriforin mires rend to be relatively lnrgc as adults. For example,
adult Australian allothyrid mires are gvpically 2-3 mm in length -larger than
many beetles in chc same foresr litter habirats and much largcr than the avemge
parasitiform mitc inhabiring rainforest lirccr. In live cxrracrions, allothyrid rnitcs
are sometimes covered with acarid hypopi, oribatids and mesosrigmarans rhar
cling to the legs and bodies of these lumbering gianrr.
Acariform mires hold the record for small s i x among terrestrial arthropods.
Soil-litter habitats in hot and cold desens and other dry ccosysrems arc ofmn dorn-
inated by mica less rhm 250 (pm in l e n d in the fmilics Bra~h~chthoniidx,
Tydeidae, Tarsonemi&e, Scutacaridae. Terpnaaridae and Nmorchesridac. For
example, Nnnorchatcr nnrarctim is a tiny, globular, hopping algivore with an aver-
age adult length of 240 @m and a width of 135 (pm. Ir is common throughour
Antarctica, as Far south as the Horlidi Mountains (85"32'S), and can occur at den-
sities of ,2000 pcr rn2 (Block 1979). Many odter cndeostigmatic mires are even
smaller. For example, A~romcrircorallium (Terpnawridac), which was collected in
liner under gum trees in South Africa, has a n adult icngd, of only 1 5 4 1 6 2 p m
and Nnnomhz~wrnrmcIrmir from pasture soil in South Africa measures 149-157
prn hom the tip of the gnachosoma ro the end of the idiosoma and is only 69-75
p m wide. Larvae of thesc tiny mites would be in the 80-120 p m length range -
seemingly near or at the lowcr lirnir for mica. These lowcr limirs also apply to thc
smallest of pamitic mites, such as cheTarsoncmoidea char artach to insect eggs, the
Dernodecidae chat live in the skin parer and ducrs of mammals and the
Eriophyoidw thar cause galls ro form in phocs. The latter. an exrremely diverse
250-5000 pm). Except for ticks, the guild of mires with the largest members
was that associated with arthropods, which includes the largest of all known
Mesostigmata, the Megisthanidae. Some species of Me@sthanw from the tropi-
cal rainforests in Far North Queensland are a whopping 4 mm in length!

Developmental rates and generation times

Given that mites are small and cold-blooded, one might expect them to have
very short generation times, at least given proper temperatures, enough food
and a lack of constraints such as synchronization with host life cycles. As noted
above, some mires have rates of population increase that are second to none
among animals, in part because of their very rapid life cycles. Many plant par-
asites have generation times of less than 10 days and economically important
spider mite pests rypically pass through a generation in 10-14 days during the
growing season (Sabelis 1985). The broad mite Polypl~agotarsonemuslatus, a
tiny tarsonemid (170 x 100 pm) that can cause devastating damage to a num-
ber of economically imporcant plants, probably holds the record. In the sum-
mer, a generation takes only 4-5 days and egg to adult time is only 3 days at
27°C (Hambleron 1938; Jeppson et al. 1975). Another tarsonemoid mite,
Acaropl~enaxmahunkai, parasirises the eggs of mealworms. The female finds an
egg to which she attaches, feeds and swells to more than four times her previ-
ous diameter in about a day. In cultures at 24-26"C, active mite progeny were
visible moving around inside the physogastric mother at 72-96 hours after
parasitism had begun and all had left the dying mother within 120 hours
(Stcinkraus & Cross 1993).
Predatory Mesostigmata also can develop rapidly. At the moderate tem-
peraturc of 25°C the nematode-predatory pachylaelapid Zygoseircr fitrcifer
dcvelops from newly laid egg to adult female in 108 * 4 hours, i.e. it passes
through more than a fifth of i t s developmental time each day. A spider mite
predator, the phytoseiid Pl?ytoseiulw longipes, can complete development in
about 94 hours (Takahashi & Chant 1992). Marrocl~elesmuscaedomesticae, a
predator of flies in chicken dung, is even faster. At its optimum temperature
of 30°C. male M. n~wcaedamesticaeaveraged 66 hours from egg to adult and
females averaged 77 hours (Ho 1985, 1989). Species of Macrorhele~predatory
on fly eggs and nematodes on the surface of a dung pat - an extremely
epherneral resource - have minimum developmental times of 34-5 1 hours at
temperatures of 30°C and above, and mean generation times of four and a half
days (Cicolani 1979, Geden et al. 1990, Ruf 1996).
Daily developmental rates of 10-20% are common among the
Macrochelidae in herbivore dung, the Phytoseiidae on plants and many soil-
inhabiting Mesostigmata (Krana 1983, Sabelis & Janssen 1994, Walter &
Ikonen 1989, Ruf 199G). These mites show a strong response to temperature,
with generation times failing rapidly with increasing temperature (Figure
4.6a). T h e lower and upper limits to this response are related to the normal
habitat of the mite. FOIexample, the small &id Gamasrllodcs vcrmivori is
found in the drier soils of the Great Plains in North America where surface soil
temperatures can rise to over 50°C in the summer (Walter 1987a). Adult mites
will survive for at least a day at 45°C in an incubator but will not lay eggs.
Eggs transferred to this temperature will not develop. The critical upper limit +
 to developmcnr is betwecn 35 and 40°C and the lower limir near 10°C. Dissociation between body size and developn~ental
However, over the 25°C range betwcen &re two exrremes, devclopmenral rate in Mesostigmata
rates increase sharply with rcmpcrarure (I:igurc 4.6b). Zygo~ciusfurcigrrfrom
high elevation meadows (>3,000 m) in the Rocky Mountains has a similar Scaled co-variation between the s i u of organisms and rhcir metabolic processes
rcsponsce: however, the curve is shifted to thc left. At 1O0C,a remperature ar is a well-known phenomenon among animals. For olample, when log membol-
which G. ucnnivornrfails to develop, % . f u r r i p is able to progrts from egg to ic raw is plotted against log body mass, species tcnd to fit a line defined by a 314
adult in 23 days. At 3 0 ° C a suhoptimum rempcracurc for G. vcnnivornx, all power function (the house-to-elephant curve'). Conversely, specific rnctabolic
Zfurcigerdied either during developmenr or ar the :tdulr moult, although thc rare (is. energy consumption per unit body mass) decreases with increasing
h t e r rook only 3 days to reach their final, faral transformarion. -
body size along a -114 curve, so that, . per -
grim of body rnnss, an elephant uses
less energy than a mouse (Schmidt-Nielscn 1984). So, smallcr organisms rend to
However, not all mircs exhibit such rapid developmental patterns. Many 51
parasites are closely tied to their hosts' life cycles and may pass through only n
singlc generation per year. Mites with complicxcd lifc cycles ohen have
- -
have Faster meed lives &an lareer oreanisms and life-hiaorv ,.oararncters d e ~ e n d -
ent on numerous metabolic processes (e.g. developmenral rime) should bc cor-
extended developmental and generation rimcr, as for example the gianr red relared with body siu. This trend should be especially obvious in related species
velvet mites thar prey on descrt-inhabiting termites during the insecrs' irregu- living under similar conditions.
lar nuprid flights (see page 44). However. even givcn similar ecological con- In spite of the generality of the 314 power relarionship (Brown 1995). s i x is
srrainrs, devclopmcntal rates show strong pl~ylogeneticpatrcms, both across nor rhe only arbirer of mewbolic ace. Bats, for uample, tend to live 5-10 c i n u
and within lineages. At tempcrarures where species in somc families or subor- as long as rodenct of similar size (Gwranre 1997). suggesting that phylogeoecic
ders can complctc a generation in less than a weck, others rake two weeks or a history may override physiological inertia. In even smaller organisms, the 314
monrh and, among oribatid mites, n rnonrh or more per insrar may be more power relationship may be irrelevnnr. Recenrly, rhe regularion OF metabolic acciu-
normal. iris of the nematode Gcnorbubdirir &gam has hecn shown ro be under genctic
The suborder Oribarida is a paraphylerir assemblage of over 10 000 control. Muwrions in nematode 'clock' genes srrongly affecr developmcnml rate.
described species distrihured across more thzn 1100 gencra. Thwe mitcs are pace of behaviours and lifespan (Ewbank er aL 1997). Mcsosrignmic n~ircschat
usually parriculare-fccding rnicrobivorcs or saprophzgcs thar retain the full
ancesrral developmental scquencc, although the prelarva is immobile and
remains within rhc egg. However, chis gurtarory and dcvelnpmenral conser-
vatism has nor b c m a barricr co evo1ution;uy success. Even rhe most excreme
rcrrcsrrial habitats, from fro-ren shorcs to hear-blasrcd deserrs, have been
colonired by several lineages of oribnrid mires. In tempcrate to subrropical
forcsrs oribatid mites are oftcn the rnosr sbundanr arrhropods, from rhe lirrer
ro rhe canopy, wirh densiries of renr of thousands to lrundreds of rhousands of
individuals per square metre reporred (Norron 1994, Wzlrer & O'Dowd
1995).
Lirrcr-soil of oribarid mites rend ro bc relatively srahle.
although these mites ohcn have long dcvelopmcnral rimes and rclativcly low
reproductive ourputs. In rhc laboratory ar tempcrarures of 20-30DC, egg to
adulr developmental times of 3-50 weeks are commonly ruporred for oribarid
mitcs frorn rempcrare zone forests. Many species appcar ro be univolrine and
those frorn colder climates clearly havc mulri-year life cycles. Few tropical
species have heen studied bur there is somc indication rllat generation rimes of
one or two months may be more typical (Honciuc 1996). Generally, species
from morc derived lineages appcar ro havc faster devclopmenral rates and,
within a lineage, there appears to he a negative relationship between body size
and dcvelopmenral rate (Norron 1994). Howcvcr, the Axigmara, a derived
group of oribatid mites that have been honoured with their own suborder, typ-
ically have very short gencration times, especially among chose thar exploit
ephemeral habiwrs (OConnor 1994).
 prey on nematodes also seem to be an exception to size-metabolism dometry.
The Mesostigmata are the dominant +up of predatory microarthropods in
spatially and temporally continuous habitats such as soil and leafliner. However,
they are also common in patchier habitats, such as herbivorr dung, rotting h i t
and rotting fungal sporocarps. Some Mesoscigmam are general predators that
- mineral soil by mid-day (aka. 'vertical migration' Whitford ct al. 1981).
develop equally well on a variety of small invertebrate prey but many have a pref-
erence for, or are dependent on, nematodes as a fbod source (Walter c t d 1987.
Wdter & Ikonen 1989).
The subordinal name, Mesostigmata, is derived from the mid-body position
of the openings to the highly branched tracheal system that ramifies through the
body of the mite (Evans 1992). Recently, a model has been p r o p d to explain
the generality of the 314 power relationship based on transport of essential mate-
rials through tubular systems such as blood vessels or arthropod tracheal tubes
(West rt d 1997). Because mesostigmatic mites have a highly branched tracheal
system, the W est et aL model (1997) predicts that they should foIlow the 314
power relationship. However, when developmend rates are p l o d against dry
weights tbr 15 species of Mesostigmata from a variety of grassland soils in
Colorado, no significant slope is generated (Figure 4.7). Although body mass
varies more than an order of magnitude across these 15 species of mites, devel-
opmental rates are much less variable and do not tend to increase with body
mass. Within a genus, developmend rates tend to be similar, irrespective of
body size.
Possibly, the flat distribution of developmend time against body size results
from constraints on exploiting ephemera1 resources, such as nematodes and
other prey whose populations flush in response to irregular desert rains or rot-
ting organic material. Larval LasMsn'us starve in less than a week (Wdter &
Lindquist 1989) but adults survive without prey for many weeks (Walter,
unpublished). Therefore, the selective pressure for rapid development of mites
to addm must be very strong in temporary habitats and may result in the evo-
-. Inmigration
lution of genetic overrides on normal dometric growth. Developmental stages,
however, appear to be genetidy fixed. Although some Mesostigmata have non-
fkding stages, they produce the M ontogenetic sequence of the suborder.
Therefore, strong reductions in body size may be difficult to achieve and increas-
es in developmental rate must occur within developmental stages, rather than by
suppression of developmental stages (Athias-Biche 1987, Chant 1993).
DISPERSAL,MIGRATION AND PHORESY
Movements within and between habitats are important components of any
organism's life history. Movement that maintains an organism within ia usual
home range can be subdivided into a number of categories that relare to its
speed, direction, and purpose; howwu, the ultimate ZCSUlt of these behaviours
is that organisms use the resour- available at a particular site to promote
growth and reproduction ( D i e 1996). In terms of mite movement within
habitats, Eoraging (movement in search of resources) is probably best studied in
the predatory mites used in biological control. Regular back and tbrth move-
ments in response to daily changes in resource availability, predation dangers or
environmend tolerances (e.g. temperature, humidity) are analogous to the daily
mwement of people to and from work or school, and have been termed com-
muting. In desert soils, mies commute into surfice litter in response to rainMl
and also have a daily commute into litter in the early morning and back into
Raaging OUZUIS when an organism leaves its previous habitat patch in search
of new resources and occupies the first suitable new patch it finds. Ranging is one
of the behaviours o h lumped under the term 'disperd. However, the result of
organisms leaving certain habitat patches and arriving at others may be an inten-
sification of aggregation rather than a dispersal of the population (Dingle 1996).
This is gpecially m e when movement is initiated by a decline in r e s o w qual-
ity or the ending of diapause or of a prereproducdve period. If, as is thc case with
many mites, it is an immature stage of an obligatory bisexual species that is 'dis-
persing', then scattering of the population could lead to many b b i i n Ousoes,
each living out their lie marooned on some lonely habitat island One might
expect then that selection would tend to fivour behaviom rhat produced ordered
and predictable movement from one site to another, or migration.
Migratory behaviour occurs when an organism suspends normal feeding,
development -and reproduction and begins expending energy to move from one
place to another. Migration is associated with specific starting and stopping
behaviours and is more persistent and less meandering than normal movement.
Most importantly, a mi-t does not respond to normally important resources
until migratory behaviour has ceased (Dingle 1991). The consequences of
migration can be dispersal of populations, aggxgations or shifts in space with
lide change in density.
Migratory stages
many cases it is not yet possible to distinguish between ranging behaviour and
in mites. For example, spider mites spread rapidly within a plant
because a proportion of newly fertilised adult females will emigrate regardless of
the population density of the natal leaf(Kennedy & Srnitley 1985). These mites
may wak to their new leaves but others cast their htes to the wind. Under high
population levels, deteriorating host plant condition and reduced humidity lev-
els, most spider mites shift from their normal sedentary behaviour, become pho-
topositive, duster on the top of plants and migrate on the wind. Some species
of spider mites in the genera Origonychuz. Eotrrmynbus and Panonychus spin
down fiwm a silken thread and dangle und a breeze snaps the thread and carries
them off (often called ballooning, as in spiders, but different in that the silk is
not reeled out on the wind until life is achieved). However, species of Eho~nychrrr
have a more complicated migratory behaviour. Females, and sometimes nymphs,
cluster at the tips of plants and respond to wind by orienting away from the
source of light, raising their first p& of legs and body surfing on the wind
(Kennedy & Smitley 1985).
Most of the spider mites that have been studied in agricul4 habitats axe
polyphagous. The&re aerial dispersal, although it must involve a high mortali-
ty, is probably a reasonable alternative to remaining on a host plant of declining
quality and increasing number of predators. Inseminated females that are able to
fked on a-rangeof plant hosts should have a chance of bunding new colonies.
However, even the highly host-specific Eriophyoidea migrate passively on the
MITES:ECOLOGY,
EVOLUTION
A N D BEHAVIOUR
wind as adult f d s and this is less easy to understand (Sabelis & Bruin 1996).
In general, eriophyoid mites fcod on perennial hosts and cause relatively minor
damage m the host plant. Most species arc able to manipulate the physiology of
the host to form a gall in which thcy live relatively well protected fiom predators.
Also, on average+eriophyoids are the smallest of all mim and ~IEspecies or even
species-tissue specific pawirer, they arc, therebre, the least W y to encounter a
new suitable host through w i v e dispersal. However, many eriophyoids show
distinct migratory behaviours, including orienting to wind currents using their
caudal lobe to spring wcll above the leaf boundary layer and increasing dispusll
with inarpdng wind speed (Lindquist & Oldfield 1996). They also appear able
to move vast distances in the air and Sufvive the ameme cold and desiccation
associated with long- distance *rial dispersal (Zhao & Amrine 1997).
The instar at which migration omus has a strong phylogenetic component
in mica that is o h correlated with ecology. Most ~ ~ ~ p t i mites b n nmigrate as
adults; how- many Asdgmarta have a deutonymphal stage erpedally modified
fix migration, the hypopus. The deumnymphal stage has been lost in parasitic
and ectocommeflsalAstigmata and movement hom host m host is either by adult
kmales or, in the case of parasites with highly modified d u l ~ by s the b.
Most Prostigmata appear to migrate as adult kmales; however, parasitcngone Lr-
w also disperse on their hosts. Mesostigmata d y migate as either m a d ,
prereproductive adult W e s (most Dermanyssina) or as deutonymphs (Sejina.
Uropodina, Parasitina, Digamasellidae). In the Uropodina, deumnympk may
exhibit a 'normal' and a 'dispersal' fbrm (wandernymphen). HOW-, the larva is
sometimes the dispersing stage in parasitic Mesostigmata (Radovsky 1994).
Phoresy
Migration is a major challenge for any mite not living in a continuous, persist-
ent habitat. Even within such ScUningIy unitbrm and extensive habitats as a for-
est floor, desirable microhabitats may be b and fkr between. Since mites arc
tiny and winglea, movement between resources that are patchy in space or time
may rquirr help. The use of one organism (the carrier) by another (the phom-
ic) for transport is termed phorrsy (fmm the G d 'to and is a common
behaviour among mires, small insects, pwudo~mrpions,molluscs, nematodes
and microbes. Mites are especially adept phorctic and o h have highly modi-
fied phoretic stages (e.g. the astigmatan dewnymph) or phase morphs (e.g.
phoretomorphs in the Hctemstigmata) (Moscr & Cross 1975) (see Chapter 9).
Phoresy begins when normal behavioun and physiological processes stop.
This is especially obviotis in astigmatan deutonymphs - which have no func-
-
tional mouthparts and, with rare exceptions, cannot & d or gmw but is also
true in any phomic individual. Typically, feeding deaeYer and may cease;
development, mating and reproduction arc put on hold; and scuching for a ar-
rier begins. For example, deutonymphs of Parasitus cokoptrvltorum L
(Mesostigrnata, Puwitidac) arc found on g e o q i n e scarab beetles rhrt f i c q m t
herbivore dung. When beetles arrive at a dung pat, the phoretic deutonympk
leave their carrier, moult to adults and rcpmduce. Female I? w&optmmwn can
lay an egg every hour (up to 25 per day) and d d o p m e n t to the deutonymph
is rapid (Costa 1969). N o d y these ~ new deutonymphs would reek out a
bade, migrate to the next pat of fresh d ' k g and repeat the cyde. Howmr, if
deutonymphs do not receive the stimulus of f k h dung, then GO-80% of l?
cokopzmtotym can delay the moult m adult for up to six months (Rapp 1959).
Mites can accidentally wander onto larger organisms and be transported to
new sites but establishment of new populations would then be largely a matter
of luck. Phoretic behaviour is not accidental, although it may have evolved from
less formal associations. Instead, phoreacs go through a sequence of behavioun
that are quite different from non-phoretic individuals. Many of t h s e behaviours
are analogous to those used by parasites to find their hosts (Athias-Binche &
Morand 1993). In a sense, all phorcsy can be considered an exploitation of the
carrier, and therefbrc, parasitic. However, species interactions must be defined in
terms of their ultimate e f ' on the fitness of the participants if thcy arc to
makt any ecological or evoludoaary sense.
i ~ ~ has been difkentiatd from parasitism by quiring the
T n d t i o ~ a lphoresy
phorctic to enter a state of cliapuse and not fked on thc host (Athias-Biiche &
Morand 1993). Howcvcr, any inmacdon beweem individuals of rrvo species that
benefits one but causes a duction in the net fitness of the other is parasitic. A
phoretic does not need to fked on a carrier to cause it harm, as has been shown fbr
southern pine beeda that am weighed down with myocs of umpodid mites (Kinn
& W~tcosky1978) or fliesso encumbered with hypopi (J%inga & Broct 1988) or
ereynead tritonymphs (Zhang & Sanderson 1993) that they are unable to fly.
Also, being fed upon does not necessarily reduce the fitness of a carrier. For exam-
ple, parrald beedes seem m s& no ill effiwrs from the hordes of large maostig-
r n v that fbrageon their bodies. More importantly, a phomic that causes no
harm to a carrier in flight may devastate the carrier's brood (Eickwort 1994). Some
asqxiations traditionally considered phoredc arc dearly parasitic or appear to be
evolving towards negative effbcts on the carriers (Houck 1994). These,and other
miu-carrier relationships, will be considered in more detail in Chapter 9. For now,
the point that we wish to cmphasise is that the changes in behaviour a'ssociated
with phomsy indicate that it is a form of migration (Dingle 1990, imspoaive of
the proximate or ultimate effZxxs on the fimess of the carrier.
SUMMARY
Mites may make medioae mothers but they are masters of ontogenetic manip-
ulation. The basic acarine developmend pattern of egg, prdama, larva,
protonymph, deutonymph, uitonymph has resulted fiom suppressions of
ancestral stages at both ends of postembryonic development. In terrestrial che-
literates, the planktonic inscars of marine ancestors either have been lost or
appear as poorly formed foetal cuticles. The first post-egg stage subsists on ran-
nants of yolk and has incompletely formed mouthparts and limbs. In most
arachnids this J1 nymph is dependent on protection fiom the mother until it
has moulted into the J2 nymph that is capable of hunting and fesdiag but in
mius this stage (called the p k ) is ephemeral, usually immobile and ofkn
featureless, and it may be completely suppressed. Mite lamc (J2 nymphs)
actively fsed ercept in a few derived lineages where feeding is fidtaave or
absent. Nymphal instars beyond the uitonymph and pst-adult moults arc
known in only a few, derived mite taxa and appear to represent means of repair-
ing cuticle or increasing body sire, rather than being retained a n d stages.
 M r r s s : ECOLOGY,
EVOLUTIONA N D B E H A V I O U R

I Suppression of one or more nymphal instars and accelerated development

are recurrent themes in the evolution of the Acari. Many oribatid mites, howev-
er, are able to maintain high population levels and a ubiquitous distribution
SEX A N
while encumbered with the full developmental sequence. Within the Astigrnata,
a derived lineage of oribatid mites, the deutonymph is a non-feeding dispersal
stage that may be fgcultatively or completely suppressed. A number of highly TRA
diverse and successful mite lineages in both the Parasitiformes and Acariformes
are characterised by terminal truncation of nymphal instars, very rapid develop-
m e n d rates and extraordinary rates of population increase. T h e Parasitengona
56 have followed a third route to evolutionary success through parasitism of verte-
brates and arthropods as larvae and by alternating active, predatory stages with
inactive, hidden stages that occur within the cuticle of the previous stage. The
ultimate in the abbreviated approach to life occurs in the Heterostigmata, where
grotesquely swollen adult females give birth to fully formed and already mated
.
adult offs~rine.
2
'

Although the majority of mites are minute, adult body lengrhs vary from
80 p n in some plant parasites to 30 000 pm in engorged ticks and biovolumes
vary by about 6 orders of magnitude. Within a group of closely related mites
with similar ecological constraints, life-history parameters, such as clutch size,
developmental rate .and generation time, are ushally positively related to body
size. However, phylogenetic constraints on physiological processes are obvious
throughout the Acari, with some lineages, such as the Oribatida, charaaerised
by long generation times and low rates of increase. Others such as Mamrbchs
have extraordinarily short generation times and high rates of increase. The most
rapidly developing acariformans are in the Tarsonemina where some parasites of
plants and of insects are able to complete development in about 3 days at mod-
erate temperatures. In the Parasitiformes, similar developmental rates are found
among the dermanyssines. These mites marure only a single large egg at a time,
irrespective of body size or ecological role, and developmental rates show no lin-
ear relationship to body size.
Mites are small and wingless but they are abundant in many patchily dis-
tributed resources. Some mites take to the wind directly bur the primary mech-
anism that mites use to travel from one resource patch to another is phoresy, i.e.
hitching rides on larger organisms. Phoresy is a form of migration and, like any
migrant, a phoretic mite behaves quite differently from a non-migrant. Phoretic
mites search for a carrier rather than food, attach to some part of that carrier,
enter a period of altered behaviour (e.g. inactivity or parasitic feeding) and
depart from the carrier at the appropriate time in a new habitat. The phoretic
relationship may be mutually beneficial to the mite and the
carrier, neutral or result in a loss of fitness to the carrier.

I
n our everyday experience, animals have two scparatc sexes. Some animals.
and many plants, combine the rwo in a single individual but they still pro-
duce ~MIC and M e gametes. This i s such a basic generality that we become
uneasy with the suggestion that there are many ran (some of them mites, see
page 87) in which males arc irrelevant.
What do we mean when we say that it is 'normal' to .have two sexes?
Fundamentally, ficmales arc individuah that produce krge gametes that are well-
stocked with tbod ( = ova)and males produce lean, minimalistic gamete (= spa-
matozoa). Having g a m e of different sizes - anisogamy - is the rule in
multicellular plana and animals (Parker 1982). In contxast, many fungi under-
go sexual reproduction by the fusion of q d - s t a d gametes - isogamy (Raven
et aL 1981). Some protozoans exhibit isogamy while others arc anisogarhousand
these states may di&r between congeneric species. Although the two types of
gametes are very difkcnt in size in most plants and animals, in protozoans the
size &rences range fiom slight to very marked (Schmidt & Ebbem 1985). As
anisogamy pr& in more derived tam,whiie isogamy seems restricted to more
ancestral groups of organisms, it is assumed that isogamy is the primitive state.
One of the basic precepts in ecologid and evolutionary theory is that
resourcxs fbr any endeavour are l i d If one makes lagex gametes, then one
must also make fewer. If one makes smaller gametes, the result is more of them.
This is another charaaeristic of anisogamous o+ims; Lrnala ~ r o d u afew
h e ) gametes and males produce many (small) ones. Although some u n i d u -
kt organisms cg. certain Chlamydawlllu) have fIagcllaced male and M e
i
gametes (Raven ct aL 1981), in the vast majority of aniso&amous taxa, mde
&metes are mode and M e gametes are sedentary.
So compared to spermatozoa, ova ace large, rare and immobile. The small.
active sperm vastly oumurnbu the cells with which they desire union. As only
one sperm can partna any given egg (with rare exceptions), ova as a resource are
in short supply. The aggressive con- between male mountain sheep, elk and
elephant seals for accessto females are simply the ourward manilktation of their
spum battling fbr acccss to eggs. Similarly, mala may compete for female a m -
tion by displaying flashy good looks or strenuous dan- Damin (1871)
termed the two types of competition in& and i n d , respeerivelp
and suggcstd &sexual selecdon was responsible fbr many extra-t male
characteristics (see page 75).
Parker (1970) pointed out that an even more basic l a d of in& com-
bat occurs bemeen male gametes competing fbr a limited egg resou~oc;he
termed this sperm competition. Sperm compedtion is probably a smng fbrce
selecting for and maintaining the small size of male gametes (Parka 1982) and
it has probably played a vital role in the origin of internal spum transfer.
MODES O F SPERM TRANSFER
Animal lifi cvolvd in the sea and it is among marine animals that we 6nd the
greatest variety of sperm transfer mechanisms. To understand how the diversity
of mating behaviours arose in mites it is helpful to consider evolutionary trends
in sperm transfer.
There is a g e n d belief that the ancestral state of sperm transfer in animals
involved external fertilisation with freely spawned sperm and eggs (eg. Parker
1978, 1984; rdcrences in Rouse & Fitzhugh 1994). Free-spawning without
dose contact between the sexes occurs in many extant aquatic taxa, both inver-
tebrate (e.g. many annelids and echinoderms) and vettcbtatc (many fish). In
such situations, sperm competition is the only competirive interaction between
males and the only way to 'win' is to produce enormous clouds of sperm. Yund
aad McMartney (1994) have demo&ted that inuasexd cornperkon for kr-
dlisations occurs in k s p a w n i n g ascidians and bryozoans. Another feature
associated with free-spawning is e e t e dilution, which sometimes results in a
high proportion of eggs going udertilised (c.g. Lcviran ct aL 1992). Parker
(1970, 1984) proposed that inaasatual selection favours males that both avoid
excessive expendim on gametes and fercilise a greater proportion of a bale's
dutch by shedding sperm only when in close proximity to a female. Although
Parker focussed on benefits of dose association to the male, pairing to spawn
benefits both male and female, as the latter may gain a higher proportion of Lr-
-
tilised eggs. Parker suggested that copulation placement of sperm by a male
into the receiving structure of a female (Hinton 1964) - evolved fiom broad-
cast spawning by progressive steps, driven by inrrasexuai selection. This scenario
is no doubt aue for mecazoan animals as a whole, although the primitive nature
of broadcast spawning is in doubt h r some groups in which more direct brms
of transkr may be ancestral (Buckland-Nidu & Scheltcma 1995, Rouse &
Fitzhugh 1994). Regardless of which came first, it is dear that some animal taxa
display a greater diversity of s p e r m - d e r modes than other. Mites, of coune,
are near the top of the list.
Distribution of sperm-transfer modes among
non-acarine animals
The ways in which gametes gec together can be classified on the basis of where
the gametes are when they meet and how much concaa there is between male
and &male. External ferrilisation involves the release of gametes by both sexes,
fbllowed by fereilisation. Males and M e s may be paired during this activity
(eg fiogs, many fish) or they may be distant (c.g. many marine invertebrates).
fimihdon reauires an aaueous or at least venr moist habitat to allow
sperm to reach and pene&te eggs. &ong anant che&ates, external f rtiIisa-
tion with pairing is resmctcd to the marine horseshoe crabs and pycnogonids
(Pnxxor 1998). Some argue that the atha eurypterids also had external fertil-
isation (Boucot 1990); however, Braddy & Dunlop (1997) suggcst that f k d -
sation may have been internal, fbllowing a scorpion-like pairing dance.
Internal fcrtilisation involves ftrdlisation of eggs while they are still in the
fkmae. Although internal fcrtilisation was probably a prerequisite fbr successful
invasion of dry land by animals, it has evolved many times in aquatic habitats
(Proctor 1998). Retention of ibdiscd eggs - - by
.
the female, brooding, ocnrrs in
-
many species s c a d through otherwise externally fedking marine taxa (eg.
echinoderms, David & Mooi 1990). Males of these raxa seldom show modifica-
tions for direct insemination, suggesting that females 'suck up' fieely spawned
sperm and use them to fenilise their eggs internally. Thus a P a r k profess of
increasing proximity of male and fmalc at time of spawning, followed by the
b a l e ' s decision to brood her eggs, may be the evolutionary scenario associated

with the repeated evolution of direct sperm transfer. AU arachnids, including
mites, have internally f e d i eggs.
Being human, we tend to fed that our way, copulation, is the only proper
way for sperm to get inside a female; however, mates and females of other inter-
nally f e d k i n g raxa are not so fixated on closeness. There are numerous dassifi-
cations of sperm-transfer modes based on the degree of contacc beween the
sexes (cg. Alexander 1964. Schaller 1971, W w l d t 1969). Here we use the
four categories oudined by Proctor (1998). Direct Uor copulation
involves the greatest degree of contact and occurs when the male places his
3 sperm on or in the sperm-receiving structure of a W e . One reason we con-
sider copulation to be 'normal' is that the land animals we are most W i i with
all transfix sperm direcdy. All amniote vertebrates (reptiles, b i i manun&)
transfer sperm directly, as do all spiders and all winged inseas, and a large num-
ber of other groups including onychophorans, leeches, flatworms and nema-
todes. In these taxa, sperm may be transferred in a liquid medium (eg.amniotes,
most spiders and insects) or bound up together in a cohesive packet called a
spennatophore(e.g. many insects, a few spiders) (Mann 1984). Among arach-
nids, all species of the Solifbgae, Ricinulei. Opiliones and Araneae transfer
sperm through copulation.
Mala need not place sperm dirmly in the female's genital opening.
Depending on the species, male onychophorans may place semen or sper-
matophores in the genital opening of their mate, or somewhere else on her body
where lytic enzymes in the spcrmatophore break down her epidermis to release
sperm into her haemowel (Eit & Briscoe 1990). Another sort of traumatic, or
hypodermic, insemination occurs in bedbugs (Hemiptua) in which the d c
pierces the female's integument with his sharp aedeagus. Although traumatic
insemination has not been reported in mites, it seems likely that ancestors of
some acarine raxa did engage in this rather rough fbrm of sperm uansfer (see
p w 85).
Pairing with indirect tram& occurs when a male pairs with a particular
female but does not introduce sperm into her. ~ a t h &he dep& a spet-
matophore on a nearby substrate and attempts to induce her to take the sperm
from it. The most Earnous of paired-indirect taxa are scorpions, which engage in
a pas-rir-dnuc or mating dance prior to sperm deposition. All Arnblypygi,
Uropygi and Schiimida pair, dance or promenade, and indirectly transfer
sperm via ofien very complex spermat~~hores, as do some spec& of pseu-
doscorpions (rekrences in Proaor 1998). Salamanders and n e w (Arnphibia:
Urodela) also typically show pairing with indirect transfer of spermatophores
(eg. Arnold 1976). as do some hcxapods and myriapods (Proctor 1998).
UnDaired, or dissociated,merm transkr occurs when malesdo not court a oar-
ticular o ales of taxa shbwing incornplat dissodation must chemicaUi or
d y contact a fimale prior to depositing a specmatophore but do not direct
their intentions toward any one i'cmalc. Complete dissodation appears the most
unlikdy fbrm of nansfk to us, as males and kmales need never conraa each other,
even chemically, fbr successful deposition and uptake of sperm. Attraction of
fimaes to the ejaculates is mediated by a variety of chemical and stcucnual mod-
ifications of the spermatophores (Proctor 1998). D i a a o n is the mode of
choice for many pseudoscorpions and springtails (Collembola).
SEX & CELIBACY
DIVERSITY O F SPERM-TRANSFER BEHAVIOURS
IN MITES
So where do mites fit in this scheme of transfer modes?They fit &ere. In
ha,mites show the greatest diversity of spcrm aanskr behaviours of any group
of arthropods. In the tbllowing section we take you on a brief tour through the
acarine Kama S u m
Reproductive anatomy
Befbre surveying sperm-transfer behaviour in mites, it is useful to know some-
thing of their reproductive anatomy. Much of the following discussion comes
fiom Krana (1978) and Evans (1992). Primary genital opadngs are those
fiom which sunen or spermatophoces (in males) or eggs (in females) exit the
body of the individual. In many mite raxa, W e s have secondarp genital
openings (variously termed sperm induction pores, copulatory pores, solenos-
tomes, etc.) into which males introduce sperm. These will be discussed in the
appropriate taxonomic seaions below. 1n-females, there may be a temporary
sperm-storage structure (a speamdaeca or s e m i d receptacle) near the wpu-
lacory opening (Alberti & Crooker 1985, Nuzzaci & Alberti 1996).
Spcrmathecac are not as common in mites as they are in insects.
In inseas, krtilisation of eggs typically occurs when eggs pass by the open-
ing of the spermatheca and the female squeezes out a small dollop of sperm.
Although some female ins#= (e.g. social Hymenoptera) can store sperm fbr
long periods, oviposition usually occurs quite soon &er sperm trans&, ofien
while the male mate is still present In most mites, fertilisation appears to occur
in the ovary after sperm has migrated there (Feicrrag-Koppen & Pijnackcr
1985); however, some taxa with spennathecac may k d k e eggs in an insect-like
W o n (Nuzzaa & Alberti 1996).
Oviposition in mites seldom occurs immediately after sperm transfer; it may
be days, weeks or months afterwards. The general lack of a spermatheca and the
temporal separation between sperm transfer and oviposition in mites means that
certain phenomena common in insects (e.g. i n t e d manipulation of stored
sperm and post-copulatory guarding by males, Thornhill & Alcock 1983) are
seldom observed in the Acari.
The ovaries of female mites may be single, paired or a grape-like duster of
lobes. There are typically paired oviducts regardless of rhe type of ovary, sug-
gesting that the original state is paired ovaries. Egg may be m a d one at a
time, as small clutches or as very large clutches of thousands of ova (see Chapter
4). Ejmusible ovipositors are present in some mites.
In male mites, testes. Likc ovaries, may be single, p a i d or form grape-lii
dusten and vasa dekrentia are usually paired. Acarine spermatozoa lack the
propelling flagellum we tend to consider the hallmark of sperm. Aflagcllate
sperm also occur in the Opiliones, Palpigadi and Soligae, while the remain-
ing groups of arachnids have Bagcllated sperm.
Alberti (1995) summarises the huge morphological variety in arachnid, and
especially acarine, sperm cells. Two major subdivisions of mites can be recog-
nised on the basis of sperm structure: the Opilioacarida, Holothyrida, kodida
and Mesostigmata have elongate spermatozoa; the Prostigmata, Astigmata and
Oribatida have more globular sperm cells. The size range of sperm cells is
enormous, from less than 2 p m in the prostigmatan Nicolerielh lrirea
(Labidoston~matidae)to 1000 p m in the tick Orrzithodorzr rholouzni(Argasidae)
(Alberti 1995). Kadwan (1996) found that size of spermatozoa varies between
individual males in the asugmatan Rhiwg~phurrobinii (Acaridae).
Sperm cells arc often transferred to the female in an inactivated state but,
once in the milieu of the female reproductive tract, they become capacitated.
Capacitation involves changes in the morphology, physiology a n d behaviour of
spermatozoa and is widespread among animals. However, this process is partic-
ularly spectacular in ticks in which the sperm cells double in length during
capacitation, undergo complete reorganisation and become capable of a creep-
ing locomotion (Oliver 1982, Sonenshine 1991).
Males of most specics of mites have accessory glands near the junction of the
vasa deferentia that secrete various products that are incorporated into the ejac-
ulate. Many acariformans produce spermatophores and the ejaculatory duct is
often modified into an array of internal sclerites and muscles, termed the ejacu-
latory c o m p l a , that plays a role in shaping the spermatophore. Barr (1972)
considered the morphology of the ejaculatory complex t o be phylogenetically
informative within water mites. Among mites that copulate, it is the rare specics
that transfers sperm directly from the male's primary genital opening to the
female's. Rather, various parts of the male's body may be modified for sperm
transfer; these are described below for particular taxa.
The Parasitiformes: elaborations o n a theme
As far as is known, all bisexual parasitiformans copulate, with males using tlicir
chelicerae to transfer sperm to the female's copulatory opening. Ticks and early
derivative mesostigmatans (e.g. Uropodina, Sejina and Trigynaspida) share a
similar method of direct transfer (Evans 1992, Walter unpublished). Males
extrude flask-shaped o r globular spermatophores from their genital openings,
which are typically l o u t e d between o r behind the coxae of their second pair of
legs. T h e male then flexes his gnathosoma ventrally and extends one of his
chelate chelicerae towards the 'neck' o f the spermatophore. Depending on the
taxon, the palps andlor the first pair o f legs are used to help remove the sper-
matophore froni the genital opening. In the Uropodina and Sejina, there are no
obvious modifications of appendages for spermatophore manipulation but some
Trigynaspida have modified sternal setae or ridges that may aid sperm transfer.
Males in the mesostigmaran group Parasitina have chelicene that are modi-
fied to receive the s p ~ r m a t o ~ h o r eEach
. chelicen has an opening, o r sperma-
totreme, o n the lower movable digit. It appears that ar the very beginning of
spermatophore extrusion, the male places a chelicera over his genital opening.
T h e spermatophore casing is extruded through the spermatotreme in its wl-
lapsed state, then filled with sperm a n d accessory gland products so that the
spermatorreme ends u p holding the balloon-like spermatophore by a narrow
neck. Male parasitines have genical openings much closer to t h e anterior of the
sternal shield. This allows uprake o f the ejaculate without the extreme ventral
flexion of the gnathosoma seen in taxa with more posterior openings.
Convergent displacements of the male genital opening (derived from Segment
VIII) to the base of the tritosternum (Segment 111) are found in Sejina, some
Antennophorina and the Dermanyssina.
Figure 5.1
Chei~ceraeof %Q rnaie derrnanyss~nernltes (ios~oserussp .Asc~daeand Dendro~oeiosprssp..
D~gamasell~dae)
rhowmg rhe finger-i~kesperrnatodacryls
Mating behaviour in the uropodinc mite C~:11)~zinrlkzper~pI10)~? is
interesting and mysterious. Females of this semi-aquatic mesostigmatan often
bear a ring of :~morphousmaterial arouncl their opisthosomac, connected to a sac
of similar material resting o n their dorsums. T h e origin and firnction of this
'signet ring' was unclcar until Cornpton & Kranrz (1978) observed their repro-
ductive behaviour. Prior to sperm transfer, the nlale mounts the female and hcer
the opposite way. T h e female produces a mass of 'ring' material froni under her
genital shield.Thc rrlalc then moves posteriorly and ventrally so that hc is beneath
her facing the same direction. H e chcn presses a sperrnatophore directly from his
genital opening into the amorphous material near her anal opening. T h e sper-
rnatophore is errvclopcd in the marcri:d and somehow a hollow tuhc h r m s in t l ~ c
material leading from the spermatophore 10the female's gmital shield. Compton
& Krantz sugg~stthat sperm travels from the spermatophore to the fesnalc's gen-
iral operling at this point. T h e male returns to his original position and uses his
legs to rnanipulatc the still-extruding ring material along the sides of rhc fernale
u p onto her dorsurn. T h e material eventually hardens to form a ciouble-chant-
hered cell on the rcmrde's back. Compton and Kmnm feel that the embedding of
the spcrmarophore in the ring material is an adaptation to prevent water damage
to the ejaculate. However, they could offer no use for the doublr-chamhcred
dorsal sac, nor for the male's involvement in its construction.
?ivo groups of nirsostigmatans other than rhe Parasitina have chclicerae
modified for sperm transfer, the Dern~anyssinaand the Heterozerconina (I'.vans
1992). Dermanyssine males sport an often elaborate, species-specific outgrowth
o n the movable digit of each chelicera that is termed a ~ ~ e r m a t o d a c t (Figure
yl
5.1). In some t.wa, tnales produce spermatophorcs with distinct casings (e.g.
Rhodacaridae, Lee 1974), while others extrude seminal droplets frorri their gen-
ital openings (e.g. Macrochelidae, Krann. 8c Wernz 1979). Some specics of this
group show the ancestral mode of sperm uptake by males, in which rhe che-
licerac are flexed ventrally to contact the ejaculate (e.g. Ologarnasidac, Kranrz
1978). A niore derived behaviour is shown by the Macrochelidae. T h e male
extrudes a tubular extension of the genital chamber tow:lrds the chcliccr~eand
 produces a droplet of seminal fluid (Krana& Wemz 1979). The male dips the
arthrodia brush (located at the junction of the fixed and movable digits) of one
cheliccra into the fluid, presumably mopping it up. He then apposes the arthro-
dial brush of that chelicua to the groove in the spermatodactyl of the opposite
chclicera, where the seminal fluid is transferred to the cheli@.tip by capillary
aaion. Among the Heterozerronina. the Discozcmnidae ha%ca cheliceral sauc-
ture that resembles a spermatodactyl, while the Heterozerconi&6 have a spiral
canal on the fixed digit that presumably conducts sperm (mating &s not been
described in either group). - ._
In the kGodida and many early derivative m e s o ~ t a n sthe , male trans&
sperm into thc female's primary genital opening. This is turned muqermy,
where t o h r& to 'bringing brth young'. In ticks, although che siu of insem-
ination on the f;cmak is invariant, the location of mating di&s between the two
major hnilies. In the Argasidae, which tend to spend lide rime on the host, sperm
dtakes place in resting sites-away .
fiom the hosr, in those M d a e which
have more lengthy associations with
their food sourccs, mating occurs on
the host's body (Yuval1994). Assembly
pheromones arc produced in some
species to fkilitate congregation for
m a ~ andg may amaa potential mates
to a currcndy parasitised host (e.g.
Rechav et d 1997).
In contrast to the above parasiti-
bm tars, male Dermanyssina transfer
spurn to a secondary genital opening
in the female. Although sperm transfer
has not been observed in the
Heterozerconina, Evans (1992) sug-
gests that transfer is also to a secondary
opening. Female dermanyssines typi-
cally have a secondary genital opening
in the unsderotised membrane at the
base of their third pair of legs. In the
Rhodarnidea,, however, these openings may be on or near the bases of their
fourth pair of legs, on ventral shields posterior to their f$urth pair, or even on
the trochanters and femora of their third pair (Figure 5.2). The proximity of the
secondary openings to legs has resulted in this form of transfix being termed
podospermy. A more general term fbr insemination via a secondary genital,
opening, regardless of its location on the kmalc, is porwpumy (Evans 1992).
Dcrrnanyssine finales have two types of podospernd systems. In the lae-
lapid type, tubes fiom each opening meet i n t d y at a sac in which sperm
appears to be s t o d In the phytoseiid type,there is no median merger of tubes
and sperm is stored in a sac near the base of each secondary genital opening-The
sperm cells of dermanyssines and to some extent, the parasitines, are modiicd
into ribbon-like structures; Aiberti (1995) hypothesises that the altered shape is
an adaptation to the journey the sperm must make once inside a female.
Whereas in ticks the spermatozoa move up the oviducts into the ovary where kt-
tilisation rakes place, in the parasitiform taxa with ribbon sperm it appears that
spermatozoa migrate through the h a e m o d and penetrate the walls of the o ~ t y
to gain accas to the ova within. Albecti (1995) m ts that the wall-penea;lt-
ing abiity of parasitine sperm allowed the evolution of the podospermal
insemination system of dermanyssines.
T h e sperm-transfer behaviour of. the Phpsciidae, the best-studied der-
rnanyssine- W y , indudes two basic pre-pulatory bchaviours (Amano &
Chant 1978, Schultcn 1985). In one type, shown by Arnbiyciu~and
Typhlo&mus species, the male climbs onto the back of the Lmale so that both
mites are f%ng in the same dimdon. The male then turns 180" and moves pos-
terior£~ and under the &male, ending up venter-to-venter with her facing in the
same direction. The other cype is shown by P&seiulus species where the male
first contacts the fknde 'head-to-head' and then flips over on his dorsum and
crawls beneath her, ending up in die same final position as in the fiat type.
Insemination occurs when the male phytoseiid introduces the spermato-
dactyl of a cheliccra into one of the female's copulatory pores (located between
the third and bur& coxae). It appears that a small, flask-shapedspermatophore
is held between the chelicerae and s q u d so that its contents arc channelled
into the copulatory pore along a pave in the spermatodacryi. The spermathe-
ca associated with that pore swells and, widin a fkw minutcs, a wall-likc struc-
ture appears to krm around the uanskrred ejaculate. Once 6 d , this wall
remains for a few days; so multiple inseminations are detectable by the presence
of more than one of these structures in the spermathem These objects arc often
referred to as 'endospermatophorcs' and the flask-like hull that remains in the
male's chelicerae, the 'ectospermatophore'. However, as the membrane sur-
rounding the sperm mass in thc spermatheca appears to be constructed after
d r , perhaps through some chemical i n t d o n between male and h a l e
fluids, 'endospermatophore' is a misleading name. Ttue endo- ar.d ectosper-
matophores are present in the ejaculates of the Ixodida (see page 73).
Lee (1974) describes and illustrates mating in a number of genera of
Rhodacaroid~As these mires also belong to the Dermanyssina, males have
spermatodaayh and f d e s have semndary copulatory pores. Lee observed a
peculiar behaviour in malcs of Eucpim'us jilamcntosus, Glulfl~seIIustmghardi,
Antunnolaclaps ammmae and AthinrcIla dcnurur Prior to extrusion of the spa-
matophore from the male's genital opening, he appeared to insert his chelicetae
beneath the epigynd shield and move them 'in and out alternately as if f d n g
on her genital region'. This is runinisccnt of the behaviour of a&, in which
males probe the f;cmae gonopore with their mouthparts (Feldman-Muhsam
1986). Males may probe the genital opening of an allospecific female but they
do not go on to anrude a spumatophore. Presumably in both tht rhodacarids
and ticks there are species-spefit;~chemicals in thc genital opening that males
sense with chem~r&~rnrs on their mouthpam.
Lec sates chat k 'tasting' rhe fEmale's genitalia, the male errtrudes a large
spumarophore about the size of the male's sternum, hence approximately 114 to
113 of the male's body length. Lee separated a male and w e Athiau& dmtata
&re mating was completed and noted that the neck of the Hask-like spu-
matophore was held betwecn the digits of one chelicera. In E t + c r i u s ~ t o n ~ r ,
the male inserted the tips of both of hi spermatodactyis simultaneously into one the huge female and shoves so violently as to turn her over. This is strangely sim-
of the fbale's copulatory porn (at the base of the fourth coxa). The sper- ilar to the behaviour of male springtails in the p u s Hetrrominthrm*r
matophorc shrank as the wntens appeared to be directed into the pore. (Collemboh Sminthuridae) in which the male inserts and rubs his forehead
N k w d s the male consumed the remainder of the spermatophore's contents and setae in the genital opening of che female (Bredild 1970). The r o s d spines
disgtrled the casing. This sequence of behaviours was simibr in the other spacies present on males,ofa Syrnbiotibll~sspecies (Symbioribatidae) from Queensland
he observtd, with males inseminating only one of the two copulatory pores. In rainforests (Figure 5.3) may indicate that this species a h engages in such geni-
contrast, Rath et aL (1991) suggest that male Tmpilae&ps c b u c (Laclapidac) ' tal stimulation.
inseminate both copulatory pores during a single mating. W+ (1394) also No other interactions were observed for E szucta but S c h w described
noted that male T &me move from the lcfi to the right side of the female during additional odd behaviour for C.ggdntea Afccr the pairing march proctods tbr
mating and added the observation that this movement is inurspuscd with bouts some time, the male moves tiom behind the b a l e to in front of her. There he 67
of stroking, in which the male rapidly runs his second leg over the epigynial are;l leans forward to balance on his first three pairs of legs with his fourth pair and his
Scvua hundred times. Pethaps the stroking s t i m k the female to take in sperm opisthosorna raked high off rhe substrate. He cmudes his spennatophoric organ
h m the spermamphore. In Phytoseiidac and Ascidae (Laziosn'~~()), the fkquency and deposits a droplet (presumablyof sunen) on his apposed fourth legs. He then
of copulations often appears to be a species-id characteristic Inseminated presents his raised fburth lcgs to the
L d e s of some spesies have only a single endospermatophore, while others may M e , who nibbles at them. During
carry eight or more in each specmatheca (Walter, unpublished). this the male taps his hind legs up to
48 times with his spermatophoric
The adventurous Acariformes o w Schuster supposed that sperm
Diversity of sperm-uansfcr modes is not uniformly distributed among b i i transfer occurred sometime after
Acuiforrnes. Within the Sarcoptiformes, asdgmatans invariably mpulate, while this display, but did not observe it.
oribatids display the opposite tendency and most have dissociated transk. It is As he saw no &standing sper-
in the Prostigmata that the greatest diversity of cranster modes Lies, although matophores in the mites' containers.
again, some groups are monocypic (eg. the Tetranychoidca. Raphithoidea, it seems likcIy that a form of direct
Cheyletoidea and Tarsonemina all transfer sperm directly with sclerotised intro- d r occurs in C gigantea
mittent orgins). In those groups that do show variation (e.g. the Parasitengona), The best evidence of (almost)
it is possible to test hypotheses about evolutionary factors that lead to changes direct trans& in an oribatid mite
in sperm-transfix mode. For example, Wirte (1984) suggested that the evolurion has been observed in a species of
of swimming by s d lineages of water mites (Hydracarina) selected for direct Pirog&mmz (Galumnidae) (Esaada-
sperm transfer because of the reduced probability of fktnales contacting sper- V'cgas et aL 1996). L i i C.&an-
matophores deposited on a substrate. Proctor (1991a) tested this idea using a cca and E. enrctrr, a male of thii
comparative approach and bund that copulation had evolved more often than svecies initiates interactions with
expected in swimming water mites than in crawling ones. The Tydeidae dso &e l q e r f k d e by pushing hi ros-
exhibit variation in transfer modes (dissociated, Schuster & Schuscer 1970; trum beneath her body but, in
direct, Knop 1985) and may also be an appropriate taxon for comparative analy- Pilogdum~,the male deliberately
st. Below we survey the sperm-transfer modes of the Acariformes by suborder. tips the h a l e on her side and then .,..
--
apposes his venter against hers. The
male maudes a mass of material
Many hundrcds of spedes of oribatids ate parthenogenetic, and never produce from his genital opening that acaues on the female's venter. The mass is about
funcrional male o&pring. k u a l species typically show diaociated sperm mans- 40% of h e female's body length and so must represent a large expenditure of
fix in which males readily deposit stalked spermatophorcs in the absence of energy on the male's part The &male. moves the ejaculate into her genital open-
f d e s . M e s have a complex of amusive sclerites 4 to shape the sper- ing with her legs. As the authors point our, deposition of spermatophores on the
matophoe that is sometimes termed che 'spermat~~horic organ'. There am a t;w bodies of L d e s is a rare behaviour among archropob, although it occurs in
taxa in which the= appears to be a doser pairing between the sexes but in which some crustaceans, and is common in onychophoransand I d e s . The behaviour
sperm transfer has not been observed. The male Emgalurnma anrctcr of the water mite Phpoolimnesiaa& (Limncsiidae) may be similar in that the
(Galumnidae) walks behind the female with his prodorsum beneath her opistho- male appears to deposit a sperm mass on the funae's dotsutn (Procror 1997).
soma and first pair of legs on her posterior (Evans 1992), as does the male Because the males of these mite species do not put sperm in the female's sperm-
CoIlohmanniagiganrca(Collohmanniidae) (Schuster 1962). In the latter species, receiving m a w e , this type of behaviour falls between the direct and paired-
the small male occasionally places hi rostrum against the anogcnital region of indimx categories defined above.
 I-female situarion), whcrcas nmlc A. siro consistently produced about 25 sper-
niatophores regardless of the number of females. For both species, the female
There is little doubt that the Astigmata evolved within the Oribatida (Norton et may initiate mating. The authors observcd that a female would follow the trail
aL 19931, so the 'Oribatida' in the broad sense approach water mites in diversity of a male around the observation chamber but it was not until the opisthosoma
of transfer modes. Although oribatids s e m stri%almost always show dissocia;- of the female came close to the male's gnathosoma that he would show interest.
ed sperm transfer with a f& examples of pairing, astigmatans invariably copulate. This suggests a localised release of pheromone on the female's part. Similarly,
Not only do male astigmatans transfer sperm directly, they do so with a sclero-
putring a female in a crowded chamber ofrcn caused males ro arternpr ro mace
tised intromittent organ rypically termed an aedeagus (morphology described by
with each other.
Walzl 1991). Presumably the astigmatans evolved from a group of oribacids that
68 had dose pairing between the sexes during sperm transfer; however, it has been (c) Prostignata
suggested that they are derived from a lineage of oribatids (see
The task of sumniarising mating behaviour in the Prostigrnata is daunting because
page 91). In either case, the aedeagus is an aucapomorphy of the Astigmata. of the diversity of sperm-transfer modes. The group most thoroughly surveyed,
Female asrigmatans also display novel genitaIic characters. Rather than accept- and most diverse, is die cohort Parasitengona. Wine (1984, 1991) has reviewed
ing the aedeagus into a true genital opening, the female receives it in a secondary sperm transfer in terrestrial pansitengoncs and Proctor (1992) that in the
genital opening (copulatory pore, bursa copulamix) located posterior to the true Hydracarina. Although some terrestrial parasitengones show pairing behaviour,
opening. In some feather mites, the female's copulatory pore is located at the end none transfer sperm directly and most are dissociated to some degree (e.g. males
of a long scleroused rube (spermaduct) extending beyond the terminus of her may require an initial contact with a female to start depositing spermatophores but
opisthosoma, which is often longer than the male's aedeagus (Gaud & Atyeo 1996). need no subsequent contacts). Male Allorhrombium Ierouxi (liombidiidae) show
The male's aedeams" is situated near the coxae of the fourth oair of lem. To coou-
2
' Iek-like behaviour in which they defend small spcrmatophore-deposition rerrito-
late, asrigmatam assume a variety of positions. In the Glycyphagidae, the male ria from other males (Moss 1960). Moss observcd one male tapping a female that
mountr the female so that both mites face in the same direction (Evans 1992). In had entered his territory but did not observed spermatophore uptake. Mumal tap-
the Aaridae, male and female face in opposite directions. Male acarids grip the ping and moving in a circular 'dance' are common to a number of trornbidiid and
smooth-skinned females using suckers on the fourth pair of legs and near the anus. erythraeid species that show paired-indircrt transfer.
Many feather mites are strongly dorso-ventrally flattened. The male lies on Water mites (Hydracarina) display all possible types of spermatophore trans-
top of the female, facing in the opposite direction, often clasping her with fer. Some species of Eykzis (Eylaidae) show the (probably) ancestral behaviour of
specialised hind legs and setae, and maintaining his grip with adanal suckers paired-indirect transfer, complete with a circular dance. Many Nerrmania
(Figure 5.0). In some species the spermaduct of the female is inserred inside the
- during- copulation
male's aedeagus - (Gaud & Atyeo 1996). Male feather mites
often exhibit remarkable intraspecific polymorphisms, with a single species pre-
senting- small female-like males (homeomorphs) and large, - elaborately modified
males (heteromorphs). Male polymorphism occurs in a number of other mite
taxa but it is especially common in the Astigmata (see page 79). Additionally,
feather mites are unique in that asymmetrical males with hypertrophied setae
and legs on one side of the body occur in many taxa. They may be the sole type
of male (i.e. in species with monomorphic males) or only the heteromorphs may
show asymmetry. Right and left asymmetry appear to be expressed equally. T h e
utility of this asymmetry is a mystery (Gaud & Aryco 1996).
Bonek & GriGrhs (1979) studied the mating behaviour and capacity of
males of two common stored-product pests, A r a m siro and Lardogfphus konoi
(both Acaridae). Aker a male and virgin female mated, a single sac-like mass
would appear in the female's seminal receptacle. The authors suggested that an
elastic spermarophore was transferred through the aedeagus into the receptacle;
however, Evans (1992) feels it more likely that a liquid ejaculate develops a wall
once inside the spermatheca, much the way that-the 'end~s~ermatophore' of
phytoseiids arises. When single pairs were kept together, after eight days the
average number was six spermatophores per female (1-13) for L. konoi and
15 (9-23) for A. siro. When single males were maintained with 1, 2. 5 (and 10
for A. siro) females, Roczek and Griffiths found that extra females induced male
L. h n o i to produce more spermatophores (four times more in the 5-female vs.
 (Unionicolidac) have 'I very complex courtship involving leg-tretnlding, foot-
stomping and leg-fmning (Proctor 199 1 b) (Figure 5.4). Newnnnm species feed
on copepods. It appears that the leg vibrations of the courting male 'deceive' the
female into striking at the male as if he were a copcpod. T h e rnale responds to
being grasped by depos~tinga large and complex mass of spermatophores and
then fanning his hind legs over them. T h e female, ifvirgin, responds to the fan-
ning by running towards the male and hence over the spermatophores. T h e
sperm packets arc sticky and become atmchcd to the female's venter, and she
later brushes them into her genital opening. Why would the male want to
70 induce predatory behaviour in the female? Males respond to contacting females
and contacting substrates recently occupied by females by trembling hut obvi-
ously only if he trembles in front o f a fenlalc will he be grasped. So the niale likc-
ly benefits by wing the female's response to ascertain that he is indeed courting
a real female rather than the chemicd residues of one, and thereby avoids
wasting his sperniatophores.
From this paired. indirect mode of sperm transfer, water mites havc diversi-
fied in both directions. Many taxa display dissociated transfer of spcrmatophores
(Proctor 1992). including some Ncurnnnia and species in the related genus
Utrionicoh. Dissociation appears to be a risky business becmse a rnale cannot be
sure that a fcmale will find his spermatophores. Methods employed by males of
dissociated species to increase the probability of spernlatophore encounter by
females arc discussed on page 74.
Direct sperm transfer has cvolvcd repeatedly in different lineages of water
mites. Proctor (199la) estimated that there havc been 91 independent evolu-
tions of copulation in the approximately 5000 species of Iiydracarina. Species
whose males arc modified for copulation occur in all major superfamilies except
for the prinlitive Scygothrombidioidea and the monogeneric I-fydrachnidoidca.
In somc cases, the ancestral shape of the stalked spermatophore is retained with
almost n o change, whilc in others tlic outward appcanncc is greatly altered.
Male I'ionn (Pionidac) transfer jelly-like blobs from their genital openings to the
females' using their modified third pair of legs; however, examination of the
I
internal structure of these blobs reveals them to he a bundle of miniature spcr-
matoptiores (14-18 in /? carncd) embedded in a gelatinous matrix (Lcimann
199 1). Proctor ( 1 99 1a) found evidence that lineages cornposed of swinlming
mites were more likely to evolve copulation than those made up of crawling
mites; however, the correlation was not perfect. There are many species of water
mites that copulate but do not swim, o r that swirn but d o not copulate. 1:actors
responsible for changes in sperm-transfer mode are likely to be specific to dif-
ferent tam. For example, Uniotticola species endoparasitic in mussels arc much
more likely to transfer spcrni directly than are free-living congeners. Proctor
(1992a) suggested chat the slimy substrate inside the mantle cavity selects against
deposition of sperrnatophores.
Kirchner (1967) described the sperm transfer of the marine mite
Hakzcareflw bnsteri (Halacaridac). Males do not deposit sperrnatophores unless
females are prcsent. When a male and female meet, the fenlale touches the male
with her palps and then climbs on top of him. T h e male then raises the fore part
of his body and lowers his genital plates to 'scour' the substrate. In this way, the
female is lifted rhythmicnlly up to a do-rxn times. Kirchlier felt that this interaction
was essential to induce the n~alesto dcposir their elaborate sperrnatophores. He
did not describe spcrnm uptake by females.
Among other prostigmatan mites, there are no known examples of indirect
transfer with pairing outside of the Parasitengona. Anystina and Eupodina.
However, many groups show dissociated transfer, including Bdellidae (Albert,
1974), Labidostommatidae (Vistorin 19781, Nanorchestidae (Schuster &
Schuster 1977), Rhagidiidae (Ehrnsberger 19771, some Tydeidae (Schuster &
Schuster 1970) and Eriophyoidea (Oldfield 8r Michalska 1996). Rhagidiid
males d o not produce stalked spermatophores; rather, they extrude thin threads
from their genital openings that bear one (Rbagidia arenrrria, R clavirrinim) or
several (R hahphila) droplets of liquid cjaculare (Ehrnsberger 1777). Maler of
the other families mentioned produce stalked spermatophores.
Oldfield & Michalska (1996) review sperm-transfer behaviour in gall mites
(Eriophyoidae). Spermatophores resemble lily pads, with a short thin stalk and a
broad, flattened, leaf-like head that is horizontal relative to the substrace. T h e
spermatozoa are contained in a central reservoir in the head. Only about 5 0 sper-
matozoa are held by each spermatophore. When a pre-emergent (pharate) female
is present, males of some species deposit their spermatophores near her body,
sometimes entirely surrounding her wich a fencc of ejaculates. When females are
not narby, nlales tend to deposit dense clusters of u p to 100 spermatophores near
their normal feeding sites. Aculm fockai (Eriophyidae) males deposit sper-
matophores at a rate of about 30 per day for nvo weeks, for a total of 420 sper-
matophores in a male's lifetime. Insemination occurs when a receritly emerged
female encounters a spermatophore, mounts it and takes sperm into her genital
opening from the central reservoir, leaving the stalk and deflated head behind.
Female Aculus robirtiarsearch intensively in the area where they moult, pre-
sumably because males usually encircle the pharate females with sper-
matophores. Spermatozoa are stored in the s p ~ r m a t h e ~Oddly,
e. there appears
to be both a systematic and an ecological difference in whether one or both spcr-
mathecae are used. Diptilomiopid females and eriophyid females from dicots
store sperm in only one spermatheca, while phytoptid females and eriophyids
from nlonocots store sperm in both spermathecae.
Among the Prostigmata, direct sperm transfer is exhibited by many
H y d r a ~ x i n a (Proctor 19921, Adamystidae (Coineau 1976), Tetranychidae
(Cone 19851, Tarsonemiria (Evans 19921, Chcyletidae (Summers & Witt 1973),
Pterygosomatidae (Mostafa 1974) and some Tydeidae (Knop 1985). T h e
adamystid Savidromw dclarmrri, like many species of Arrcnumwater mites (e.g.
Proctor & Smith 1994), has a form ofdirect transfer that appears to have recent-
ly evolved from indirect transfer. When a sexually interested male and female
meet, he female crawls on top of the male, facing the opposite direction
(Coineau 1976). T h e male's first pair or legs, with which he holds the female's
third and fourth pair o f legs, are more robust and presumably stronger &an
those of the female. T h e male presses his genital aperture to the substrate and
lifts his posterior opisthosoma, drawing out a large, thick-stalked sper-
matophore. T h e male then rotates 180° so that the female's genital opening is
above the spermatophore tip. He then bows down and lowers the fcmale so that
she is impaled on the spermatophore. Thus the male is responsible for the place-
ment of the sperm but docs not insert it with an intrornittenr organ.
 Male PterygnsorncI nrctcIbifis (Pcerygosomatidae) demonstrate behaviour inter-
mediate between chat of S. dehtmreiand that of taxa with intromittent strucrures.
Pterygoma mrrtabiliris an ectoparasite of agamid lizards that spends most of its life
beneath scales, feeding on host blood (Mostah 1974). Males have a dorsal genital
opening. Mostah observed one male wandering over the sumce of his host, appar-
ently in search of a femalc. The male had extruded a long, sac-like spermatophore
from its genital opening and was urrying it on his back. Then the male discovered
a female resting nearby and attempted to insert the spermatophore into her geni-
tal opening by walking beneath her, lowering his anterior end and raising his pos-
72 terior. The female refused to open her genital valves and the male eventually gave
up. Mosrafa noted that the male then tried to draw his spermatophore back into
his genital pouch, presumably for use on a more fonuitois ocusibn.
Figure 5.5
D~versicyof spermarophore morphology in the H y d r a ~ r i n a .
Unionicola
SPERMATOPHORE STRUCTURE
AND FUNCTION
External spermatophore morphology in mites ranger From the stripped-down and
purely h c t i o n a l droplet spermatophores of oribatids to the baroquely decorated
ejaculates of halacarids and bdellids. A sampler of spermatophores from just one
clade, the Hydracarina, illustrates this great diversity in morphology (Figure 5.5).
Although some of this strucrurc may bc designed to internally court females, as sug-
gested by Eberhard (1985). other strucrural aspeccs are likely to reflect selection for
an increase in the stability of spermatophores or for an increase in the encounter
probability of spermatophores and fen~alcsin dissociated species (Proctor et aL
1995). Internally, even oribatid spermatophorrs display a surpriiing complexity of
layers (Alberti etaL 1991).The most intricate internal morphology is shown by the
spermatophores of ticks: their complex and mysterious sticrure discussed below.
Exploding sperm packets
Sonenshine (1991) summarises the structure and behaviour of tick sper-
matophores. After a male tick finds a suitable and interested female, he produces
a flask-shaped spermatophore that is composed of two basic layers, the ecto- and
endospermatophore. First he exudes a clear droplet from his genital opening that
is composed of a viscous mixture of proteins and n~ucopolysaccharides.This liq-
uid congeals at the surface to form a membranous skin. Into rhis ectosper-
matophorc flow opaque seminal fluids and immature spcrnm cells (prospcrmia).
Then the endospermatophore is introduced inro the ectospermatophorc, sealing
it at the male's genital opening. Argasids introduce two endospcrmatophorcs
into each ectospermatophore but ixodids produce only one. In both groups, thc
endospermatophore is bilobed and filled with several proteinaceous substances,
one of which may inhibit the proliferation of bacteria.
The strangest ingredient found in the spermatophores of some species is the
symbiotic yeast-like fungus Adkrorystis. Adlerocysts may help to maintain via-
bility of the spermatozoa until the femalc is ready ro oviposit. Evidence for this
is that in ticks that oviposit soon afier copulation, adlerocysts d o not attach to
sperm cells, while in those species that may experience a long delay between cop-
ulation and oviposition - up to years in some Argasidae - the symbioncs do
adhere to the spermatozoa (Feldman-Muhsam 1991).
When the spcrmatophore is complete, a process taking only about 30 sec-
onds, the male grasps i t with his chelicerae and inserts it into the female's geni-
tal opening. In argasids, the male reaches down to his gonopore to grasp the
emergent spermatophore but in ixodids the male maintains his chelicerae in the
female genital opening, where he introduced them prior to spermatophore pro-
duction, and moves the spermatophore to his n~outhparrsvia contortions of his
body. Sonenshine (1991) states that the spermatophore is not a passive tool in
sperm transfer but rather 'is an active partner in copulation and itself accom-
plishes the process of sperm transfer' (p. 321). Once the spermatophore is placed
on the female's genital opening, a C 0 2 'bomb' goes off inside the ectosper-
matophore, causing the neck of the ejaculate to extend into the female's gono-
pore, forcing the contents - sperm, seminal fluid and Aderocysris- into the
endospermatophore and shooting the endospermatophore into the female's
 reproductive tract. This extrusive explosion continues wen if the spermatophore
is separated from the ti&. In argasids, the paired endospermatophorcs head off
into the paired uteri, while in kodids the single cndosperrnatophorc is held in
the kmale's seminal rcceptade. The ecrospermatophore, its role complete, drops
off the female. The s p v m alls complea the!capaatation within the fknde
(see page 62) and in atgasids may be stored in the uterus fkr many years, allow-
ing the h a l e to fcrdlise her eggs without seeking fiarther copulations.
Fields of fragrant spermatophores
/-
To humans, with our reliance on direct spurn transfer, the kof dissociat-
ed transfer that seems most precarious is the apparently low probabiiry that a
small &male mite will stumble aaoss a much smaller droplet of sperm in a vast
volume of soil or waur. Males of dissociated species, however, have w o l d an
array of devicts that increase the thanes of k n d e s finding their ejaculate. Most
obvious among these arc signalling threads and tracks, which are produced by
oribatids and many terresaial and aquatic proscigmafans, as wcll as other disso-
ciated arthropods (millipedes, CSpauropods, pseudoscotpions) (Proctor 1998).
These filaments mcchanidy u~crrasethe radius of interception of a sper-
matophore. They can a h help guide the fimale to the location of the ejaculate.
which may be at the centre of radiating threads (Oppodisano tt ai 1995) or at
the &d of a zigzag aadc of dmeasing width (e.g. W ~ t t e1991).
Terrestrial parasitengones have the most elaborate and diverse repertoire of
signding devices. For example, johnrtonima manr Uohnstonianidae) deposits a
linear zigzag uack at the midpoint of which is the spermatophore; at each
change of angle is a 'signalling stalk' that looks like a scaled-down spcrrnatophorc
minus the sperm cells (Wme 1991). Some dissociated species of wata mites also
have such sign* devices (e.g. h'ydrrrchna. fimmcham) but in comparison to
their terrestrial relatives' theirs arc crude and haphazard tracks.
Less rradily obaavcd but likely common a,all species with indka sperm trans-
fix (both paired and dissociated)is the use of spumacophonxsmckd pheromones
to amaa females. Bchaviod cvidena b r pheromones indude observations of
mites moving rowards spermamphorcs h m a distance, males touching their genital
openings on che substrate behe or afier depositing spumatophores, males !bring
thdr legs owr spermamphoms m dirca warn currents mwads fkmalcs and the loss
of acPaEtivQless of spamatophorcs ovcr time (implying dissipation of a chemical)
(hoaor 1998). Wiea (1984) su%gestad that attraction of kmales duough spa-
matophorpassoda&d pheromones is more important in wam mites,
where fimales may movc through the warer column rarher than bung &Chad a,
a twodimensional substrate. In such situations, deposition of huge fields of +t
spemmophores may allow fkmles to d n e a the presence of ejaculates even when
swimmhg some distana Erom the source Exccnsii dense 'lawns' of spa-
matophores arr produced by d e Hjehdmz (Hyddddae) and dumps of dacos
w huadx& of spamatophorcs are also commonly produced by male Limned
(Limdidac) and l+hz$vr~ (Hydrodromidac) ( h c m r 1992).
As well as amactants that act at a distance, there are undoubtedly contact
chunicals that allow &males to mognise spermatophores of their own species.
Thii would be particularly i m p o m c for dissociated species that share
deposition sites with closely related taxa. To our knowledge, no studies have
investigated whether females of dissociated mite taxa difkentiate between sper-
matophorn of conspecifics and related congenus that share the same habitat
however, Oldfield & Michaska (1990 describe spermatophore recognition by
&male gall mites fiom diffirrnt host plants and note that, fbr some species,
PmpU discrimination requires that the funale be on h a own host.
A third way to increase the probability of contact between fbales and sper-
matophores involves the placement of ejaculates where females are Likely to
encounter them in the course of their daily activities. For example, the water
mite Hydmdroma dkpicims (Hydrodromidac) fcods on the eggs of chironomid
midges. Male H. dapicicnr deposit spermatophores pdkentially on these egg
masses (Proctor 1992). Fern& in search of f;ood will thus also encounter a sup-
ply of sperm. Males of some @ mites encircle the bodies of quiescent pre-adult
W e s with spermatophorcs so that when they emerge as adults, the sperm will
be conveniently within reach (Oldfield & Michalska 1996).
SEXUAL SELECTION
When Darwin (187 1) split off sexual fiom natural selection, he considered only
two categoria: conflia between members of one sac &ni( competition)
and attraction becwatn members of the opposite sexes (iiruMxual selection, typ-
i d l y M e choice of males). However, a third category has recently b a n iden-
tificd: conflicts of inarest betwccn the sexes (itaserua co&a). Most
cxamplcs of s a d selection in mites fall into the first category; however, evi-
dence b r krnale choice and i n t e r s d conflict is growing.
Intrasexual competition: male modifications for mate
monopolisation
~ o m ~ c & i obetween
n males h r access to the eggs of femacs has d u d in the
evolution of a range of secondary sexual characters, both behavioural and mor-
phological. Thii is as true fixmites as it is for all other organisms with separate
sexes. One maior difkcnce between mites and the best studied erouo of arthro-
PO&.insects, k that sequestering of a female a h r insemination % wiShpreadin
Insecta (Alcock 1994) but is extremely uncommon in the Acari. The only doc-
umented ammples in mites arc Rbieoglphus mbinii (Radwan & Siva-Jothy
1990, the special cases of biparental defence against predators in spider mires
(TCtranychidae)(Saito 1986a, b) and of harems in mud-inhabiting water mites
(cg. Davids eta2 1988, see (a) below) and spider mites (Saito 1990).
In contrast, prccopulatory (or more precisely, pre-insunhatoy) guarding is
very common. This may be becaure: Lmale mitcs o h become unreceptive
1' soon aFter mating (eg. Tetranychidac, Cone 1985); because the period between
mating and oviposition is very long and so a male would gain more by seeking
other mates than by sequestering his current one; or because first-male sperm
p d e n c e is very sttong. In Armunrr water mitcs, male and W e o h
d n physically attached fkr hours afkr sperm &has o c d (Proctor
& Smith 1994). This may be a type of mate& (Alcock 1994). or it may
be a subtle form of postcopulatoy courtship that is necessary to convince a
kmale to take up sperm (see Eberhard 1985); this would place the bchaviour in
the realm of intersexual seIecdon through female choice, although the distinc-
tion between the two types of sexual selection is often subtle.

(a) Mate-gunrding and agqresssiovi
Guarding of pre-imaginal females occurs in many groups of mites with direct
sperm transfer. When i t involves close physical contact benveen the male and
pharate female it is termed prewpula In the Mesostigmata, pre-copulatory
guarding has been observed in the Phytoseiidae, Ascidae, Laelapidae,
Ameroseiidae and Macrochelidae (Yasui 1988, Walter pers. obs.). In some a c i d
and laelapid mites, the males may even ride around on chc backs of female deu-
tonymphs and adults, presumably waiting for a chance to mate.
B
In the Astigmam, precopula has been observed in the parasitic Psorpotidac
and Chirodiscidae (Evans 1992) and in some feather mites W~talinskiet al.
1992) in which males use suckers to attach to tubercles, disks o r lobes on the
female tritonymphs, holding on to them until the adult femalc emerges.
Witalinski (1990) and Witdinski etaL (1992) discuss che fine structure of adanal
suckers in male astigmatans. The Astigmata also demonstrate a rare occurrence of
post-copulatory contact that appears to serve as mare-guarding. Radwan & Siva-
Jothy ( 1996) have demonstrated that in Rhizogbphur mbinii (Acaridac), a species
in which individuals of boch sexes may mate several times a day, a male increases
his fertilisation of a clutch by prolonging his attachment to a female for up to six
hours after copulation. Since many asrigmatans stay in copulo for extended peri-
ods, this phenomenon may be of more general distribution.
In the Prostigrnata, precopula occurs in the Tarsonemina, ?j.deidae,
Cheyletidae, Eriophyidae and Tetranychidae (Michalska & B o a e k 199 1, Evans
1992). In the Tarsonemina, males use their modified fourth pair of legs (when
present) and a sucker-like device termed a genital capsule to hold onto the
pharate female (within the larval skin) (Figure 5.6). Garga er dl. (1997)
Figure 5.6
Male Pdyehagotanonemus
h s (Tarsonemidae)
canying a pharace female.
(Illustration courtesy of
Cacherinc Bryant)
Sex & CELIBA~:Y
observed that the fourth pair of legs of 7izrsonernrcr co~fitsus(Tarsonemidae) arc
also used in aggressive contests benveen males for possession of pharate females
and that the size of these was a better predictor of which male would win than
was general body s i 7 ~Male Tanonemtrs may trundle about with an attached
pharate female for up to 24 hours before the adult female emerges; however, chc
act of mating takes only a few minutes at most, after which the pair separates
(Evans 1992). In the Podapolipidae, another group in the Tarsonemina, males
seem to have grown impatient and copulate directly with the larval femalc
(Evans 1992). In the Eriophyidae, malc Vaatcs robiniac will guard quiescent
deuronymphal females by lying beside their still forms until the adult female
emerges, grappling wich other males that attempt to take over (Michalska &
Boaek 1991). If the first male fails to chase away the second, the latter may
become a co-guarder. In the late summer, when pharate females are scarce, there
may be as many as eight males guarding each deutonymph.
Pre-copulatory associations and malc aggression have been very well stud-
ied in the Tetranychidae. Mites of this family lack the rritonymphal stage,
moulting directly from deuconymph to adult. Deutonytnphal females close
to transformation construct a silken pad o n which they settle to await their
moult (Cone 1985). T h e closer a fenlale is to eclosion the more attractive she
is to males, presumably through incrcased release of arrestant pheromones.
When a male encounters an attractive pharate female, he settles down besidc
her, ready to defend his nubile booty. T h e male lays down several strands
of silk over the quiescent female; these allow him to monitor both her
movement prior to moulting and the arrival of any other malc. Femaics
typically are interested in mating for only a short while immediately after
eclosion, whereas males are able to mate many times; so thcrc is an oversupply
of amorous males, vfhich leads to great competition for pharate females. Males
vie for possession of females by sparring with thcir front legs, by spitting silk
and by stabbing at each other with extended chelicerae (Potter ct nl. 1976,
Enders 1993). Occasionally, one malc pierces the ocher, resulting in the rapid
exsanguination and death of the wounded male. Larger males arc usually
successful at defending their females. If neither rr~alecan overpower the other
they may become co-guarders of the female; Potter et al. (1976) found that
the co-guarding male that assumes a position on top of the female tends to be
the first to copulare.
The greatest extremes of mate-guarding arc shown by males that keep
harems. This behaviour has been best studied in mammals such as elk, horses
and elephant seals, in which the harem-master has greatly elevated reproductive
success relative to those males without harems. For a male to sequester a group
of females and guard them from other suitors, the females must be defensible
(Emlen & Oring 1977). The tendency of most ungulates to form herds may
allow stallions and stags to guard females and the limited space on breeding
beaches makes calving females defensible for male elephant seals.
Harem-keeping has evolved in two groups of mites wich very different
lifesryles. Many species in the water mite genus Unionicokz (Unionicolidae)
dwell inside the mantle cavities of freshwater mussels where they feed on host
fluids (see Chapter 7). Sex ratios of mites inside mussels are often extremely
fcmale-biased. O n e explanation for such biases is female-skewed primary sex
 ratios such as are found in many mites and insects inhabiting small patches of
habitat (see page 89). But, in such cases, it is typically the dosdy related
descendants of a single founding female that occupy such patches. In con-
trast,Unioniroloin mwels are very unlikely to be related to e d other b e c a u ~
larvae disperse from naral mussels in search of midges to parasitkc and n m
mites entering mussels are likely to be derived from various sources.
D i m d (1983) studied the bchaviour of male UnioniroIrrfimwsa fiom
mussels in North Carolina. Most mussels (86%) harboured only a single male.
whereas females ranged fiom 6 7 8 per mussel. Dimodc found only 23 of 360
mussels to have more than one male and in these cases it was usually a small-
er, perhaps recently emerged, male ~ a i r c dwith a larger o n c To determine
whether the sex ratio could be a produa of intermaIe aggression, he compared
the survivorship of mal+malc pairs, male-female pairs and fcmae-female
pairs Iefi together for three days. Survivorship in pairs with one or two f k m . 4 ~
was almost 100% but all male-male pairs were reduced to a single living malc.
Combat between male U.firmosa involved grappling until one malc grasped
the other's leg and pierced hi rival with his chelicerae. To determine whether
mortal combat also took place within the m d , D i m d introduced addi-
tional males into the mantle cavities of freshly collected bivalves. After three
days he removed the inhabitants and h u n d in 23 of 24 cases only a single li-
ing malc was present. In the 24th mussel, two dead males were found locked
together. Edwards & Dimock (1991) found that larger male LI. firmosa were
much more likely to emerge viaorious from paired combat. They also
observed that the palps of males are larger than chose of f d e s , presumably
the result of i n u a s d selcaion for stronger weapons.
Not all mussel-dwelling UnwnicoLr show such aggression. D a d s et d
(1988) compared the behaviour of males of the European species U.ypsilopho-
ra and U. intmnedia. Like U.fimosa, males of LI. ypsitophom fight to the
death. In contrast, male 0; intern& show no aggression towards potential
rivals. The species diffir both in male phenology (U.ypsilphora males are pres-
ent throughout the ycar, Ll interm& only in the summer months) and in
mode of sperm transfer (U.ypsilphonz males arc not modified for d i r m trans-
fer, 0; intmnrdia are); however, it is not dear whether one or both of these dif-
fkrences contributes to the contrast in inmsexual aggression. D i k e n c a in
aggression may also explain why LI. ypsihphora are able to exclude U. in-
dia &om the mussd Anodonta cygnea, a host that the latter species will use in
the absence of 0; ypsihpbora
Similarly, Saito (1990) observed variation in intermale aggression between
two congeneric species of spider mite (Tktranychidae). Male Schbfr~ranychru
l n g w tolerate the presence of other males, whereas those of S. miscanthi are
extremely aggressive, climbing on r i d and stabbing them to death with their
chcliceral stylets. Both Schbtmnyhils species live in communal nests com-
posed of numerous adults, juveniles and eggs. Saito surveyed the inhabitants
of 110 S. longus and 86 S. m k n t h i nests. For S.longus there w u e 0-32 males
per nest, whiie fbr S. mirconthi the range was 0-3. For the first species, num-
bers of males per nest increased with overall nest sizc, while for the latter there
was no such &rrelation: most nests contained only a single male monopolis-
ing a dozen or so &males. Saito could think of no demographic or behavioural
factors that could explain why one species shows harem polygyny and the
other a scramble-type polygyny.
Aggressive behaviour &ay also vary inaaspecifically. As mentioned previ-
ously, male polymorphism (andropolymo'phism) occurs in a number of mite
taxa, indudig the Dermanyssidae and Macrochelidae (Mesostigmata),
Chcyletidae and Anystidae (Prostigmata), Acaridae and numerous hniIies of
fea9her mites (Astigmata) (Gaud & Atyeo 1996. Xnuns et al. 1981). Male
feather mites of many species show an additional Nvist to polymorphism in that
heteromorphs may display asymmetry of the body, 1% or scfae. According to
Gaud & Atyco (1996), this asymmetry is equally expressed on left and right
sides, the adaptive value of such asymmetry, however, is unknown.
The causes and consaquenccs of andropolymorphiim haw been best stud-
ied in the Acaridac, where the aristence of multiple male forms has been known
for more than a century. Polymorphism occurs only in the subfimiiy Acarinac,
where males are represented by up to four morphs (limms et aL 1981). The
homeomorph has a third pair of legs that are similar in sizc and shape to those
of the h n a l e and has body setac of a similar length to the female's. The
b i i o r p h has a longer body and setae than the female. The heteromorph has a
very much thickened pair of legs, rypically the third pair, but has setac are sim-
ilar to the female. The pleomorph has a pair of thickened legs and has a longer
body and longer sctae than the female, i.e. it has the characteristics of the
bimorph and heteromorph combined. Occasionally malformed males with
only a single thickened leg occur. Not all species exhibit all possible morphs and
the presence and ratio of di&rent morphs may also vary between populations
of the same species. Morph type may be inherited (e.g. in Rhiwgii$phus mbinii,
Radwan 1995) or determined by environment, as T i et d (1981) showed
for CaCog&phuc (= Slsncrrrsania) berhsei Regardless of paternal rype, d e C.
bmhsn' reared in low-density situations became pleomorphs (well armed), whiie
those raised in low-density chambers grew up to be bimorphs (poorly armed).
T~mmset aL (1980a) determined that a volatile chemical (or mixnue of chem-
icals) was produced by large colonies of b m k i that suppressed the produc-
tion of well-armed pleomorphic males. In a companion study (limns et aL
1980b) they found that pleomorphic males attack and kill newly emerged
bimorphs and pleomorphs by grasping them firmly with their modified third
pair of legs and puncturing the integument with the fourth pair. Pleomorphs
killed bimorphs regardless of whether females were present. Older males of
both types were more heavily sclerotiscd and better able to survive attach. If
two older, well-armed plcomorphs encountered each other 'they would back off
and advance in di&at directions'. Bimorphs were non-aggressive, both
among each other and towards pleomorphs.
Radwan (1993) investigated the trade-off between being an aggressive pleo-
morph vmus a passive bimorph in C bmhei He consuuctcd colonies of two
sizes: small, with LSVO individuals each of the fighter and non-fighter morphs
and six fimales; and + with 30 individuals of each morph and 80 females.
He found that in small colonies, aggressive pleomorphs had higher reproduc-
tive success because a single male could kill many,often all, of his rivals. In large
colonies, fighters had lower reproductive success because they spent more time
fighting,less time copulating and were much more likely to be killed than were
non-fighters. Radwan suggests that pleomorph males will do best in recently
founded (and so small) colonies where individual males can readily do away
with their rivals,' while peacefid bimorphs do best in large colonies where the
a t e of encounter berween males would mean chat plaomorphs would spend all
of their time fighting and little time mating. This hypothesis matches well with
the observations of Tunrns et u l (1980a) that development of pleomorphs is
suppressed in large colonies.
(b)S p m competition
Parker (1970) was the first to note that competition between ejaculates of dif-
ferent males was likely to exert strong selection on male morphology and
behaviour. Being 'first in' is very imporrant for male spider mites because
tetranychids exhibit first-de sperm prrcedence. That is, the first male to
copulate with a female ferrilises the majoricy of her eggs (Cone 1985), partic-
ularly if he is allowed to mate with her without interrupdon (Potter &
Wrensch 1978). The structure of the female's internal reproductive system and
the path of spermatozoa after insemination arc thought to play imporrant roles
in determining the patterns of fertiliition priority in arthropods (Kaster &
Jakob 1997). In sp~dermites the spermatozoa appear to migrate from the sem-
inal receptacle, through the haemocoel of the female, into the ovary (Feierrag-
Koppen & Pijnacker 1985). So sperm from the first copulation get a head s t m
on those fiom subsequent matings.
The occurrence of pre-copulatory mate-guarding in the mesostigmatan
MacrocheIn r n ~ ~ ~ ~ l ~ d o(Macrochelidae)
m e m ~ c ~ would seem to predict a similar
phenomenon. In this species, the male rides about on the back of the
deutonymphd female and mates with the adult female immediately after her
emergence. Males of this species are heavily armed with spines on their second
and fourth pair of legs, which they use to am& rivals (Yasui 1988), and also
to hold the female during sperm transfer. Yasui (1988) used double matings of
electrophoretically different strains of M. muscrZC&mcsticae to determine
whether there was first-male precedence. The evidence was overwhelming:
only one of 410 ospring were produced with sperm from a second mating. If
the path of sperm inside the female in the Macrochelidae involves travelling
through the haunocoel, as it does in the T m y c h i d a e , then one would pre-
dict thac other dermanyssines also show f i r s t - d e precedence.
In striking contrast, double-mating experiments with irradiated male deer
ticks (Lxodcr damrninz) revealed chat the second male fertilised the most eggs
(Yuval & Spielman 1990). Yuval and Spielman (1990) suggest that the pro-
longed probing of the female's genital opening by the male may allow him to
remove the ejaculate of the previous mate, so that when he introduces hi own
spermatophore there is a reduced number of competing sperm. This is an
intriguing suggestion and a plausible one considering that female ixodids store
sperm in a seminal receptacle (Sonenshine 1991). Argasid funaes store sperm
in their uteri, possibly out of reach of the male's mouthparts; therefore, one
would predict thac last-male sperm precedence is unlikely to occur in this
group of ti&.
Sperm competition in some Acaridae (Astigmam) also involves last-male
precedence. Radwan (1991) found in G2log~phruberksei that the second male
to mate fertilised on average 7 4 4 6 % of a female's eggs, and that last-male
precedence was maintained even when a female mated with three males. This
contrasts with the findings of Zeh & Zeh (1994) for pscudoscorpions, in
which last-male advanrage breaks down if there are more than two matings.
The degree of precedence decreased with the interval between first and second
matings; afier six hours, there was no significant difference between fertilia-
tions from first and second males. Radwan & W ~ d i n s k (1991)
i examined the
spermathecae of k n d e C bcrhsei after compIeting mating with a single male
and after interrupted mating with several males. TEM seaions indicated that
when matings were interrupted, males had not transferred sperm cells; rather,
they had pumped the female's spermatheca full of an amorphous fluid. The
authors condude that C bcrksei males first h e r a substance thac pushes
previously deposited sperm away from the openings of the efferent ducts Iead-
ing to the ovaries and then deposit their own spermatozoa in this region. Thus
the last male to mate positions his sperm where it will be used soonest by the
female.
In another acarid, RhiwgIyphus robini, there is no consistent last-male
advantage; rather, the paterniry of second males ranges from 0-93% (Radwan
& Siva-Jothy 1996). Radwan (1996) found that the strongest predictor of
male fertilisation success was the size of his spermatozoa. Males that produced
larger sperm cells were more Likely to fertilise eggs, a phenomenon independ-
ent of the male's body size. Radwan suggests that larger spermatozoa may sur-
vive longer in the spermatheca, or perhaps move fister through the efferent
sperm ducts leading to the ovaries.
. When Parker (1970) developed the idea of internal sperm cornpetition as
a selective agent, he suggested that this gametic battle was simply a continua-
tion of the ancestral war engaged in by externally fertilising animals. In such
fiee-spawners, winners were (and are) likely to be determined primarily on the
sperm output of the male. The more tickets in the lottery, the more likely you
are to win the prize - ferrilisation of an egg, in this case. For arthropods with
dissociated sperm transfer, external sperm competition of this sort still holds
(reviewed in Proctor 1998). Males that deposit more spermatophores will
(cctrrisparibus) be more likely to have their ejaculates intercept a female. But
unlike free-spawners, these arthropods have an a d d i t i o d tactic in their arse-
nal: physical destruction of a rival's spermacophores. In most dissociated taxa,
when a male contacts a previously deposited spermatophore he will trample,
crush or snap it off and typically deposits a new spermatophore near or even
on the crushed one (Schuster & Schuster 1970, 1977, Alberti 1974, Proctor
1992, 1998). This behaviour often results in 'trees' of dozens of sper-
matophores piled one on top of che other. Although earlier authors interpret-
cd these behaviours as maintenance of a fresh sperm supply for females, it is
dearly a rype of male competition. Arnold (1976) intcrprered the rernarkabty
similar behaviour of spermatophore destruction by male salamanders as intra-
sexual corn~etition.
How db male mites benefit fiom these behaviours? Most obviously, they
reduce the number of competing spermatophores. It is also possible that by
depositing near or on the remnants of other spermatopho& chey gain by
'stealing' the pheromonal effort of previous males (Proctor 1998). Evidence for
pheromone theft is that males of a number of species begin depositing sper-
matophores when they encounter those of other males but do not destroy the
previously deposited ejaculates (Moss 1960, Davids & Bclier 1974,
Ehmsbergcr 1977). It may also be that many males deposit at the same area
because of some special characteristic of that site, for example, approprim sub-
strate or humidity.
Intersexud selection as an agent of morphological and
behavioural change
Although D a d s contemporaries were quite willing to accept the idea that
aggression between males could result in the evolution of elaborate masculine
characters, they were sceptical that female animals could select males on the basis
of 'beauty'. It was not until the 1980s, almost a century afccr Darwin's book on
sexual selection, that scientists began to investigate the role of female choice in
the e ~ I u t i o nof male secondary sexual characters.
(a) F d choice
Early efforts exploring the role of female choice in dselection fbcussed on
tan in which females select one malc h m a simulanmus array of potential
mates. Evidence rapidly accumulated that the most extravagantly decorated,
loudest or most vigorous of males tend to be chosen (Ryan & Kcddy-Hmor
1992). This has been best documented for animals that court visually (e-g.
birds, fish, dticid spidus, many inseas) or vocally (e.g. birds, h o g , many
insects). There has been little work on those that rely primarily on chemicals
for mate attraction (e.g. many mites and insea), in part because it is mote dif-
ficult for humans to ascribe a female's decision to mare with a given male to the
attractiveness of hi 'aroma'.
This type of choice may be described as an 'active' dispIay of preference by
the female and is dosest to D d s idea but the definition of female choice
has been stretched so that it encompasses a broad range of &male characteris-
tics. Females may exert passive choice, an unfortunately oxymoronic phrase, if
some aspect of their sensory system or morphology results in them being more
likely to mate with males with certain atuibutcs (cg. if &males red very
well, then reddish males may have higher mating suu;css). Females may also
exert cryptic choice if they manipulate males' cjaculatcs internally to favour
one male over another, or mate again if their first mate did not meet their stan-
dards. Males may be selected to court females both e x t d y , where their
actions arc visible to human observers. and internally. Eberhard (1985. 1996)
has accumulated a huge body of evidence suggesting that cryptic W e choice
and copulatory courtship are widespread, and that M e choice is responsible
for much of the elaboration and species-specificity of male genitalia. Is there
any evidence that female mites choose their parmers?
There are very fkw obsefyations that support the idea of active female
choice in Acari. Edwards & D i o c k (1991) found that large-bodied male
Unionicolafimostz tend to have larger harems. Although this may be the result
of kmales choosing to reside in mussels that are controlled by b e males, it is
also possible that large haruns arc more eagerly fought
- f$r by males so that only
the strongest and largest can maintain corkol.
Passive female choice is a much more likely phenomenon in the Acari. The
copepod-mimicking courtship of malc Namum2 water mites is a good exam-
ple of males taking advantage of sensory b i e s in females. Is funale choice pos-
siblc in dissociated species in which kmales never meet fheir partners?
Conspicuous secondary sexual chaaaus are typically absent in taxa in which
males and fiemaes do not contact each other during spmn rransfer (eg. water
mites, Proaor 1991a), implying that-femalechoice does not act on male mor-
phology in these species.
Eberhard (1985) and Proctor etd (1995) found that morphology of sper-
matophores was also less elaborate in dissociated species than it was in species
with -paircd-indkcct trans&, suggesting that female choice is not actkg as
strongly on spermatophore morphology either. It seuns most likely that &male
choice in such species acts on the a t ~ ~ t i v e n eof
s s chemicals associated with
spermatophores.Howevcr, although M e mites can diffkrentiateamong spa-
matophores based on the age of the ejaculates (c.g. in oribatids, Woodring &
Cook 1962), to our knowledge there is no study of whether they diffexntiate
among maIes based on spermatophores. Work by Hedlund et af (1990) showed
that W e OrchcrcCla cinctu (Collembola) picked up spermatophores produccd
by males of their own 'rearing' p u p more ofien than those produced by males
from a different group, proving that mate choice in dissociated species is possi-
ble.
A particularly tenuous type of f&nale choice is that associated with the cjac-
date oumut of males. Parricularlv tbr males with indirect d r . in which
female encounter with spumatophores is not guaranteed, number of sper-
matophores deposited may be the best prediaor of male mating success.
Spermatophore output in pseudoscorpions and mites has been shown to be
aff;cccedby male age and nutritional status (Proctor 1998). Females, by pas-
sively encountering the spermatophores of well-fed males mote ofcen than
those of starving ones, may exert some selection fbr males with better abilities
ro garner resources. Female mites may also exert cryptic choice by remating if
unsatisfied with their first mate. However, there is little evidence for this.
Proctor (unpublished study) manipulated the spermatophore output and
vigour of male A n m u f l ~mnubr&vr
~ (Arrenuridae) to test whether females
were more M y to remate if their first mate was of poor qualif. Although
many females m a d with a second male when given the opportunity, there was
no correlation with the first male's 'quality' and the l i M i o o d of the W e
rematine.
Mating in copulating species of mites is characterised in many cases by a
remarkable la& of W e choice. In many taxa, males sequester females prior
to adulthood and mate with them immediately upon edosion. In such species,
females tend to mate only once or have long refractory periods before rcmat-
ing. In the Tarsonunina, brothers may copulate with sisters inside the body of
their mothu; here there seems even less potential for choice (Killiszewski &
W-ch 1993). In taxa that mate repeady, there is o h a predictable pat-
tern of first- or second-male sperm precedence. Consistent patterns of sperm
precedence are problematic for advocates of cryptic female choice (Schneider &
Elgar 1998). Unless, for example, the second male is invariably the higher qual-
ity one, consistent precedence is evidence that selection on males to fcrtilise
MITES:ECOLOGY,EVOLUTION
AND BEHAVIOUR
eggs is much stronger than it is on females to choose which male gets the hon-
OUT.
&hard (1985) argued that daborace male genitalia were the result of
Lmale choice. Complex, species-specific intromictent organs are common in
many taxa of mites that uansfer sperm by copulation (e-g. water mites, spider
mites, dermanyssine mesostigmacans). However, it is difficult to determine
whether such modifications are the result of selection to titillate the female or
to sabotage another male's' ejaculate through internal manipulation of sperm
(e.g. Radwan & Wkahki 1991). In summary,female choice of the kind evi-
denced by birds,fish and many instc~has yet to be shown in the Acari.
Students of sexual selection seem particularly prone to fids. Over the past cen-
wry, paradigms for the interactions between males and females have changed
from that of cooperation for the good of the species, to males fantically uying
to amact the attention of females that exert their choice actively, passively and
cryptically, to the emerging belief that 'intusurual conflict' is the prevailing
force behind the evolution of both male and &male craits. Adherents of the
'conflict' school feel that there is a batde berween males and Females for control
over fcrtilisation. The courtship dances and elaborate genitalia of males are
interpreted not as offerings to please choosy b a l e s but as armaments to coerce
or deceive females into giving up their eggs. Females in turn raise their thmh-
olds of sensitivity to such male subterhge, resulting in cycles of deception, dii-
belief and stronger deception. This sexual arms race is thought to be a driving
force in the evolution of diversity (Parker & Partridge 1998), just as the battles
between hosu and parasites and plants and pollinators are considered engines
of diversification (Brook & McLennan 1991, Mitter et aL 1991, Pellmyr
1992).
Several predictions derive from the intersaual conflict hypothesis. The first
is that females arc often induced into mating when it is not in their best inter-
ests. There is good evidence fbr this in drosophiiid flies. Femde Dmophikz
mekznogarmthat mate repeatedly die earlier than singly mating W e s (Fowler
& Partridge 1989). Rice (1996) showed that when female lineages are kept
from coevolving with male lineages, the lifespans of such females are even more
reduced from mating than arc those of cocvolved W c s . This implies that
males and females are in a constant battle in which toxic chemids in male ejac-
ulates usurp control over fertilisation and oviposition. Another prediction of
the conflict hypothesis is that morphological and behavioural tactics of each sex
will change over cime, as modes of attack by males are rendered ineffective by
evolutionary changes in Female defences. This pattern may be recoverable
through phylogenetic analysis (Holland & Rice 1998). One might predict that
male courtship would accumulate embellishments over evolutionary time,
while female coyness would increase. So, male genitalia may become more
complex in derived species and female sperm receptacles may evolve more tor-
tuous paths.
This appears to be a l i l y explanation for the secondary female genital
openings common to many taxa of copularing mites. The l o & l site OFentry
for sperm, and the one used by all non-copulating mites, is through the primary
genital opening but in dermanyssine mesostigmatans, all Astigmata and many
prostigmacans (e.g. Tetranychidae), fkmales have a secondary opening used
solely to receive the male inaomirrcnt oqpn. Why have these openings been
relocated?
A due may lie in the mating behaviour of some nematodes, velvet worms,
tardigradcs, leeches and bedbugs. Species in these taxa uanskr spurn by hypo-
dermic insemination (also known as haemocoelic or traumatic insemina-
tion). In this form of &pulation the male introduces sperm into the female's
body cavity directly through her integument. This may be via spermarophores
spiked with lytic enzymes (e.g. in velvet worms) or needle-like inuomittent
organs (e.g. in bedbugs). Chapman (1971) described a scenario for the wolu-
tion of hypodermic insemination in the Cimiwidea (Hemiptcra), the group to
which bed bugs (Cimicidac) belong. In Alloto~nchwj%vipes,the male's acdea-
gus enters the primary genital opening of the female but pierces the wall of the
female's vagina with a sharp apical spine so chat sperm are injected into her
haemocoel. They move through the female's body cavicy, eventually congregat-
ing around the ovarioles where they penetrate the membrane surrounding the
eggs and fertilise them. In Primin'mex the sharp aedeagus penetrates an inter-
segmental membrane on the female's back to inject sperm. In chis taxon, sperm
end up being stored in a pair of pouches near the oviducts. In Xylocorir g a k -
inus, the Lmale has a sdemtised cuticular ouch (the ectosverrnanlaee~
b&en thydorsal sclerites of abdominal segmkts 2 i d 3 that'receives ;h;
male's aedeagus. Sperm is then conducted chrough a cord of cells that leads
fiom the ectospermanlage into the haemocoel, and they then accumulate in a
seminal rece~tadeat the iunccion of the ovarioles. In Anthorotis and Oriur
(Anthocoridae) insemination is no longer haemocoelic. Rather, a copulatory
tube opens between the ventral plates on abdominal segments 7 and 8 and
sperm are stored in a sperm pouch. From here a conducting cord leads to the
oviducts so that soerm is never free in the hacmocoel.
The situation in Anthocotis and Otius is remarkably similar to that in der-
rnanyssine mites, where secondary genital openings siruated on the female's
v e n d plates or on her legs receive sperm from the male's chelicerae. Can one
discern a pattern in parasidform mites parallel to that of the Cimicoidca?In the
Ixodida, males introduce their mouthpam into the primary genital opening of
the female where they fiddle around doing mysterious things, sometimes for
hours (Feldman-Muhsam 1986). It is only after the mouthparts are withdrawn
chat the spermatophore is applied to the genital opening. In the Dermanyssina,
rhodacaroid males do l i prior to mansferring sperm into the fu&s sec-
ondary genital opening. k there a stage in primitive mesostigmatans, as yet
undiscovered, in which males pierce the female's vaginal wall to pmvide their
sperm with a shortcut to the o k i e s ? And if one were to plot the movement of
sperm-conducting cissues and sites of inseminarion in the Maostigmata, would
one observe a pattern of males shifting penetration sites and funales attempc-
ing to regain control of the movement of sperm? Have male spermatodacryls
become sharper and more penetratingover time? It is surprising that no one has
perfbrmed such an analysis.A similar study might involve investigating bchav-
ioural and morphological patterns in the water mite M y Arrenuridae, in
which sexual dimorphism ranges from almost zero (e.g. wuY&), where sperm
 A N D BEHAVIOUR
ECOLOGY,EVOLUTION
MITES:
transfer is presumably indirect, to copuladon without intromission (e.g.
Amnurur (MegaCuracaw) spp.), to transfer via complex intromittent structures
(e.g. Amnutrcs (Armunrr)spp.). The huge diversity of transfir modes and male
modifications fbr sperm transfer displayed by the h i is an unclploited
treasure-trove fbr students of sexual selection.
PARTHENOGENESIS
Although pmkaryora have thrived for perhaps four thousand million years with-
out sex, wc expect organisms with chromosomes mcased in a nudeus to undergo
meiosis and sexual ~ m b i i t i o n No
. mammals or birds do without sex and fkw
reptiles or amphibians arc asexual. Mias, however, are not such prudes.
W h y have sex?
Despite the temptation w answer flippantly, this is one of the most profound
questions in evolutionary biology (Bell 1982, Steams 1987). Sexualicy - the
merging of gcnomes fiom two individuals to produce 06pring - is the over-
whelming rule in mulucellular a n i d . Nomn and Palmer (1991) note chat
obligate parthenogens makc up less than 1%of the animal kingdom. Yec there
is a basic incfficiencyto producing both male and W e oflipring. If one placed
two females in competition, one that produced only female oapring and one
that produced a 5050 ratio of males and f;unaes, the all-hale lineage would
rapidly outproduce the bisexual one Also, fiom the fbunding fimale's point of
view, she would transmit a much higher proportion of her genes if she and her
daughters reproduced donally rather than having to bring in male genomes
every generation. This waste of resources on unproductive males has been
termad the 'wofbld cost of sex' (Maynard Smith 1978).
So why bother with sexuality?Many hypotheses haw been advanced (Steams
1987), although empirical evidence fbr most is rather scanty. At the species-selec-
tion level, sexuality may d u c e the probability of extinction by generating greater
genetic diversity (through recombination), allowing more rapid adaptation to
changing environments. Its parallel at the individual level is bet-hedging in vari-
able cnvironmcncs, one should not put all of one's eggs in a single generic basket.
Changing environments may be biotic as well as abiotic. Parasites and dis-
ease-causing agents typically have an advantage in that their more rapid lifi
cycles allow them to adapt quickly to the host. If hosts are invariant in their
genetic makeup, this allows diseases to rapidly sweep through populations. It is
dear in this case that recombidon allows host organisms to stay in the arms
tace. The opposite side of the coin is that sex helps to prevent undesirable vari-
ation through DNA-repair, where chromosomal damage fiom one parent can be
repaired by undamaged infbrmation in the homologous chromosome fiom the
other parent. The DNA-repair hypothesis applies m all cukaryota regardless of
the vacillations of their environments.
Some combination of theseselective!agents, acting both at and abwe the level
of the individual, may explain the overwhelming dominance of sexual rcproduc-
tion in animals. Most vertebrate parthenogens seem to be rcccndy derivbd h m
sexual species, suggest@ that loss of sex shunts a lineage into an evolutionary
dead end (eg. Bell 1982). However, there are a f m niggling taxa that seem to
flout these rules. The most celebrated of these are the bdelloid rotikrs, a p u p of
several hundred species in which d e s have never been discovered. Bdelloids are
o h represented as *thechief counterexample' to the evidence that dline-
ages are short-livcd (Stearns 1987). But they arc not alone. Several hmilies of ori-
baud mites, comprisii hundreds of species, are obligatorily parthenogenetic, as
arc numerous mm in the Prodgmam and Mcsostigmata (Norton et af 1993).
Despite the d t h of examples in the Acui, they have been virtually ignored
by most evolutionary biologists interested in the problem of all-&male
parthenogenesis. In contrast, mica have played a starring role in the develop
ment of sat-ratio theory (Hamilton 1967). Below we outline some of the out-
standing fkanuesof asexual reproduction in mites in the hope that someone will
take the ball and run with it.
Distribution of parthenogenesis in mites
Norton et al. (1993) catalogue the distribution of modes of reproduction in
the Acari. These can be categorised as: diplodiploid, in which both sons and
daughters are produced from fertilised eggs and have two sets of chromo-
somes; arrhenotob, in which sons arc produced h m unfertilised and
are haploid; and thclytoky, in which daughters are produced asexually and
retain diploidy. Examples of amphitoky (or deuteroky) in mites, in which
both sons and daughters are produced asexually, appear to be mistaken
instances of arrhcnotoky (Norton et aL 1993). Panhaploidy, also known as
pseudoarrhenotoky, involves the production of haploid sons from firdised
eggs that lose the paternal genome early in development.
Nothing is known of the genetic systems of the Opilioacaxihrmes or
Holothyrida but they appear most likely to be diplodiploid. All a& arc
diplodiploid with the exception of the thelycokous Amblyommri rorumhzhrrn
and HkmaphysaCri longicornk, the latter of which is triploid. The
Mesosupam contain representative diplodiploids, arrhenotokcs, thelytokes
and parahaploids. Of the last, the Phytoseiidat are the best-studied and, except
for a f m thelytokous species, most appear to be parahaploid
Among the Acariformes, the early-derivative h i l i e s collectively known as
the Endeostigrmta are about m n l y divided between thelytokous species and
bisexual ones, although it is not dear whether males of the latter taxa are pro-
duced sexually or arrhenotokously. Among the Prostigmata, all Parasitengona
appear diplodiploid, although there is one suspected case of rhelycoky in a
species of BalbuJtium. In other an,urhenotob is widespread and thelytoky
crops up in numerous lineages. Many species are known to be haplodiploid
but the relevant genetic mechanisms (arrhenotoky or parahaploidy) have not
been determined. As mentioned above, oribaridr indude a large number of
thelytokous species (about 10% of the ca 7000 spp.). Most of the lrmJning
species appear m be diplodiploid, with a smattering of haplodiploidsof m a r -
tain mechanism. In the Asugrmta most species are either diplodiploid or
urhenotokous, with very few examples of thelytoky.
One of the most remarkable things about Nonon et aL's (1993) survey of
genetic mechanisms in mites is how flexible they appear. Variation in repro-
ductive mode occurs within families, genera and even within species. For
example, the cyclamen mite Pbytonemus paUidzu (Tarsonemidae) appears to
 MITES: ECOLOGY,EVOLUTIONA N D B E H A V I O U R
have thelytokous and sexual popuiations. Occasionally, non-functional males
appear in othenvise thelytokous populations. These males oftcn produce few,
spermless spermatophores or exhibit hermaphroditic structures. Thii suggests
that the genetic machinery for constructing males is still present in the
genomes of many overtly asexual mites. The other point of note is that asex-
uality, panicularly in the Oribatida, is dearly not a n evolutionary dead end.
Thelytokous lineages have radiated to produce hundreds of species, much as
thev have in the bdelloid rotifers. The mediction from 'normal' genetics
wokd be that a s e x h lineages would soon'khaust variation and bec&e dan-
88 gerously homozygotic. Palmer and Norton (1992) did indeed find that, rela-
tive to sexual oribatids.- thelvtokous s~eciestend to show fmer mdtilocus
- - -
8
genotypes. However, mean heterozygosity was still high. Wrensch ct al.
(1994) suggest that the peculiar nature of mite chromosomes (they are holo-
kinetic and undergo inverted meiosis) may allow retention of diversity and
even genetic repair.
Given the wide occurrence and repeated evolution of thelytoky. do pat-
terns in the Acari support any of the hypotheses about the value of sexZ Norton
and Palmer (1991) surveyed the distributions of thelytokous species of orib-
atids. They found that thelytokous taxa were common in recently disturbed
soil habitats, including tilled and frequently flooded land. They are also more
common in deep soil than in the h c e litter layer. The authors note that
under these situations, the biotic diversity of the habitat is rather low, and so
presumably is the need to 'keep up with the Joneses' via sexual reproduction.
This supports the idea that sex is useful in biotically complex habitats. Other
evidence in Favour of this idea is that thelytokous endosagmarans are also very
common in deep soil. However, many of these thelytokes are small and the
average size of soil mites tends to decrease with depth in the soil W t e r ,
unpublished). Thus, it may be that that mate-finding is diEcult in deep soil,
thereby selecring against sexual reproduction (Norton et aL 1993).
In dermanyssine Mesostigmaca, thelytoky is common in soil-litter inhab-
iting species but of sporadic occurrence (Walter & Lindquist 1995). Most the-
lytokes appear to have close bisexual relatives and only a few taxa (e.g.
Protogamarelk, the Asca aphidioides species group) appear to have radiated as
asexual lineages. Again, small thclytokous species appear to be relatively more
common in deep soil. Unlike in oribatid mites, however, the distribution of
all-female parthenogenesis appears to be independent of disturbance and the
degree of biotic complariry of the habitat: both diiturbed habitats (e.g. agri-
cultural fields) and pristine forests have many thelytokous species (Wdter &
Lindquist 1995).
Thelytoky is also very common among oribatid mites that inhabit stable
habitats. For example, freshwater and bog-dwelling oribatids are often thely-
cokes. For these mites Norton and Palmer (1991) suggest that osmotic dam-
age co spermarophores may select for reproduction without males. This is
plausible, although water mites appear to have adapted very well to indirect
sperm transfer under water. Norton et at! (1993) note that thelytoky is remark-
ably rare among mitts that parasirk animals (only rwo ticks and one suspm-
ed parasitengone), while it is quite common in non-acarine animal parasites.
They offer no explanations for this relationship.
Sex-ratio manipulation
It has long been noted that for scxually reproducing animals, the mwt common
ratio of male to female o&ipring is 1:l. The selective h r e s behind this are quite
simple (Charnov 1982). Suppose chat in a population, male oflipring are rarer
than f d e s . Because sex is required for the production of oflipring, each male
mates with more than one M e , thereby achieving a greater individual repro-
ductive success than the f d e s . Parents that tend to produce male of&pring,
therefore, have more grandsflipring than those without such tendencies. In
subsequent generations, male oflipring become more common and the advan-
rage to producing excess males weakens, eventually resulting in an equal pro-
duaion of males and h a l e s . While this ratio is the norm in vertebrates, there
are many examples of invertebrates in which the sex ratio is very female biased.
Hamilton (1967) noted that this expected 1:l sex ratio was dependent on
there being a large, panmiccic population. He observed that biased ratios were
often found among arthropods living in reproductively patchy habitats and
where brother-sister rnatings were common. How might these characteristics
select for female-bied sex ratios?Consider the following population structure.
Habitat consists of 'islands' that are colonised by a single fertiliied female. The
female produces oflipring that mate on the islands and then the fertiliied
daughters disperse to alonise new patches. If a mutation arises such that a
W e prodaces tinver sons and more daughters, then that female will produce
a larger number of colonists than femdes with 1: 1 sex ratios in their oflipring.
This assumes, of course, chat the smaller number of sons are able to fertilise d l
daughters. This advantage of female-biased progeny is reduced as the number
of founding females per patch increases, for sons become more valuable when
unrelated daughters are aMilable to be ferrilied. The predicted oflipring sex
ratio when there is such local mace competition (LMC) is simply: proportion
males = (number of foundresses - l)/(number of bundresses x 2) (Charnov
1982). When there is a single foundrcss, proportion rndes = 0, meaning that a
female should produce only enough sons to be certain that her daughters are
m y W i s e d , When there are two foundresses, sex ratio is predicted to be 25%
males and 75% females. When three, then it is 33% males and 66% females,
and so on until a 1:l ratio is approached.
Bulmer and Taylor (1980) and W i o n and Colwell (198 1) considered what
would happen if multiple generations were spent in the original patch, and
&en a dispersal event took place in which mating occurred randomly beween
o&pring fiom &rent patches. Their models predicted that the more genera-
tions spent in the original patch, the more female-biased the sex ratio should
be, because high-bias patches produced many more colonists than low-bias
ones. This is a process of group selection, because it is only through the scruc-
cured nature of the populacion that k d e - b i a s e d sex ratios are selected (see
Sober & W h n 1998).
Hamiiton (1967) n o d that there was 'extreme economy in the production
of mald among parasiroid wasps, some bark beetles and thrips, and numerous
raxa of mites in which sex ratios were as low as 2 4 % male. In these species,
mating tends to occur between siblings, eirher in a host insect, the nest of the
parent or, fo? Tarsonemha, inside or near the body of the dead mot he^ The
rather gruesome incestuous mating of the latter has been popularised by Gould
MITES: ECOLOGY.EVOLUTIONA N D BEHAVIOUR
(1977). Clearly, these examples fit the idea of localid mating prior to dispersal.
Hamilton a h observed that many of these species exhibited arrhenotoky and felt
that this mode of reproduction readily allowed the female to control the sex
ratio of her offspring.
Thcre is a huge body of literature dealing with sex ratios in mites, fiu too
much for us to cover adequately. We therefbre recommend interested readers to
peruse the volume edited by Wrensch & Ebbert (1993). in which patterns and
causes of biased sex ratio in mites and insects are thoroughly reviewed. Here we
simply skim the s&ce of rhi sea of idormation and highlight evidence that
it hard to explain using conventional sex-ratio theory. Wrens& (1993) points
out that sex ratio is not fixed within a species, or within an individual h r that
matter. She notes that funale mites appear to control the h a i o n of eggs that
become females on a dailv basis, rather than over their lifetimes. So the 'ideal'
sex ratio may change, debend& on the stage of colonization, the quality of
h o d and the overall density of individuals in a patch (these hctors arc usually
.
in terrwi ned)
Kaliszewski and Wtensch (1993) surveyed sex-ratio evolution within the
Tarsonemina. Four families exhibit physogastric reproduction (see Chapter 4),
and the degree and location of incest varies among them. Males of +motes rrit-
in' (Pyemotidae) emerge from their mother's body first, help their sisters to be
'born' and then mate with them. In Luciaphorus hawen' (Pygmephoridae), mat-
ing rakes place withii the body of the motha. However, males will also mate
with non-sibling females that have 'escaped' fiom their ruptured parent before
their brothers got to them. K a l i i k i & Wrensch (1993) note that brothers
fight amongst themselves fbr access to their sisters. This aggressive bchaviour
makes sense when one rmlies that the brothers are not clones but haploid
rearrangements of their mother's genome. W~thinthe Tarsonemina, sex ratio
ranges from 3:l to 98: 1 in favour of daughters. Species with temporally patchy
b d supplies and those that are parasitoids of insects tend to produce very
Female-biased ratios. However, m e parasites, such as the tracheal mite of hon-
eybees, tend to produce only slighdy biased broods (2.4-4.4 females:l male).
Phytophagous species also tend to produce I w biased sex ratios (although the-
lytoky is common in some groups of plant parasites).
Kethley (1971) discusses the ecology of the quill-dwelling feather mite,
Sjvingophiloidcr minor (Syringophilidae). Fertilised females invade the open
umbilicus of developing quills of the house sparrow, Pmer dornczn'cus. As the
feather matures, the umbilicus doses. Typically, only one female colonised each
feather but occasionally as many as ten enter a quill. The h a l e lays 11-13
eggs, the first to develop always being a male and the remainder being fimae.
The foundress dies as the fim generation matures. The offspring mate among
thernsclves and these females lay 10-12 eggs, with only one male per mother.
When the second generation matures the calmus is packed with mites (usually
121 kmales and 10 males). Thus, one female 'produces' enough mites in two
generations to fill the frathers. There is lirtle support for the LMC prediction
of more males in multiply founded tiathers, as Kerhley h u n d that 'multiple
fbunders each perform similarly to isolated hales'.
Hamilton (1967) made special note of the correlation becween arrhenotoky
and extreme sex ratios because it provided a mechanism whereby females wuld
control the sex of her ofipring. Although this generally holds true fbr mites
(e.g. Tetranychidae, Tarsonemina), it is not true for a l l acarine taxa. In the
~h>oseiidae, which almost invariably have female-biased ratios (sometimes
up to 90% females), both sons and daughters come from fertilised eggs.
However, the paternal genome is destroyed early in embryopesis so that male
phytoseiids arc e&ctively haploid. Are sex ratios in the Phytoseiidae fixed or
can the f ' e d e manipulate them? Sabclis & Nageke& (1993) suggest that
they can to some extent, as f d e s at the start of their reproductive life typi-
cally produce a son first. They suggest that this may be insurance so that if no
other males are present, ehe fkmale's daughters may be fedisad by her son. As
well, the daily sex ratio produced by kmale Grrlcndromw oc&tcrlir was very
precise, as if controlled by the mother rather than being a probabilistic ratio.
Exactly how females might select which eggs are 'cleansed' of their father's
genome is not c l e a ~
Fiy,there are some puzzlin~,examplesof biased sex ratios in mites in
which no obvious way to b i i sexes exist. Water mites (Hydracarina) often
exhibit sex ratios in the field that are strongly biased either to males or to
f;emaes; however, they are a l l apparently diplodiploid Some of this can be
explained by the sexes having different lifcspans or phenologies, so that fbr
example, a sample in spring may show female bias while one in late summer
may be male biased. However, rearing experiments with Ncurnania and
Unwnicoh (Unionicolidae) suggest them is a subtle but significant 2:l bias
towards females, while di&nt female Amurirs manubriator (Arrcnuridae)
produce hmiiies that were either very female b i d , male b i i or unbiased
(Proctor 1990. Amnurus chromosomes appear to behave oddly during sper-
matogenesis (Sokolov 1954). Proctor (1996) suggested that sex-determination
in Arrrnurus (and perhaps in the unionicolids) may be similar to that in sdarid
flies, in which a parahaploid mechaoism can resulr in the production of all-male,
a l l - m e and mixedsor broods ( M a1938).
Immaculate conception:
did sexual astigmatans arise from asexual oribatids?
The belief that d t y is a 'dead end' is so ingrained in the general evolu-
tionary literature, that it is hard to believe that any asexual lineages contribute
much to biological diversity. So the concept of an a s 4 group giving rise to
a species-rich sexual lineage seems doubly unlikely. In various papers (Norton
& Palmer 1991, Palmer & Norton 1992, Norton ct ad 1993),however, Norton
has proposed that a sexual line-, the Astigmata, has arisen from an a d
one: uhypochthonioid oribacids.
This hypothesis has two major implications. The first is phylogcnecic the
Oribatida as aurendy defined exdudes the Asagmata and is, therefbre, para-
phyletic Norton et d (1993) discuss the pros and cons of redefining these
well-known groups and they fbel that the disadvantage of temporary raxonom-
ic confusion is outweighed by che benefits of a more dadistically truthlid' das-
silication. The morphological similarities between astigmacans and juvenile
oribacids overwhelmingly support the idea of the former arising fiom the latter.
However, the fact that the oribatids most similar to early-derivative astigmatans
belong to an entirely thelytokous group has much greater implications.
MITES: ECOLOGY,
EVOLUTION
A N D BEHAVIOUR

How can sex 're-evolve' from an asexual taxon with a long evolutionary those males best adapted to the sensory biases and morphology of females, seems
history? One possible mechanism is cyclical parthenogenesis. Although this a more likely scenario.
alternation of a s u r d and s e x d generations is common in aphids, it has never The idea of passive mate choice merges with that of intessexual conflict as a
been demonstrated in mites. perhaps the answer lies in the-occasional rcpro- driving force behind the evolution of male and female dadaptations. Males
ductive 'accident'. Spanandry refers to the appearance of a very few males in may benefit by insemimating funales that would ratha not be m a d , which
an otherwise extremely female-biased population. Spanandric males pop up should lead to an arms race between the sexes for conaol over f;crtilisation.
among the ofipring of many otherwise thelytokous raxa (Walter & Kaplan I n d confiia should be strongest in copulating species, where m& have
1990 c, Norton et a,! 1993) and they do not appear to function as sexually the possibility of tbrcing unwilling females to accept sperm. Secondary genid
active males. The oribatid ancestor of the Astigmata may have produced a rare openings in &male dennanyssine and astigmatic mites may have evolved
functional s~anandricmale that somehow encouraged a female to cake up his through intersexual conflict over the site of pcneu-ation, as it appears to have
sperm. one-difficulty with this scenario is that all istipatans transfer s & m done in the hcmipceran group Cimicoidca.
via an aedcagus, while there is only one documented case of semi-direct trans- Mites also excel in the opposite of sex. Asexuality has arisen many times in
fer amongst oribatids. This species is from the Galumnidae, a member of the the Acari, both as arrhenotoky (production of males fiom u n k i h e d eggs) and
derived group Brachypylina. In the phylogenetic hypothesis diagrammed in thelpky (asexual production of fkmales). No dear parrerns exist to explain why
Nonon ct al. (1993), the Astigmata and Brachypylina are shown tsuing from some taxa reproduce thelytokously whii related groups are sexual;however,
a common ancestral group, the Desmonomata. NO pairing species are known them may be a uend towards greater occ-urrence of thelytoky in abiotically con-
from this taxon. However, another ancestral group, the Mionomata, does stant habimts with low biotic diversity (e.g. deep soil). Sex-ratio biases in mites
contain a species observed to engage in a sort of pairing dance, CoUohmannia often fbllow the predictions of local mate competition theory but indude
gigantea Clearly, to support such a radical hypothesis, much phylogenetic numerous counter-examples as well. The huge number of thelytokous oribatid
study remains to determine the origin of the Astigmata. species presents a panicular problem for evolutionary biology. Not only have
they spedated and diversified - thought almost impossible in asexual Lineages
SUMMARY of eukaryotcs - bur they m a y have produced a very succcs&l group of
entirely sexual species, the Astigmata.
As in all things, mites are extremely diverse in their sexual habits. They display
a mind-boggling variety of sperm-transfer behaviours. This ranges fiom com-
plete dissociation between male and female, to, pairing and subsuate-deposited
spumatophons, to direct transfer of sperm via an intromittent organ. Sperm-
transfer behaviour is unknown in the Opilioacariformes and Holothyrida but in
the remaining Parasitiforma it is uniformly via copulation. T h e Acarikrmes are
more imaginative and display the entire range of possible modes. Copulation has
evolved dozens of times and water mites appear particularly prone to evoIving
direct sperm transfer. In both copulating and non-copulating taxa, sper-
matophores are seldom passive pedesds for sperm but rather they take an active
parc in atrracting and inseminating females. In particular, the spermatophores of
ti&, with their explosive sperm-delivery mechanism and helpful symbionts, are
astounding in their c o m ~ l structure.
a
Thereereare many c&mples of innasexually selected characteristics in male
mires. Males compete with each other for access to W e s through fighting (eg.
harem-keeping water mites), sequestering Fern* before they have emerged as
adults (e.g. Tmnemidae) or through trampling of other males' spermatophores
(many dissociated parasitengones). They may also do battle internally through
sperm competition which, although not as common as in inseccs, appears to
exist in some ticks and astigmatans. In contrast, overt &male choice seems are
or nonexisunt in the Acari. In copulating species, females are o h impregnat-
ed afier being 'kidnapped' (cg- in Tmnernidae) or whiie still in the bodies of
their mothers (e.g. in some Pygmephoridae). Among dissociated species, iris not
dear whether females can differentiate bccween spermatophores of &rent
males, a prerequisite b r active mate choice. 'Passive' choice, which selects for
 The soil ecosystem is tbc poor man? tropicalrainform
(Usher et aL 1982)

M
ore than any other habitat, the soil-litter stratum is the province of
mites. Densities of 50 000-250 000 or more mitts per square metre
in the upper 10 un of soil arc commonly reporred (Petersen 1982)
and a handfid of humus from a temperate forest may contain thou-
sands of mites representing dozens of species. Even parched, sandy soils are home to
many species (An& et al. 1994). This diversity and abundance translates into eco-
logical importance. Las than half of the energy fixed by the sun is respired by plants
and above-ground M webs; most is returned to the soil and its organisms
(Madidyen 1963). Litter, decaying vegetation, dung and animal remains accumu-
late on the surface of the soil. If thii organic matter did not decompose, then plant
growth would soon grind to a halt for want of essential nutrients. Microbes slowly
burn off detritus, stoked and dampened by myriad other soil organisms. Worms.
millipedes, termites, beetles, crustaceans, springtails, maggots, mites and others chop
and grind plant and animal remains; they move the bits through the soil profile and
release the nutrients bound up in biomass. The larger compostcrs, earthworms and
grubs, are the ones we tend to see, but in numbers of individuals and of species, the
microfauna dominate and they are mostly mites or mite food (Wallwork 1976,
Crossley 1977, Swift et al. ,1979, Seastedt 1984, Moore etaL 1988, Lavelle 1997).
Mesic forests with well-developed surhcc organic layers and a predominance
of fungal over bacterial decomposition are home to the highest diversities of mites
but even the driest, hottest and coldest of soils are dominated by Acari. Likewise.
the smelliest compost, herbivore dung and carrion are home to specific suites of
mite caxa A survey of the mites in these systems would take a book in iaelf, but
that is not our intention. Rather, we will commence with a brief review of the dii-
tribution of soil mites. Then we will take a more detailed look at the one system
where soil mites are the best known and, beyond any doubt, the most diverse
form of terrestrial life. Finally, we will consider the roles of soil mites in food
webs, gudd analysis, feeding behaviour, habirat partitioning and as bioindicators.

MITES AND THE RHIZOSPHERE

Half or more of all primary production is out of sight, below ground. Roots,
tubers, bulbs and rhizomes are resources for microbes, nematodes and d r o -
pods. In terms of plant health, mites are generally considered beneficial in
below-ground systems. They are major predators of root pests, especially nema-
todes, and only rarely nporced as feeding on below-ground parts of vascular
plants. The soil h u n a tend to be concentrated where resources are in greatest
supply. in the surfice litter layers and the area around roots in mineral soils -
the rhizosphue (Curl &Truelove 1986).
This conccnuation of species and individuals can be especially prominent if
the roots have been colonised by a diversity of darkly pigmented fungi, many of
. \
which are mycorrhiie (Klironomos & Kendrick 1995). These interactions
between soil mites and other components of the fiuna of plant roots are little
studied but are potentially of great importance for understanding plant health
and ecosystem processes.
DEEP SOIL
Mites usually escape notice because they are minute and hidden (ctyptozoic) in
litter and soil. Thqr may escape even acarological notice when they are deep
beneath our kt. Soil is rarely sampled below 15 cm (Kethlcy 1990) but mites
descend at least as deeply as roots penetrate and in some soils a fifth or more of
mite abundance occurs below 2 m depth (kice & Benharn 1977). Though kw
acarologists dig themselves deep into the soil profile, when they do, they find
strange and wonderful mites, such as the worm-like Nematalycidae (Schubart
1973, Coineau naC. 1978) or the enigmatic Pomeranaiidae (Price & Benharn
1976).
Traditional extraction techniques based on using light bulbs on dry soil to
drive mites out are effective only in organic horizons; flotation tedmiques are
usually required to find more than a trace of the abundance and diversity pres-
ent in mineral soils and sand (Walter et aL 1987b, Andd et at! 1994). These
mites may never approach the soil s u k but others commute up and down
the horizons rcgdady.
Mites can be involuntarily moved down the soil profile, too. A spectacu-
lar example was the explosion of Mt St Helens in the north western United
States that knocked down entire forests and buried Forest humus layers under
10 cm of volcanic ash. A year later, chis blanket of ash itself contained no
mites but the layers of humus it had sealed off from above contained numer-
ous oribatid mites going about their business seemingly unaffected by the
blast and entombment (Walter, unpublished). The alternating bands of dark
organic marter and lighter ash layers that one can see in road cuts in that
-
region testify to i u long volcanic history and probably also to layers of fos-
silised mites.
MITES AND DECOMPOSITION
In contrast to deep soil and the rhizosphere, the interactions between mites
and other members of the decomposer system are better understood, espe-
cially in ephemeral detrital habitats like dung, carrion, and rotting fruit or
fungi where predation is their primary mle. In the soil, mites conuibute to
the regulation of decomposition and nutrient cycling by preying on decom-
poser worms and arthropods, comminuting organic matter, feeding on
microbes, and vectoring microbial propagules (Seastedc 1984, Moore ct aL
1988, Bal 1992). This htter function may be of major importance. Although
most soil respiration is microbial, microbes have limited abilities to move
from one resource patch to another. Once the energy in a particular patch has
been expended, microbial biomass shuts down and remains dormant until
new resources become available. This has been referred to as the 'Sleeping
Beauty Paradox' (Lavelle et at! 1994, LaveUe 1997). The dormant microbes
require the 'kiss' of arthropod 'Prince Charmings' to awaken. This rather deep
kiss (i.e. ingestion) results in microbial propagules being mixed with fresh
resources in the f e d pellet, and often their transportation to new sites in a
manner that is directly analogous to the dispersa of seeds by fruit-feeding
vertebrate..
SOIL MITES IN A SIMPLE SYSTEM:
ANTARCTICA
The southern polar region is a huge expanse of ocean with numerous small
islands and one continent, Antarctica. More than 520 species of mites have
been reported from this area, mostly from subantarctic islands, marine collec-
tions (water column and benrhos) and as parasites of birds and marine mam-
mals (Pugh 1993, 1994). Although the acarine diversity of the subantarctic
region is respectable, the fiuna of the continent itself is much less diverse.
Except for narrow rocky coastal regions where the snow cover melts in summer,
windswept parts of mountain ran& and extreme desuts where precipitation of
any kind is rare, 95% of the Antarctic continent is covered with permanent ice
and snow. The lowest tunpvanues known on Earth have been recorded in
Antarctica (-89.G°C) but the lack of available water may be a more severe stress
to the arthropod fiuna (Cannon Q. Blodr 1988).
Exduding parasites, synanthropes and spurious records, about 50 species of
mites, 20 of ~pringailsand one chironomid midge manage to survive among
growths of cryptogams (cyanobacreria, green algae, lichens, mosses, liverworts)
in the tussocks formed by two species of vascular plants (a grass and a pearl-
wort), in accumulations of detritus around penguin rookeries and seal wallows,
in beach wrack and in the thin mineral soils (Block 1992, Pugh 1993, 1994).
Of the 30 or so mire species known from inland Antarmica, most are endemics
(Block & Smry 19%. Marshall & Pugh 1996). Antarctic mites ~IC interesting
in themselves, but as major components in the Ead+ simplest h d webs and
most extreme terratrial ecosystems, they offer us a means of addressing basic
questions about Food-web structure.
Antarctic mites
The oribatid h k o u t u an*~Minrris probably the best studied Antarctic mite
(see Blodc & Convey 1995).Adults are among the largest of Antarctic arthro-
pods (>I mm in length), arc heavily sderotised and weigh 200-330 pg. They
roam rhe ice-free patches of the Anrarctic Peninsula keding on algae, lichens,
and detritus. Herds of several hundred thousand h k o u t c s of all stages
have been found grazing on the foliose alga h w h c r i p a but they a h arc abun-
dant in intertidal debris, penguin guano, seal wallows, bird nesa and lichen-
encrusted rocks and bones.
A h k m can survive being hinto a block of ice but will die if their cis-
sues freeze, They tolerate cold by depressing their s u p u a ) ~ b point below the
minimum winter temperafure they eJrperiena. Adults have an average supercool-
ing point of ca -30°C and that of immature scagts averages s d degrees lower
(Cannon & Blodc 1988). As might be expected in a cold dimace with only short
periods above fiezing dcvdopmtnt is slow. Females usually accumulate 4 4 eggs
in their bodies and by them as a batch. Many femaes may use the same oviposi-
don site, d t i n g in Lyg.e masses of eggs under r o c k and in other sheltered spos.
Eggs hatch in the spring, 1-2 months a h being laid. At the end of summer froac
thaw cydes, incrcasing fiostr &ulate the immature mitcs m dear thcir guts,
secrete a n t i - k t s into their harmolyrnph and f$rm moulting dusters. The
moult to the next k x a r usually occurs the fbUowing spring and one moult per year
 MITES:ECOLOGY,EVOLUTION
AND BEHAVIOUR
is normal. Adult females do not produce eggs u n d their second year but thcy may
survive for several years and can produe several batches of eggs. &madon time is
at least five ye=. Mortality is primarily from fieainpj desiccation, scuvation and
p d o n , with the latterconcentrated in the earlier developmend stages.
About a dozen other species of oribatid mites in the genera Antarm'cola.
Antarctvacter, EZwardecta, Haloectcr, Liochthoniul, MageIloert# M a d d m i a
and Oppia are fbund on the Anmrctic mainland, grazing on d m lichens, hngi
and detritus, along with about twice as many species of Prostigmata One of the
latter, Nanorchcrttr an*urrinrs,has the &uthernmost distribution of any arthro-
pod (85'32's) and also has the widest geographic and altitudinat distribution
(3-2245 m) of any Antarctic mite (Blodc 1979, 1984). Hundreds of thousands
of these tiny (adult live weight = 3-4 pg) hopping mites can be found grazing on
microalgae in each square metre of some barren rodcy areas.
In less Qmeme coaseal sites, thick nrrfS fbrmed by mosses and oher bryophytes
are dominated by species of N a n o r h ~and t ~ other small p m s i p a m u with p-
-on times of 2-3 yeam (Usher & Booth 1986). As usual, the larger the animal.
the berccr known its f+ habits but small pmaipamm (eg. N ~ m c h x r ,
Eup& Apohioph9ctur) are thought to f;eed primarily on miaxalgae and hmgi.
Howrwr, Erryntta species am probably predators (Krana 1978, Zhang &
Sanderson 1993)-Grazing mites are most abundant in rich sites, such as the algae
growing on &then of long dead penguins (Grmitt & Shoup 1967). Species of
~~ are h e largest of the pnmipman herbivom at 600-700 pm in length
(3040 Clg). and are especdly abundant (20-2000 m-2) in mosses and lichens.
Compared to the interior, the Antarctic Peninsula is relatively diverse and
well studied. The Peninsula's fauna indudcs the only species of fm-living
Mesostigmata known h m the Antarctic mainland: GamaseUus tncm,ifertrfertr and
NydrogatnaseUus antarctin*r(Pugh 1993. Marshall & Pugh 1996). The latter has
not been well studied but GamarcIC1~~ mcovimi is the top predator in maritime
Antarctica and feeds on any animal it can overpower (Lister 1984, Block 1984,
Usher & Bowring 1984, Liter et al 1987, 1988). Other predators include the
prostigmatans Rbalgidia ge~lacheiand Tubcrosstoma kcchi in the Rhagidiidae, and
Errynetes macql~l~ticnris in the Ereynetidae.
Thc inland acarohuna of the fracn continent is composed of slightly more
than two dozen species of prostigmacans and three species of oribatids (Marshall
& Pugh 1996). Two species of Tubttostoma (formerly Cocmrha+) am the only
predators (Gless 1967). Many of the barren rodcy sites have only microalgae and
cyanobaaeria as primary producers at the base of the food web and a few
prosagmatans and nematodes as top grazers. The ice-fk Dry Valleys of
Southern Victoria Land ofren lack mites and have an impoverished fauna of
nematodes and the occasional tardigrade or rotifer (Fredrman & V i 1997).
An Antarctic food web
A simple way to express fkdng relationships is a hod web, ic a map of who eats
whom or w h a ~a picture of an organism's place in its tmphic univcrs.Like all art,
a tbod web is strongly in0uenced by the puccptions and abiliaes of its crcatot
Food webs can emphasise the consumers of a particular species or resource (source
webs) or of a particular consumer or group of consumers and their f$ods (sink
webs), or they can attempt to show all the &ding links of the organisms at a
particular geographical locality (communitywebs) (Cohen 1978). O n a more for-
d level, food webs also arc used to model the movement of nutrients and the
uansfer of energy among the components of an ecosyst~(Odum 1991).
Invariably, the consauction of food webs reflects the theory of wphic Iev-
els. Indeed, food webs are usually consuucced in trophic steps h m the basal
species (usually primary produ&rs or detritus) to the top carnivore and the
species within a trophic level are ofkn Iumped together, to one degree.or anoth-
er, to fbrm 'trophic species', guilds, and the like (Mwre af 1988. Hunt ct aL
1989). T p i d y , the larger the organism, the more likely it is to be treated as an
individual species in a fbod web. Simple food webs tend to resemble food chains,
ie. the pht-herbiirccarnivore sequence that reflects one of our most basic
views of ecosystems (and of our own place at the top of these systems). Upon
closer scrutiny, however, even very simple systems be&ne ensnared in a d&e
web of feeding relationships.
Food webs have been a central theme of the ecological literature but they
have been construaed with Iide consistency D i r e n t studies have covered
wide ranges of spatial and temporal scales,e.g. from ephemeral ponds to ocean-
ic systems, but have rarely reflected the dynamics of fiding links that change
over ecological or ontogenetic time or those that result from movement among
habitats. The vast rnajoriry of pubiiihed food webs were produced by field biol-
ogists as simplied illustrations of the feeding relationships considered impor-
tant for their study, not as standardised descriptions of community wphic
dynamics. These diagrams, however, have become the grist for a guild of math-
ematical modellen. The resulting 'hod-web theory' has had tremendous appeal
- at least judging fiom the frequency with which it has appeared in leading sci-
en&c journals, leavened with measurements, coated in jargon and sprinkled
with 'empirical generalisations'. Perhaps the major claim of food-web theoreti-
cians is that real food webs are kept short and simple by the c o n s d n t s of sta-
bility and energetics. We will examine this datn by looking at two measures of
-
food web complexity -chain length and extent of omnivory using a simple
food web from the least diverse continent on Earth.
. . .. webs can be considered to be com~osed
Food - - of one or more food chains.
The length of each chain is the maximum number of times nutrients and ener-
gy are transkrred fiom a non-consuming basal species to a top consumer, and it
is equal to one less than the number of species in the chain (Cohen 1978). For
example, Figure 6. la shows a simple sink web for the maritime Antarctic pred-
ator G a m z d w racovirzai on a mat of the foliose alga PrasioIn crispa that has
been colonised by the isotomid springtail Cgpojgp antdntinrs (Usher &
Bowring 1984). This system has a chain Length of 2, i.e. FNO fixding links unite
the three trophic species (one at each of three wphic levels). Primary produc-
tion at the base of the web is rcpresenccd by the alga that captures energy from
sunlight and nutrients from rocks or penguin guano to support its growth.
Gram, represented by the springtail, aansfbrm plant-captured solar energy and
numents into animal biomass that mpporrs the top predator G. *acovitzai We
could upand this web by adding someof the othe; grazers, e.g. Alazkoac~sand
Stmotydnrr viU0su1, to the middle wphic level; however, chis would simply add
two more chains of two links and not &a the mean chain length. We could
also partition Alarkozetes into two crophic species: armoured adults and a
soft-bodied immature stage. Since GarncLIcUus preys on the nymphs and larvae of
ALuRoec~s,but not the adults (Block 1984), the average chain length would
drop to 1.75 (i.e. three chains of length 2 and one of l a g & 1).
Mean chain length in published food webs ranges fiom 2.71-2.89 (Polis
I99 11, i.e. energy and nuuients produced by basal species pass through only 2-3
additional mphic levels on average-That a food web in one of the most extreme
habitats on Earth is a bit on the short side is not surprising and our simple web
suppom two of the strongest empirid generalisations alledged by hod-web
theory: real food webs have short mean chain lengths and ornnivory (i.e feed-
ing at more than one trophic level) is relatively rare ( P i 1982). In general.
the greater the number of links in a fbod web, the less mathematically stable it
is. Links caused by omnivory are especially insidious because an omnivore both
competes for resources with other consumers and preys on them (Pimm &
Lawcon 1977. 1978, P i 1982).
As an acample of the problems that omnivory can cam, suppose that
Giunarck fkd omnivorouslyon the alga as well as on the sprhpil. According to
theory, such behaviour is uncommon because the intermediate spaies would tend
to be squeezed out Thus, if model parameters allowed GarncLIellur to both graze
on algae and prey on sprinpik, a relatively larger predator population would
develop. More predators means both more predation on the springrails and h e r
algal r e s o w to support springtail populations. Eventually, spspringrail numbers
would dip to zero and the model predator would have only green algal slime to tat
But. GarncLIck does not eat algae and F i 6. la does not have those prob-
lems - it is short, simvle and stable. All we need do is tadr on some eauations.
form some gcncralisati&s about simple fbod webs in cmune habitats A d send
the lot off to Namr or Skience. However, if an editor should be so misguided as
to send the paper to an Antarctic ecologist fbr review, then we might encounter
a snunblig block Even a relatively simple maritime Anmctic food web based on
mats of a single species of alga is W y tb entangle a diversity of mites and other
invutebcates living in the surrounding primitive soils, lichen encrusted rocks,
moss d, e t c (Block 1984). Appearance of these animaL on a parricular algal 1
mat will depend on distance from source populations, weather condiaons, the
presence of appropriate cues (e.g. prey must colonise h e algae b&re a scuching
predator is likely co remain)and other stochastic h r s (Kitchii & P i 1985,
Kitching 1987). but eventually a more complete community web will develop.
Figure 6.lb shows a more comprehensive set of feeding relationships based
on the available Literature (e.g. Fiasimons 1971, Blodc 1984, Lister 1984, Lisrer
eta/. 1987.1988. Cannon & Block 1988). our own experiencewith soil animals
and consulrations wich Antarctic researchers. In this representation, 13 trophic
species, 30 feading links and 7 trophic I d are shown. Two differences from
F i e 6.la are immediately obvious: (1) mean chain length is much more dif-
ficult to calculate and (2) tieding at more than one trophic level is common. The
top predator Gamasek, for example, feeds on all of the trophic levels beneath
it except for the alga, and most of the grazers f d on at least rwo trophic levels.
Therchre. rather t h a being rare, omnivory appears to be an imporrant W n g
strategy in k-living Antarctic arthropods -as it is for many animals, indud-
ing ourselves (Walter 1987. Sprules & Bowerman 1988, Pimm 1991).
The longest of the uadiaonal (unshaded) food chains in Figure 6.1 b result
from three simple changes. The first is including another predatory mite in the
system, the prostigmatan Rbagidia gmlachci, a monster of 1400 pm length
(Strandtmann 1967). The second is partitioning the arthropod grazers into six
trophic species. Even thii level of resolution, however, is a simplification. Only
the five largest grazers (three springtails and two mites) are ueated individually:
small prosagmatans and oribatidsare lumped into a single uophic species -
'small mites'. The final chanee is indudine another rsource/consumer in the
system: fhgi. An algal mat E actually a &mplex of algae and other miuoor-
ganisms that focd on the algae and on each other, and in turn are eaten by larg-
er organisms. Fungi are caten along with algae by most larger consumers and are
prefurntially grazed by small mites. The new feeding relationships account for
six chains of length 2 (alga-consumer-rop predator), five of length 3
(alga-fungi-grazer-top predator) and four chains of length 4 (alga-fungicon-
sumer-RhagidLwop predator) for an average chain length of 2.87. Therefbn,
by adding more realism to the f;ood web, we have been able to raise a simple
Antarttic system, completely free of vertebrates, to the upper end of the chain-
length averages reported fbr a l l food webs (Polis 1991).
Additionally, Figure G.lb shows a simplified bacteria-basad cornparunem
(shaded) in the food web. Although often ignored, nematodes, protozoa and
bacteria are invariably present in any food web and the Antarctic Lno exception
(Block 1984, wncent 1988). In even the simplest of Antarctic food webs - in
MITES:ECOLOGY.EVOLUTIONA N D BEHAVIOUR
the Dry Vdcy deserts -microbivore and predator-ornnivore nematodes can be
found (Fdaxmn & Ross 1997). Adding even this simplified bacteria-based
compartment also adds two chains each of lengths 4 , 5 and G and one of length
3. As a result, the mean chain length inuares to 3.45 -considerably above the
average range daimed for all fbod webs.
The longest chains d t h m the pivotal position and the b r d diet of
GamascUw. Like many predatory soil mites (&?alter ct d 1988), GamzscU.is a
generalist that attacks most of the invertebrara of appropriate size that it
encounters (Block 1984). Effoaivespeckhation may result Cmm habitat pref-
erences of the predator, size changes in the predator during ontogeny,mterac-
' draw of those relationships (Polis ct aL 1996). Real systems arc so complex that
tions with other predators or variations in relative abundances of prey. Howevers
predators arch as Gamasclluz that actively search for prey (see page 112) will
encounter a variety of acceptable prey types over their lifetime and success at
prey capture and feeding will be primarily a h c t i o n of prey defcnas (see page
117). Such opportunisticpredation resulting in broad diets is not limitad to soil
mites aud is not rare (Polis 1991).
Grazers also have kding behavioucs dut ddy simple uophic clsdfiotion.
For example, we Mdit our nematode 'mphic spedd with d o w i n g only bac-
teria and protozoa but, in d r y , any organic bit of the appropriate size would be
s w a l l d , induding miadgac and fbngi (yeam; small conidia), which would
add more, longer chains to the web. Other maritime A n w c nematodes fked
only on h g i , are predators of other nematodes or eat just about anythkrg (Spaull
1973). The only aduopod known to be a predator of nematodes in chis r y s ~ l is
C;.anrrlbrr (Block 1984) but the isommid spriagailt undoubtedly eat nemamder
as they garc algae and detritus (dotad lines in Figure 6.lb). Although there is
good evidence that grazing mites and springtails actively supplement their diet
with nematodes competing for the same microbial rsoutce (\JCralter1987b), such
deliberate consumption is not a prerequisite of en- flow and nutrient tmnsfkr.
Although the information content of Figurc G. 1b far exceeds that of 6. la, it
is still a gross simplification of the maritime Antarctic fwd web. For example,
two species of rhagidiid mites inhabit the Antarctic Peninsula (Saandanann
1967, Zacharda 1980) and their presence can rffm prey selection by Gizrmrurllw
(Usher ct nl 1989). Rhagidiids may feed on larvae or nymphs of Gamascks
adding a loop to the web (Polk 1991). The other maritime A n d c mesostig-
matan, Hydtog-cllur amarcrinu, occurs in habitats similar to those of
Garmar& (Pugh 1993) but none of the possible interactions between thae
species seem to have been explored. We present Sttrcotyuh as a &a herbivore,
although it also may foed on f i q i (Fimimons 1971). The small mite 'mphic
species' may contain both fungal and algal specialists and probably contains one
predator, E ~ c ~m q ~ r i m rwhich k , may fked on small mites (including
immature stages of the larger arthropods), eggs or nematodes. Akzskoactcs has no
way to avoid eating protozoa and bacteria that live in the algae and may 'acci-
dentally' graze on nematodes. None of the W a c k loops from higher to lower
trophic levels are shown (rg. h, mr& and death-providing resources for
microbes algae and arthropods), and disease and cannibalism arc ignored.
Bacteria, fungi, protozoa, nematodes and small mites are complexes of species
but all are treated as if they are single 'uophic species' and other groups are
entidy ignored (e.g. viruses, d g r a d e s ; rotifers).
As additional species and links arc added to this web by more detailed stud-
ies -or as layers of complexity are added through consideration of seasonal or
-
lifk-stage variations in M n g or the relative strengths of d i f k n t links the
variok bod-web metria h-t have been will vary widely. Antarctic
webs arc not unique in this respect, Food webs are merely d h p m m u i c sum-
maries of our knowledge about feeding relationships in particular systems -
useful tools for generating hypotheses about community organisatin (Wilbur
1997). Understanding these systems will come b m studying the organisms in
them, not &om analysing the dynamic constraints of the simplistic diagrams we
even detailed community food webs arc rarely more than grotesque renderings
of a d relationships and the pattcrns they show d e c t the limits of the analy-
ses more than they-depict an~ecosymmbr evolutionary trends (Moore et r;L
1989, Polis 1991).
The use of species or mphic species as black-bod system variables may be
us&d br mqdelling energy and nutrient dynamics and understanding con-
straints on ecosystem-level processes. Howeversic is important to remember that
it is energy, nor organisms, that flows through ecosystems, temporarily residing
at &rent uophic levels. Organisms use enexgy h m many levels within their
ecosystems and selection fivours survival and reproduction, not stable mathe-
matical modeis. To paraphrase Robert Paine's (1996) commandments of food-
web research: avoid jargon; let nature guide mathematics, not vice versa; honour
species; and pay attenaon to small organkms.
FEEDING GUILDS AND FUNCTIONAL GROUPS
Ecological interactions ouxv among individuals and can change with lik stage,
season, time of day, physiological need or in response to many other variables.
Studying all of the species plus all of their interactions is a daunting task, even
in a simple ecosystem like maritime Antarctica. In more complex systems it is
virtually impossible. Therefkc, community ecologists must reduce that com-
plexity to a manageable size. Two common, if intellecfcLaUy vacuous, approach-
es to dealing with the diversity and complexity of soil animals have been to sort
them into coarse taxonomic or size categories. Not surprisingly, counting the
total number of mites, or mites per suborder, in various samples provides plen-
ty of tedium, but little insight. Size categories, e.g. microfiuna (< 100 mm),
mesofkuna(100-2000 mm) and mqpfiuna (> 20 mm) (Swift ctd 1979, Beare
et aL 1995), at least cut across taxonomic boundaria -soil miw primari-
ly into the mesofiunal category, along with other arcane groups Lik springtails,
pawpods and symphylans. However, size categories tend to be used as conven-
ient srcwes for ignoring organkns that arc larger or smaller, rather than for
d y i n g the relationships betweenbody size and d w a n t ecological fbcmrs such
as soil-pore size.
~naltunativeto arbitrary size or taxonomic classification is based on the
hypothesis that communities are composed of dusters of firnctiody similar
species. The most popular term h r such a duster is guild Root (1967) origi-
nally proposed the term to describe the birds on a Calibrnia hillside that
obtained most of their food by gleaning insecc prey from oak foliw. He argued

that studies of assemblages of organisms thai used biilar resources in a similar
manner were ecologically relevant alternatives to studies based on taxonomy. To
Root, guilds reflected ecological relationships ainong species much the way that
V e r a reflected phylogenccic relationships. He also explicitly stated that com-
petition for resources was inherent in guild membership and was the primary
reason that guilds were relevant for study.
The word 'guild'has been a dear success but a shadow has Men between def-
inition and use Uaksic 1981, Walter cf aL 1988, Hawkins & M d a h o n 1989,
Siberloff & Dayan 1991). Rarely has competition been shown to be limiting,
or even strong, within guilds; and typically, guilds are defined with little concern
as to the full range of species using similar resources in a.similar manner.
Although Root might argue that only birds could glean insects from f o l i i in a
similar manner, one wonders why none of the predatory insects and spiders,
stalking insecrs in the foliage or hawking from perches in the canopy, did not
qualify. The answer is simple. Almost invariably, and usually implicitly. the first
criterion of guild membership has been belonging to the cixonomic group of
interest, whether it is vertebrates, b i i mites or the like. Some authors have pro-
posed terms for more finely resolved guilds, c.g. feeding guilds, leagues or ensem-
bles (eg. Walter etaL 1988, Faber 1991, Fauth etaL 1996) but none come to grip
with the inherent taxonomic bias and untested assumption of cornperition.
Originally, a guild was a group of like-minded people organis& for m u d
aid and protection -a concept at odds with Root's (1967) anlagonistic ddini-
tion (Simbcrloff & Dayan 1991). In the botanical literacure, plants that are
interdependent at some 1 4 , from m u d i m through commensalism to para-
sitism, have been called guilds (Amam& ODowd 1976). In the zoological liter-
ature, 'guild' has been used to enhance the ecological impoftance of h o s t any
Iwd of ecological association from congeneric pain of species to mass collcccions
of unrelated animals. Acarological studies are well within the zoological main-
stream with guilds deCincd as assemblages of congeneric parasites using s i m i i
hosts (e.g. Downes 1986), astiginatam migrating as hypopi from ephemeral
habitats (Kniille 19951, predatory mesostigmatans of similar size and reproduc-
tive mode (Water & Kaplan 1990~).predators using diering pursuit and inges-
tion modes (Walter et QL 1988) or oribatid mites with similar feeding
capabilities (Siepel & De-Ruitcr-Dijkman 1993, Kancko 1995). Other studies
tend to ignore mites or to lump them with other poorly understood groups into
such guilds as 'other predators', ic predatory arthropods that are not insects
(Stork 1987). In fact, guild can have any number of meanings, and thus no
meaning (Siberloff & Dayan 1991).
A uscll alternative to guild was proposed by Cummins (1974), who divided
saramdwelling animals into fbctional p u p s based on the size of the fbod par-
tides chat they c a p d Although i a subsequentdetinition has con+ on guild
by induding the manner in which the resourcesare used, and some consider ' h c -
tied group' a less elegant synonym of guild (Dayan & S i b d o f f 1991), in prac-
tice functional groupings have been more consistendy applied and kdr the
assumption about the i&nana of competition among ~eArnbus. By co-mt-
ing on mource use first, taxonomy second and competition not at all, the h c -
n o d group concept o& f a fim approximation to dencirjring clusras of species
that may be ecologically Linked Democl~tratingwhere and when these links may
I & SOIL SYSTEMS
MITESI N DETRITUS
I
iduence the n&tenancc of soil biodiversity, decomposition ram, nutrient
, dynamics or other eoosysrun fiuraions should be a usdirl goal of soil -logy.
Below, we consider the major h c t i o n a l groups of soil organisms that have
mites as members. Each group is defined by the resources used, modified by
what we believe are ecologically important di&rcnccs in use and raking into
account how the use of resources by one group may change their availability to
other organisms (Jones n aL 1997). Where relevant, Life history racrics are dii-
cussed as well (see Siepel 1994). Fun&onal groups are usell heuristic devices
for considering the trophic roles of miox in pamcular habitats - but they are
hypotheses, not k. Sice rhk is a book about mites (and long enough as it is),
we will concentrate on the acarine munben and onlv brieflv consider other
organisms that may process resources in a similar manner. Also, membership in
a functional group is not necessarily exclusive - an organism may belong to
more than one fimctional group over irs lifirtime. Functional groups made at a
coarse level of ecological function arc preferable to those based entirely on tax-
onomy or size; however, finer subdivisions of these functional groups will ofien
be appropriate (e.g. Walter et aL 1988, Faber 1991, Sicpel& De Ruiter-Dijman
1993. Siepel & Maaskamp 1994).
Comminuting microbivore-detritivores
-grazers & browsers
Most soil-inhabi~gsarcoprifonn mites (Oribatida, Astigrnata) feed by biting
off spores, chunks of hyphae or strands of algae and swallowing hem. Some of
the larger and more heavily sderotisod oribatids carry chis feeding one step fix-
ther by eating dead vegetation and animal material (saprophagy) d m support
microbid growth, and so they directly contribute to the reduction of detritus
(dead organic mactcr). During feeding, a bolus of food panides accumulates at
the base of the oesophagus and as it passes through the venmdus it is covered
by a thick pericrophic membrane. As digestion continues, the pellet passes along
the gut until it is eventually defecated. Oribatid droppings are compact and gen-
erally smooth-su&d particles, up to 200 x 140 pin size, without the min-
eral indusions ofien found in the fecal pellets of other soil animals (Rusek
1985). Microbial spores within these pellets are often viable.
Sod-inhabiting oribatid mites are known from the earliest turestria hums
(Norton ct aL 1988) and pdculate f d n g is probably the ancestral state in this
taxon (Norton 19851. The earliesr oribacid mites, alone with the carliest coilem-
b o b ; may ha& gazed ptimarily on the microflora Zbeaches and earIy term-
trial soils, much as A l u k o m dnanticw does today. Saprophagy probably
developed as a means of capturing s u M e microbial tissues (Norton 1985) -
eating the pie crust to get at the fillin%. 'Saprophages' tbed on both detritus and on
l i g mihbes, and sometimes exclusively on the lamer (Behan & Hill 1978.
Behan-klleticr & Hill 19831 but either diet leads to the formation of small oarti-
cles that contribute toki &ucture. Oribatid W pellets have been major A m -
ponetats of soils at least since the Carboderous In coal beds formad by ~ l a n t in s
l k n q b m h swamps,both aerial and mot remains of dub mosses, sphenopsids.
ferns, seed ferns and cordaites contain oribatid borings and b (Iabandeira et
aL 1997). The reduction of detritus and patches of microbial biomass to small pel-
lea is a direct engineering of the habitat and results in the production of

MITES: ECOLOGY,
EVOLUTION
AND BEHAVIOUR
microhabitat spa- that can be used by smaller mites, nemamds, protozoa, fungi
and bacteria. By burrowing duough i n d tissues of decaying vegetation, sar-
copdform mites both m u pore s p a s and dispuse microbii propagules. Mim
appear to have limited abiiaa to directly modify pore structure in mineral soil
(Norron 1985) but, at least in dry soils, some of the krger species are able to bur-
row among soil aggregates (Tevis& Newell 1962, Coineau 1973).
When a miuobivodeuitivorc fix&, it may obtain nutrition fiom ingest-
ed material in a variety of ways. For example, to some mites, fungal spores may
be much like fruit is to many vertebrpm: a rvty and digestible o u m coating
with an indigestible core. However, when living cell walls arc ruptured during
feeding, the cell contents become a rich source of food. For sucking-microbi-
vores (see page 108), these cell contents may be the only source of numents.
Miuobivorc--deuitivores, however, ingest d walls, as w d as cell contents.
Mites that are able to digest the structural elements of cell walls have extra nuui-
ents available. Additionally, dead cells (microbial as well as those of higher
plants) then become a viable food. Coprophagy is a simple, and probably com-
mon, meam of obtaining nutrition fmm cell-wall materials by reinge-stingheces
aftcr microbial digestion has taken place in the 'external rumens of the soil
(LaveUe 1997). However, some mites may be able to produce the appropriate
enzymes themselves or through a mutualistic assodation with gut microbes (see
discussions in Norton 1985, Sicpel & De Ruiter-Dijman 1993).
Recent attempts to refine the guild structure of oribatid mites have
emphasised enzyme capabilities and have spawned a swarm of feeding guilds.
For example, Siepel & De Ruirer-Dijman (1993) pulverised 50 species of sar-
coptiform mites and measured the activity of their carbohydrases on car-
boxymethylcellulose, chicin and uehalose (Siepel 1990). The production of
glucose after incubation with carboxymethylcellulose was interpreted as an
indication of the presence of cellulase in mite guts and as an ability to feed on
'greed plants, i.e. algae and vascular plants that have cellulose in their cell
walls. Thiryfour spcaes had cellulase activity and 16 species showed no e l -
Iulase activity. Chitinase or uehalase activity was interpreted as the ability to
digest, respectively, chitin in fungal cell walls or carbohydrates stored in fun-
gal cell contents. Twenty-five species showed chidnase activity and 39 species
were able to digest trehalosc Seven possible combinations of activity and inac-
tivity of the three .enzymes are possible, and all seven were found.
Siepel & De Ruiter-Dijman (1993) then assigned digestive capabilities to
each mite and divided their 50 species into seven guilds based on each of the
possible combinations of enzyme activity/inacavity. Even the one species with
no demonstrated carbohydrare activity was assigned to a guild! Although the
industry of these workers should be applauded, the conclusions need to be
talcen with a grain of salt. For example, Sicpel & De Ruiter-Dijman (1993)
assume that the ability to digest mehalose or chitin denotes fbgivory; howev-
er, neicher compound is restricted to fungi. Although they have some discus-
sion of the distribution of these compounds in plants, the presence of
mehalose, chitin and N-acetylglutamine in nematodes (Nicholas 1984), a
known food of many sarwptiform mites (see below), is ignored. Also,
chidnase should be present in animals with chitinous exoskeletons irrespective
of their diets.
I & SOILSYSTEMS
MITESI N DETRITUS
I
I
I
I
1
Earlier attempts to classify oribatid feeding behaviour were based on the rel-
ative proportion of various types of food in gut contents and emphasii the role
thae mites play in the comminution of organic matter (Siepel & Maaskamp
,I 1994). Although the jargon that developed tends to obscure rather than clarify
feeding habits, certain panuns arc dac large species consume more demnu,
I
medium-sized species consume more fungal hyphae and small species tend to
fccd on &gal spores or 'amorphous' material (Schwer 1956, Anderson 1975
a, ba 1978a, Lunon 1972.1979). Species fading on dmying plant mzmr tend
to have massive chelicerae (Kuleko 1988). P&rences Tor particular laourar
can be related to digestive capabilities and can vary between adults and juveniles
of the same species (Siepel1990). The distributions of some sarcopriformans are
positively corndated to the amount of &gal hyphae and the diversity of darkly
pigmented fbngi present in the soil (I(lironomos & Kurdridc 1995). However,
rhss are general trends and most s~coptiformansappear to be highly oppor-
tunistic in their choice of foods (Behan & Hill 1978, Behan-Pelletier & Hill
1983, Usher ct aL 1982, Norton 1994, Siepel 1995).
One especially relevant opportunism is kcultative predation. Many other-
wise decent fbgivores will take small, defenceless animals such as protozoa,
rorifers, nematodes and collemblans when the opportunity arises (Rockm &
Woodring 1966, Rockett 1980, Walter et aL 1986, Walter 1987b, Walter
1988b, Wdtcr et aL 1988, Walter & Kaplan 199Oa, Norton et aL 1996). This
behaviour can result in effects much k t h e r up the hod web when oribatid
mites ingest the infective stages of mpeworms, become intermediate hosts and
are ingested by mammals (Sengbusch 1977). Feeding on algae is also very
common and, fmm an ecosystem point of vim, algae arc primary producers
and their consumers are herbivores.
So, microbivor+deuitivores are especially difficult animals to assign to a
simple uophic category. Depending on the habitat, time of year or stage, a
particular individual may be a predator, herbivore, fimgivorc, sapmphage or
omnivore. In all cases, however, this feeding contributes directly to soil struc-
ture through cornminution, inoculation (many ingested microbial propagules
pass through digestive tracts without damage) and the formation of fecal pel-
lets. Grazing may also have a strong stimulatory effect on the growth of h n -
gal hyphae (Visser 1985, Moore et aL 1988) and remove significant numbers
of fungal propagules (Gochenaur 1987).
Mites that function as microbivofo-deaitivoresdLpcne primarily as adults,
have long-lived tdults, relatively long generation tima, arc d y p h o d c and
have repeated bouts of reproduction (iteroparity). These trends are characteristics
of oribatid mites, which ye the primary mite constituents of chi group and these
&history traits may say more about phyiogcnetic inertia than about adaptations
to the grazing role (Norton 1985, 1994). For example, stigmacans in the genus
T j g w arc common in some soils but have relatively short generation timer
(Wdm a aL -1986), and other soil-inhabiting kigmata use phonay m disperse,
Similarly, most graze& are bisexual and diplo-diploid but thclytoky is common
and arrhenotob known in some taxa (Norton et aL 1993).
In addition to the sarcoptibrmans discussed above, many collunbolans,
insects, crustaceans and myriapods h a i o n similarly in soil litter. In Australian
forests, talitrid amphipods, osuacods, isopods, millipedes, the catcrpillm of
 MITES:ECOLOGY,
EVOLUTION
A N D BEHAVIOUR
m p h o r i d moths and the grubs of cryptoccphaline chrysomelid beetles are
important processors of surface litter. Their f;ecal pellets provide an additional
resource for the mostly smaller sarcoptibrmans and the larger of these arthro-
pods no doubt act as incidental predators when they consume immature stages
of oribatib and other small animals that burrow in litter.
Piercing-sucking microbivores
Prostigmatans M only on fluids -that is they pierce their host with stylet-like
I
108
chelicerae and drain the fluids and externally digested remains of their food.
Mycophagous Prostigmata (e.g. Eupodidae. Tydeidae, Tarsonemidae,
Scutacaridae, Pvgmepboridae) are o h very abundant in soil-litter habitats,
especially in d m , grasslands and dry forests ( W e y 1990. Curry 1994).
Some small oribatid mites with attenuated mouthparts (cg. Suctobelboidea)
appear to M primarily on fluids (they do not form gut boluses). This is also
true of a number of firdies of Endeostigmata (Walter 1988b). Sucking miao-
bivores tend to have relatively short generation
- times and to be more variable in
time and space compared to grazes.
Piercing-sucking is functionally d i k t from parride fieding for a number
of reasons. Most obviously, prostigmacans directly contribute little to soil struc-
ture.They do not comminute limr and their fieces Zue liquid, so only their exu-
viae and bodies are added to the physical s a u of~soils. In some sense, their
focding is more Likc parasitism than grazing, especially in physogastric heterostig-
matans that a d to a hypM mass and become engorged (Kaliszewski et aL
1995). Fungal spores are no; ingested and any moveme& i f microbial propagula
must be of those adhering to their cuticle or sequestered in special myarngial
pouches or spomthecae (~ind~uist 1985). Also, &kers m o t use their mouth-
pam to bore into derricus to obtain rniaobes benearh the su& Algae and
nematodes are fed on by some sucking 'fungivores' and, as in grazers, a simple
vophic classification can be misleading. Aradid bugs, nean+e coUernbolans,
tylenchid nematodes and proturans feed on fungi in a similar manner.
Filter-feeding microbivores
Hitiostomatid astigmatans are the only mites known to filter bacteria, yeasts,
protozoans and ~ r fine y particulate organic mamr for a living w a t e r
& Kaplan 1990a). Their chelicerae and palps are modified into brushes
that sweep fine parrides towards the narrow (5 mm diameter) buccal opening.
These mites arc common and often exawnely abundant in any kind of
wet, decomposing organic matter, e.g. carrion, rotten fiuic, rotting h g i ,
sap fluxes and wet lim Generation times are relatively short and dispersal
is by phoresy of the heteromorphic deutonyrnph, usually on an insea. Rhabditid
nematodes, some maggots and copepods filter feed on similar resources.
Direct plant parasites
Root-grazing or -sucking insects, plant-parasitic nematodes and fossorial
mammals are well-known below-ground herbivores (Andersen 1987) but
mites that feed on below-ground parts of higher plants are poorly studied.
Some tecranychoid mites (Tuckem&, Linotemnw) are common in soil samples
I
from grasslands and open forests (Smith-Meyer & Ueckermann 1997) and
possibly feed on the crowns or roots of grasses. The above-ground parts of
grasses and herbs are attacked by a variery of eriophyoid and tecranychoid (e.g.
Bryobia, OCigonychus. Tmanychrrs) mites that sometimes seek refuge in the soil.
Algae and bryophytes on the surfice of the soil and on logs and rocks har-
bour a diversity of prostigmatans whose darkly pigmented internal body w n -
tents probably represent chlorophyll and its breakdown products. Species of
Edpreus, an aberrant genus of the mostly predatory Stigmaeidae, hed on
mosses (Gerson 1972). The Penthalodidae (Smotydnrs, P~mthalodcs) are
thought to feed on moss leaves. The closely related earth mites (Penthaleidae:
iY,aloydnrJ, C h m m o t y ~PmthaCws, LinopenthrsCnrz and Linopenthalodcs)
are parasites of low-gowing planrs and, as their name implies, are often fbund
in soil, as arc the large, long-legged Eriorhynchidae (Etiorbychus) in
Australian forests (Qin & Halliday 1997).
Oribatid mites are occasionally reported as boring in live roots or tubers
but these attacks are probably secondary after damage and invasion of plant
tissues by fungi. Few records exist of oribatids burrowing into healthy plant
tissue except in aquatic habitats (Krantz & Lindquist 1979). However, some
astigmatans, especially species of Rhiwg&phur, can damage tubers or other
underground storage structures or seeds (e.g. peanuts). These mites seem to
feed at the juncture of healthy and fungus-infected tissues, and avoid decayed
tissues. Many sarcoptiform mites feed directly on algae and lichens, and so act
as herbivores in an ecological sense. In general though, mites are not impor-
cant below-ground plant parasites - at least not directly.
Indirect plant parasites
Mycorrhizal fungi are ‘digestive mutualists' that colonise roots, infiltrate the
rhizosphere soil and sequester and vansport phosphorus, nitrogen and other
nutrients into the roots of higher plants in return for carbohydrates (Lavelle et
d 1995). So, these hngi are mutudistic extensions of the roots of plants.
When mites and other soil animals feed on mycorrhizae h e y are, in effect, also
feeding on the plants. By removing senescent mycorrhizal biomass, dispersing
the propagules of mycorrhizae or atracking plant-parasitic fungi in the rhizos-
phere (Wiggins & Curl 19791, thii grazing may be beneficial to plants. Also,
some mpxrhizae may preferentially form their spores within the shells of
dead oribacids mites (Rabatin & Rhodes 1982). However, high densities of
mycophagous mites, especially of sucking h g i v o r e s or other fungal-feeding
soil arthropods and nematodes, may reduce the effectiveness of mycorrhizae
and limit plant growth (Edwards & Stinner 1988, Lussenhop 1992,
Klironomos & Kendrick 1995).
Nematophages
One long-neglected aspect of soil ecology is the relationship between nematodes
and mites. Thii neglect is not es+y surprising, since the serious study of free-
living and plant-parasitic nematodes is an even younger discipline than acarolo-
gy. Historically (and b i i e l y ) the study of soil-inhabiting nematodes - plant
parasites, bacteriavores, fungivores and predators - is a discipline within plant
 pathology-, rather than zoology. As a result, few soil zoologists know much about
nernatodes and, when plant pathologists look fbr natural enemies of nematodes,
tk tend to concentrate on m i d i diseases, nematode-trapping h i and
predatory nunatodestodes However, understanding the population dynamics of soil
mites and soil nematodes requires understanding that fbr many mites, especially
MeSOStigznata, nematodes are a prdkred prey (Karg 1961, 1983, Muraoka &
Ishibashi 1976, Sharma 1971, Stirling 1991, Van de Bund 1972, W d w 1988b,
W k et aL 1987%Wdtcr & Ikonen 1989, Walter & Kaplan 1991).
In addition to the discipliiary disjunaion between soil acuology and nema-
110 tology, two mistaken assumptions have impeded understanding of the strong
interaction between mites and nematodes. First, soil-pore spaces can exist in air-
Wed or water-filled states and mitcs have been assumed to be restricted to the
brmu and nunatodes to the latter. Althoy& some nematodes (e.g. dauer lar-
vae with double cuticles) arc able to inch their way - and even to jump -
through air-filled spaces, most nematodes do best when fiee water is available
and many require a film of water fbr movement (Nicholas 1984). Even the
thinnest film of water, howevef, may be enough and mites readily extend their
chelicerae into water to extract nematodes. Soil mires probably do best in air-
Wed soil porcs but they survive periodic flooding and many are able to fbrage
fbr nematodes, and even protomans, within a water layer Wdter & Kaplan
1990a). So, the fiunal dichotomy between air and water in soil pores is not as
strong as has been assumed.
The second mistaken assumption is that nematodes have extensive size-based
re&& where they are safi: fiom harvest by predatory mites. Nematodes are very
slender and soft-bodied, and they can enter very small soil-pore spaces unavail-
able to the mostly broader and less flexible mites. However, many
nematophagous mites are elongate, flexible and/or capable of extruding their che-
licerae considerable distances into small soil pores. Except in highly compacted
soils, it is likely that much of the pore space available to nematodes is also acces-
sible to probing mite cheliccrae and refUgia must be small indeed to protect the
worms. Most bod resources will not be restricted to those reftgia, so nematodes
must eventually come out -and run a gaundet of hungry mites. Nematodes are
better protected when they dehydrate during cryptobiosis but, even then, some
sarcoptihrm mites will eat them like so many dried snacks (Walter ct aL 1988).
Many if not most, Mesosagmata that live in soil, decomposing vegetation,
compost, dung and carrion will Ebad on nematodes. Ofien these mites show
their most rapid development, lowest mortality and highest f a d i t y when f;ed
nematodes (Walter et aL 1987a, Walter & Ikonen 1989). Species that p&r
nematodes or that M only on them arc especially common in the &milies
Ascidae, EviPhididae, Macrochelidae, Uropodidae and ZRrconidae. Some genera
of laelapid mites that tend to be associated with ant nests (e.g. Laclllspii,
CbnnoI;rclaps) also seem to be specialised nematophages (\rt7dter 1988a). More
general predators that d y feed on nematodes arc hund in the Laelapidae,
Parasiadae, Rhodacafidac and Ologamasidae.
Nematophagy in the Acuiformes is less common but some Endeostigmata
are primarily nematophagous (e.g. Alyw and Ahrhagk) ~ a l t c 1988 r b). A fkw
predatory Pmtigmata will rake nematodes, eg. some Bdellidae (Pugh & King
1985) and Cunaxidae Walter 8c Kaplan 1991). However, some of the most
important reports of significant levels of ncmatophagy involve the Tydeidae,
mites oficn thought to be primarily hgivorous (Santos & Whitfbrd 1981,
Santos et aL 1981). In Chihuahua desert soils, tydeid mites have a keystone
posiaon - their dimhation is associated with exponential increases in rhabdi-
cid nematodes which then overgraze soil bacteria and reduce decomposition
rates (Whidord 1996)- Nematophagy may be common among other soil arrhro-
pods, both predators and gnzus,but it has scarcely been studied. However,
many tardigrades, nematodes, firnd, protozoa and bacteria eat nematodes (Sayre
& Wdter 1991, Stirling 1991).
' Predators of arthropods
Eating mites and springtailsis the traditional role assigned to predatory Acari and
they carry it off wd. Early derivative acarifbrm mites graze or suck on microbes
but arthropod predation has arisen in a number of lineages,especially within the
Prostigmata. The snout mites in the Bdelloidea (Bdellidae, Cunaxidae) are entire-
ly predatory, as are the h-moving, pale Rhagidiidae and the slower,heavily scle-
r o t i d yellow to green mites in the Labidostommatidae. Seven of the eight
families in the Anystina (Anystidac, Caeculidac, Teneriffiidac, Adamysudac,
Paracydeidae, Pseudocheylidae and Pomcrantziidae) prey on arduopods, as do the
red velvet mite (Erythraeoidea;Trombidiioidca). Red velvet mites are ofien large
and brightly coloured and, like the closely related water mites (see Chapter 7),the
larva is usually a protelean parasite of an insect (although arachnids and verte-
brates arc also am& see Chapter 9). One subihily of cheyiedd mites, the
Cheyietinae, arc primarily predators of mites and other small arthropods, and
ofien seem to p&r astipatan prey. T h e Raphignathoidca consists of nine h-
ilia of predatory mites or presumed predatory mites. The well- studied taxa in
the Srigmaeidac and Eupalopsellidac are mostly pradatory on mites and small
insens but other fimilies arc more enigrnaac. Raphipthoidea are ofien major
componentsof dryland soils (eg. dry psslanb, deserts, eucalypt woodlands) but
little is known about their biology.
Mesostigmatans in the Laelapidae are among the more aggressive
predators found in soil. Some of these species have proven usdid for control of
pests in glasshouses and several species are now mass reared in commercially in
North America. The most imporrant group are the hypoaspidines (i.e. Hypompu
s e m &to), especially species in the genera (subgenera of some authors)
Geohhps (= Gaohe&ps) and Sh;atjohhps. Thrips arc vulnerable when they
enter the soil to pupate, h g u s gnats are attacked in the l a d and egg stages
and bulb mites are attacked at aU stages (Barker 1969, Harnlen & Mead 1979,
Lobbes & Schotten 1980, Giespie & Quiring 1990, Chambers et aL 1993,
Wright & Chambers 1994, Lesna ct d 1996, Ali et al 1997).
Most free-living Mesostigmata are predators, prcdator-scaven&ersor preda-
tor-hgivores (e.g. hctokze&pr, ~togamuseUi)and only a fkw lineages appear
to be primarily firnkivores (eg. Amecosciidae) (Walcu & Proaor 1998a). Some
Uropodina can be don f b g i (Woodring & Galbraith 1976, Hutu 1991) but
others are known to be predators of fly larvae and nematodes (O'Donnd & Axtcl
. 1965, OsDonncll& Nelson 1967). Many mesostigmacans that cap- arthropods
also f kion nematodes and other sofi-bodied invertebrates, and can be considered
general prcdatots (l!G!alter etd 1988, Walter & Oliver 1990). The predatory role
 of mites is important for understanding their influence in soil systems and espe-
cially in peripheral soil-liner systems such as dung or carrion. So, in d ~ next
e xc-
tion we will consider predatory behaviour in soil mites in greater detail.
PREDATION IN THE SOIL
T h e dominant acarine soil predators are in the Mesosrigmata, especially the sub-
orders Dermanyssina and Parasitina, and in numerous families in the
Prostigmata. Predatory prostigmatans are highly variable in their search behav-
112 iours but most dermanyssine mesostigmatans are restless animals, constantly on
the move, searching through litter o r soil pores for prey. This is reflected in the
Greek-derived ending of many
generic names, e.g. -seiur ('to move
to and fro, shake') and -helaps ('a
(Mooodtder superbus. hurricane'). Being constantly on the
Macmctrehdae) shanng prowl means that they can readily
locate patches of sedentary or less
mobile prcy (e.g. nematodes, aphids,
eggs, pupating thrips) and this is one
factor in their importance as com-
mercial biocontrol agents. Many
mesostigmatans are extremely
aggressive and will worry at the leg
joint of a much larger arthropod
until thcy draw blood (Walter &
Oliver 1990). It has even bcen sug-
gested that some of these animals
will hunt in packs (Usher & Davis
1983). Group feeding on a larger
arthropod is common ( B l a d rr al.
1990, Seeman &Walter 1997) but cooperative hunting is unlikely. Typically, the
initial attack is by a single mite and then either the t h r s h i n g of the prey attracts
the others or thcy stumble across the dying prcy and commence feeding
(Figure 6.2).
Ambush or sit-and-wait predators
CoLosriwrarcly stops moving except to moult, mate, feed o r lay an egg. Howcvcr,
N e o s r i d sp., another mite in the same subfamily and living in the same habitat
(Walter & Kaplan 1991), has a much more sedate style, oken pausing to rest and
covering only about 1 cm per minute (about 30 body lengths). Even less energetic
are cunaxids in rhe subfamily Cunaxinae (e.g. species of Arnmcirus, Cunauz,
Dartybsrina and Rubrosrim). These animals spend most of the time standing in
one spot with their large, spiny palps recurved over their bodics (Figure 6.3).
When a springtail or mite walks past them, they pounce. T h e palps are whipped 113
forward and the victim is impaled on the snout-like chelicerae.
Ambush predation is common in the Prostigmata. For example, Caecdidae
are related to the whirligig mite$ discussed above but have a very different strategy
for ambushing springtails and small insecrs like bark lice (Coineau 1973). We have
observed an Australian representative of this group, Neoraerrtlzu sp., from die
Wollemi region of New South Wales. This circular mite is covered with armoured
plates and knobby setae, and its first pair of legs arc very stout and long with thick
spines o n their interior faces. It will stand for days in one spot with these legs ele-
vated at a 45" angle to the ground, completely relying o n the movement of its prey
to bring about an encounter. Whcn a springtail wanders under the upraised legs,
they come cmhing down, scooping the victim into the hook-like chelicerae. A
number of water mites use similar behaviours (see Chapter 7).
A very unusual form of ambush behaviour ('fatal flatulence') has bcen
reported for nymphs of the tronibiculid Womersia stratzdnnanni (Hubcr 1978).
Springtails arc attracted to the posterior of these mites, which thcy tap with chcir
antennae. In response, the mite elevates its rear end a n d secretes a drop of fluid.
T h e springtails imbibe the drop and then begin a zigzag run which ends when
they fall paralysed. A trombiculid may poison a series of springtails before
encountering a paralysed victim and feeding.
Saltatory search
T h e amount of time and energy spent searching for prey can be viewed as a gra-
dient (O'Brien et al. 1990). At one end are the speed demons, like most

Cruise or pursuit predators

Mesostigmata characteristically search rapidly and pursue their prey. Similar
behaviours also occurs among the predatory Prostigmata. For example, whirligig
mites (Anystidae) are relatively large, often bright red and speedily spin across
ground, rocks and vegetation hunting for small insects and mites. Some cunaxid
mites are also constantly on the move. Cokosrim s i n l p h travels 20-23 un per
minute at 25OC W d t e r & Kaplan 1991). Since Cofeoscim has a snout-vent
length of 580 pm, this means that the mite runs almost 400 body lengths in a
minute. In human terms, this would be equivalent to sprinting 800 m every
minute - for hours on end. Prey are rapidly circled and subdued by a series of
rapid jabs with the chclicerae and finally grasped between the palps and chelicer-
ae, elevated above the substrate, and drained of their fluids. The crumpled cuticle
is [hen discarded.
 mesostigmatans, anystids and Cokosn'tw. At the other end are the patient and
deadly, like Neocac~~Iw. However, most predatory prostigmatans and some
mesostigmatans fhll in between the rwo extremes of constant movement or days
of patient anticipation, and instead show a series of starcingand stopping behav-
iours called salcatory search (O'Brien et al. 1990).
Many snout mites (Bdellidae and Cunaxidae) search an area by walking fiom
spot to spot, probing crevices with their antenna-like palps and elongate che-
liceme - looking much lik red bags on stilts with a hypodermic needle at one
end. Using rhis strategy, Cyta htimrrrrj is able to prey on well-armoured oribarid
l4 mim. When a beetle mite is encountered, C p squirts out a strand of sticky silk
to entangle its victim and then uses its short, scout cheiiceral hooks to pry open
a hole in the mite's armour (Alberti 1973). Other snout mites fiised on sofi-bod-
ied mites or springtails, speedily circling the victim while enta.q$ng its legs and
body with strauds of silk (Alberti & Ehmsberger 1977, Walter n d 1988).
ParasiriCormans in the primitive uropodine genus Po&qis and in the more
derived dermanyssine genus VZiggai are also rather deliknte in their searching,
and often pause in wait. Species in both genera have very elongate cbeliceral dig-
its used to snap-trap their prey. Like many of the soil mites on the ambush side
of the gradient, these mesostigmatans are specialised predators of springtails.
Constraints and variations
Cruise predators are more likely to rake sessile or dumped prey and, in general,
they will capture relatively smaller and younger prey compared to ambush pred-
ators (Gmne 1986). For aample, nematodes an relatively small and tend to
occur in high density patches. Nematodo are not eaten by cunaxid ambush
predators but d e n by cruise predators in the family, such as Cokosrirw and
Neoscirula (W'ter & Kaplan 1991). Red velvet mites (Erythraeoidea,
Trombidioidea) arc great wanderers and capable of rapid movement. Some
species capture springmils and insects (e.g. Young & Welbourn 1987); however,
many specialise on non-motile, dumped prey like the eggs d springtails or
insects (Lipovsky 1954, Sharma et al 1983, Wohlmann ct nL 1996). Similarly.
macrochelid mites rapidly search dung for dusters of fly eggs (Krmm 1983).
Ambush predators arc ofien capable of capturing relatively large prey
(Enders 1975).The energetics of ambush predation, however, demand that these
prey be highly mobile and predictably present (Hun/ & Pianka 1981).
Springtails are common and usually abundant soil animals but maiiy arc hst
moving and have the ability m jump away from dangu. The sudden pounce,
raptorial limbs and squimng of silk wed by ambushing mites represent a variety
of solutions to springtail escape behaviour.
However, &me cruising mites are efficient predators of springtails.
C o l c s n ' w is so fist that it simply runs over its prey, impaling small spapringails
b e h their escape bchaviow can be activated. In contrast, some c r u i s i i
mesostigmatans alter their behaviour when a relatively large prey icun like a
springtail is encountered. When Anrornosciiur janw comes upon a springail,
rapid movement stops andothe victim is stealthily approached. When dose, the
predator pounces, using the antennitorm fim pair of legs, the second pair of legs
and the gnathosoma to form a basket-like arrangement chat scoops the victim
into the snapping cheliccrae (Lindquist & Walter 1989).
I
I
Intraguild predation
1 Predators are animals that prey on other animak, and we tend to think of these
I
I interacting organisms as filling into two classes: predators and prey. However, the
vicdm may itself' be a predator and, if the two also compete f ix prey, then the eco-
I logical and evolutionary implications of this interaction (i@d predation)
arc quite di&rent from 'normal' predation (Polis et aL 1989). Inuaguild preda-
, tors not only gain the immediate benefits of the energy and nutrients in the vic-
dm's body; they may also eliminate a potential predator of their young and may
husband resources by reducing the level of exploitation competition k r other
prey. Humans, of course, ate tather deliberate intraguild predators, although in
Wescern societies the use of the eliminated carnivores as trophies is more highly
valued than their use as meat. Other animals tend to be less deliberate in their
hunting of potential competitors but within-guild prcy are o h a high propor-
tion of the harvest (Polis ct aL 1981, 1989). This is espcckdy m e of datively
large predatory-nr in soil fibod webs (eg. W k & O liver 1990).
, Degree of prey specialisation, relative size and efkiveness of &a are the
three main arbiters of incraguild predation in mites. Specialid ncmatophagcs do
not attack other predatory mites but they will feed on predatory nematodes,
thereby reducing competition for p 9 (Walter rt al 1988, Walter & Ikonen
1989). Uropodid mites are heady sderotised as adults and generally well pro-
d from predation. Those uropodids that f;eed on nematodes, worms and
1
maggots are often relatively large but do not attack even much smaller and d -
iy sderotised mites. Similarly. ambushing cacculid mias ignore many prcy of
seemingly suitable size until a springtad or psocid walks by (Coieau 1973).
Species of rhagidiid mites in the maritime Antarctic appear to be primarily pred-
ators of Patrrrjotoma and C~yptopyp springcds and have not been shown to be
inaaguild predators. However, Rhagidia remains can represent a si@cant pro-
1 portion of the prey detected in the guts of its competitor and i n d d predator,
G-eUus racovirzai (Lister et aL 1987).
Many soil-inhabitingmesostigmatans have feeding behaviours similar to that
of G. rrzcwi& (see Figure G. 1b), i.e. they are general predators that may attack
any arthropod or worm that they encounter, at least within a given size range, and
the success of the a d depends primarily on chance and the efficacy of any host
defence. For example, Pugh and King (1985) used field observations, supple-
mented by protein electrophoresis and laboratory tests, to study the &ding
,, habits of the ologamasid Hydmgamanrs salinzu in the British intertidal zone. In
the field, H. &nus was observed preying on nematodes, oligochaetes, springtds
, and l a d and adult flies, and scavenging on damaged barnacles. Elcctrophoredc
I analysis supported the field observations and also found indications of inaaguild
I predation on another ologamasid mite. Other intertidal mesostigmatans and
bdellid snout mites had similar feeding habits, including occasional f k b g on
' other predators (Rqh & King 1985).
Ittaaguild predation can be intense enough to scvucly rtduce the populations
; of some predators. For example, in research glasshouses in Orlando, Florida, the
, ascid mite Lariosciur sub~mrzncwcolonises the soil around the roots of potted
,
, plants infisted by rootknot nematodes where it can reach densities of over 400
mites per Liac of soil (Walter et d 1993). Lasio~w is larger than most of the other
halfdozen species of predatory mites in this system and readily fixds on them.
 However, when the larger and more ag~ressivelaelapid mite, Geokzehps sp., matans with approximately 50:50 sex ratios also readily attack and eat their
colonises pors, Lasioseizu populations decline precipitously (Walter & Lindquist immarures Walter, unpublished). Cannibalism among adult mesostigmatans,
1995). In laboratory arenas, Gcohehps sp. quickly captures and eats Larioscitu, and however, is rare - probably because of the protection offered by sclerotised
presumably the same behaviour contributes to the rapid decline in Lvioseiw pop- plates and equivalent size.
tdations in pots.
Although Geokzehpssp. is the top predator in this system and can capture and AVOIDING PREDATION - DEFENCES OF
eat any of the orher predatory mites, mycophagous rnites, springrails and nema- MITES AND MITE PREY
todes present, it is not immune to attack. Nymphal and larval Geokzekzpsare poor-
ly sclcrotised, relatively small and susceptible to predation by the cunaxid snout Soil-litter often contains both high densities and high diversities of predators,
116 mite Cokoscirur simpkx Walter & Kaplan 1991). Cokoscim also feeds on the and the predation pressure on arthropods and nematodes often must be 117
immature scages and relatively small males of dle second largest predator in the sys- intense. Not surprisingly, a variety of ways of avoiding being eaten have
tem, L. subterra-, but Larioseius in mrn is able to capture nymphs of Cokosrinu evolved. Escape via large size is a 'defence' common to both arthropods and
(Figure 6.4). Only active nymphs are captured. When preparing to moult, imma- nematodes that are stalked by predatory mites. The thrashing of large nema-
ture Cokoscim enter a crevice and spin a web around themselves which provides todes can dislodge and fling off attacking mires (Walter & Ikonen 1989); how-
good protection from other predators (including other Cokoscirur). Because of ever, most soil nematodes are relatively small, soft-bodied and the vermiform
their speed and size, adult Cokoscirruare immune to predation from all except the stages have no obvious defence. Adult female rootknot and cyst nematodes
largest predator, Geohkzps, but smaller curlaxids (e.g. Ncosciidz) and mesostig- become embedded in root tissue, where their bodies swell and become covered
matans (e.g. Ga~eIlories)in this system are constantly at risk of being eaten by with a gelatinous cap into which they lay their eggs. This stage is well pro-
larger predators and by each other Walter & Kaplan 1991, Walter et a l 1993). tected from predators, although some mites d o attack the egg masses (Inserm
& Davis 1983). Many rhabiditid nematodes produce a resistant dauer larva by
Cannibalism retaining, and sometimes modifying, the skin of the previous moult (Nicholas
1984). This stage is more resistant to environmental stress and the thicker
Some scorpions are their own worst enenlies (Polis et a l 1981) and this may be cuticle may provide protection against predation. Dauer larvae of enromoge-
true of some predatory mesostigmatans as well (Lindquist &Walter 1989). In one nous nematodes are able to avoid predatory rnites by climbing or jumping
species of phyrosciid mite, the rate of cannibalism has been found to vary gco- onto their backs. Although they rarely infect mites, they do use them as
graphically (Croft & McMurrry 1971). Generally, however, predatory prostig- phoretic carriers and are capable of leaving the mites to attack insect larvae
matans are more likely to eat their own kind, including their own oKipring, than
(Epsky ct n l 1988).
are predatory mesostigmatans.
The reasons for this dichotomy arc not clear but may relate to the prevalence
of inbreeding and parthenogenesis in the Mesostigmam. When members of a pop-
ulation are closely related, then a reluctance to eat one's relatives mnkes longtern1
evolutionary sense (Saito 1997). For exan~ple,adult females of Lvioseiru rienlranu
eat conspecific nymphs only when starved (Walter & Lindquist 1995). Since L.
detltanu is an all-female species that reproduces by rhelyrokous parthenogenesis
(see Chapter 5). in many popularions a conspecific is likely to be part of an idcn-
tical, or at least very similar, genetic lineage (e.g. sister, daughter, daughter of a sis-
ter). However, irs bisexual relative, hioseiru subterranezu, will eat conspecific
nymphs even when alternative prey is available (Walter & Lindquist 1995).
Bisexual species of Larioscius are probably parahaploid (Norton ct al. 1993)
and therefore the only functional chromosomes in males are maternal (see
Chapter 5). Migration in L. subtermnew is by inseminated adult females, which
produce broods with highly skewed sex ratios (80% female). Therefore, sib-
mating and a high level of inbreeding are probable characteristics of popula-
tions of this mite. Although they are cannibalistic on conspecific nymphs,
attack rates are relatively low (13%) cornpared to other bisexual ascid mites
with more even sex ratios and probable diplo-diploid reproductive modes
(Walter & Lindquist 1995). For example, in laboratory populations of
Antennoseirrsjanw (57% female), both adults and nymphs are aggressively can-
nibalistic (Lindquist & Walter 1989). Other probable diplo-diploid mesostig-
MITES: ECOLOGY,EVOLUTIONA N D BEHAVIOUR
Jumping
Rapidly leaving the vicinity of a larger, potentially dangerous animal k always a
p o d idea and many mites can produce quick spurts of speed, either h d or
backwad Jumping, the ultimate in rapid egress, is a common exapc machanism
of colIembolans (springads), especially those that live on the soil s& and in the
litter layer. HOW~YU, jumping also has evolved indepcndendy a number of times
in soil-inhabiting Acari. Species of N r
uul
taC
lrrtrr (Endeosci&mata)arc tiny (4300
p), spherical mites that bound away when approached by a prtdacoc. Species of
&pot& Cprostigmata) are very actin runners, both brwand and badwad, that are
able to leap when dosepresscd. Species of Tq-tlcs (Endeostipam) graze on
fungi in dry soils and also readily jump, as do some Scutacaridae @bermann
1995). Oribatids in the genera Ituhtxitia (Schubm 1967) and Zhvmhhc~ks(Krana
1978, Krisper 1990, 1991) are also able to jump. Microtrombidiid btvae have
highly modified tarsi on their hind legs and ate suspected of being able to jump,
both to escape and to latch onto passing insects, as do some hypopal astigmatafls.
Jumping parasitifbm mites, howcver, arc rare. To date only an undesaibcd trigy-
naspid genus (Mesostigmata) fiom rainfbre~t~ in Queensland is a known jumper.
This mite is sometimes tbund on passalid beetles and, as @ hopping hypopi,
jumping may h a i o n as both a d&tt and to fkilitate migration.
The jumping mechanisms used by these mites are only partially understood.
Species of &pot& have characuristically e d a q d hind h o r a which prcsum-
ably give them their W. Zkirtorchesta have a cuticular catapult mechanism at the
base of their bunh pair of legs that allows them to spring away (Ktispcr 1990,
1991) in a manner analogous to springtails. However, the box mite Ikhriria cf
h e m m ' c h i a uses hydraulic extension of all four legs to achieve emraordinarily
rapid takeoff (0.5 ms), a leap it is able to repeat two or three times in a row
(Wauthy ct a4 1997).
Chemical defence
Springtails are dassic jumpers but some species rely on a coating of easily shed
scales or chemical d&m to hi1 predaton. For example, the springless springtail
T i c l g i agramrl;zklproduces small droplets on ics body when ateadced Predators
encounter these drops when theyattempt to bite the sprinpils -and then quick-
ly badr away and can be seen vigorously cleaning their mouthparts. Subsequent
attacks arc o h succcssfll, sugpting that the chemical rcservcs arc quickly
depleted (Walter et aL 1988). Many astigmatans produce alarm pheromones that
may have a deterrent effect on predators (Matsumom ct aL 1979, Kuwahara
1990). Some metastriatc ticks produce gland secretions that protea them fiom
ants (Yoder ct al 1993) and some oribatid mites produce a s i subscanoe that
t
e Ologamasidac are predators of arthropods, and it seems likely that this species
deters ant attach (Matsuko 1994). Nymphs of Allodyws mites (Holothyrida:
Allothfidae) produce droplets from gland openin&swhen annoyed and thcse pre-
sumably represent d&nsive chemicals (Walter & Proctor 1998a).
Autotomy, armour, hairs, dirt and thanatosis
When a predator attacks an arthropod, it must first grab hold of its potential vic-
tim, and protruding from most arthropods are a variety of tempting handles -
the legs. Opilioacarans are able to shed legs (autotomy) to escape predators and
subadults are able to regow them at later moults (Wdter & Proctor 1998a).
Many long-legged prostigmatans (eg. Eupodidae) are able to lose legs and sur-
vive, although they appear unable to regenerate the missing limbs. Another
response to a looming predator is to curl up the legs against the body and play
dead (tkanabnsis). For example, adult AUocrC?yrusrely primarily on heavy armour
and thanamis for protection h m arthropod predators (Widter & Proctor
l998a). When attacked by ants or beetles, these relatively large mites (2-3 m m
in length) pull the legs against the body, fill over and remain modonless. After
a few snaps at the mite, the aggressor (possibly also influenced by mite seac-
tions) usually gives up and leaves.
Armour is by fir the most common d&nce mechanism in soil mites and it
is ofiem combined with thanatosis and curling of legs against the body or with-
drawing appendages into protected recesses. Adults of many major taxa are
encased in thick, sderotised plates and shields. Adult Mesostigmata usually have
one or m o shields covering most of the dorsum and several plates covering the
venter to varying extents. Adult males are often completely encased in armour
but females must be able to expand their opisthosomas to accommodate the
large eggs and generally have extensive areas of soft cuticle laterally and ven-
trally. However, both sexes of most uropodid mites arc completely encased in
armour. Many uropodids also have recessed areas in the shields into which
they can withdraw their legs (pedofossae - 'leg ditches', see Plate 29 in
Eisenbeis & Wichard 1987 for an excellent picture), and are often called tur-
tle mites (the same common nime has been applied to the Scutacaridae).
Adult holothyrans are also completely encased in armour, as are adult
Labidostommaddae and Penthalodidae in the Prostigmata. Other prostig-
matans (e.g. Adamystidae, Caeculidae, Stigmaeidae) have extensive develop-
ment of sclerotised shields.
Many oribatid mites have thick, waxy cuoteguments that may supple-
ment their armour. In Australian rainforest soils, some species of
Ologamasidae, Uropodidae and Oribatida have sticky ceroteguments that
accumulate thick, even encrustations of suongly bound soil particles. These
'dirt' mites are typically slow-moving and stop when touched. The soil may
simply increase the efKectiveness of the armour coating but it may also act as a
kind of camouflage by hiding the taste or feel of the mite fiom its predators.
This crypsis may also be used offensively. An undescribed species in the
GarnaseIIusfiIn'gcr complex fiom Queensland completely encases itself in a
fine coat of soil particles soon afrcr a moult -even the leg segments are cov-
ered with soil. The d o d tactile setae extend above the dirt armour on long
pedicels. Although the behaviour of this mite has yet to be studied, other
gains an advantage in ambush from its coat of soil. Some oribatids with sticky -
cerotcgumcnt accumulate a cap of detritus (see Plate 34 in Eienbcii &
Wichard 1987 for excellent pictures) and eupherederm oribatids carry 'scalps',
i.e. the top part of the exuviae fiom previous moults.
Early derivative oribatids have sderodsed, leathery or mineralid plates
protecting their bodies, and some (e.g. Comochhoniru, BcRCnnishryia) have
hypertrophied setae that can be erected to physically keep a predator away
(Walter et aL 1988). Several Lineages have independently developed an all-
 M I T E S :ECOLOGY,E V O L U T I O N
AND BEHAVIOUR
encaking body armour. However, the legs of these mites, although themselves
armoured, are weak points in their defence. A solution to these Achilles' heels
has been derived independently by several lineages of 'box' mitcs with ptychoid
('folded') arrangements between the anterior and posterior body regions (Figure
6.5). Box mites look like strange Swiss army knives with the legs protruding
blade-like from a cavity between an anterior carapace and a posterior, heavily
mineralised body (Norton & Behan-Pelletier 1991). When attacked. box mites
I
120
withdraw their legs into the cavity and seal it off by lowering the carapace, thus
presenting a smooth, featureless ball to a predator. Rolling into a ball, unfortu-
nately, is no protection from politicians. The late Australian $50 paper note
Figure 6.5
Armoured mites often have a variecy of behav~oursthat increase the effectiveness of their
defence. For example. box mites (left) can wrthdraw their legs into their bodies and close
-
the 'box' by jackknifing the anterior part of the body against the posrerior part a Astigmata) and atmoured mites for any mites with well-developed sclerotised
process called ptychoidy-The species of bsmochthonius (right), however. is not as flexible.
Instead. this mite has long. spiny seee that it can erecr to physically keep a predator away
from ia body.
carried a representation of a box mite, strategically placed below a microscope,
on the side featuring Clunies Ross (presumably to represent his interest in mites
as intermediate hosts of sheep cesrodes). Perhaps the only currency in history
to feature a mite, alas, neither scientist nor mite have survived the conversion
to plastic bills.
T h e so-called 'higher oribatids' include the majority of the 10 000
described species. They have a cap-like shell that covers the dorsal opisthoso-
ma and is separated from a ventral plate, which in turn is immovably amached
to the sclerotised prodorsal region. Some higher oribatids have accessory tecta
(roof-like processes) and shields that protect their legs. Some recta are mov- 1
able, hinged or wing-like (pteromorphae) and can be pulled down to cover
the legs. Oribatids, and other similarly well-defended mites, are oken called
1
i
beetle o r armoured mites ('panzer' mites in Russian) in the literature. For con-
1 sistency, we will use beetle mites as the common name for Oribatida (less the
~
I
or mineralised plating.
Specialised predatory mites such as Cyta latirostrir are able to penetrate the
I cuticle of otibatid mites but most other predators are thought to be limited to
feeding o n the more lightly sclerotised immature stages. Certainly, feeding on
adult oribatids is a tough proposition. Predatory mesostigmatans can be
observed attempting to feed on adult oribadds but usually give up A c t a few
minutes. However, some ologamasid mitcs are able to feed on oribatids, as are
adult Labidostommatidae. The smaller phthiracaroid, oppioid and haploze-
roid species that are relatively lightly sclerotised seem to be most at risk but
even large galumnoids are common victims. However, the most common
predators of well-sclerorised mites appear to be non-mites.
ACAROPHAGY-
MITES AS FOOD FOR LARGER ANIMALS
Pieces of mites can be seen in the gut contents of centipedes, scolopendrellid
symphylans and campodeid diplurans (Walter et al.1989; Walter, unpublished),
and many other common soil-liner predators, e.g. spiders, pseudoscorpions,
opilionids, ground beetles, rove beetles and ants, also are likely to include a high
proportion of mites in their diets (see Eisenbeis & Wichard 1987). Although
these feeding relationships have rarely been studied, the abundance of mites in
soil and litter suggest that they should be imporcant prey. Certainly, larger mites
are readily eaten by ants. For example, ticks of all stages, including engorged
females, are captured and killed by ants (Wilkinson 1970, Butler et aL 1979,
Dawes-Gromadzki & Bull 1997). While many predators take soft-bodied
species or stages, armoured mites are not immune.
Eating armoured mites
Although armour is the most common form of defence in soil mites, it is not
necessarily effective. Some groups of small insects appear to specialise on well
sclerotised mites. For example, armoured mites (especially Oribatida,
Uropodida) are reported ro be the prey of beetles in the families Pselaphidae
(Park 1947), Ptiliidae (Riha 1951, Cancela da Fonesca 1975), and
 MITES IN DETRITUS& SOILSYSTEMS

Scydmaenidac (Schusrcr 1966, Schmid 1988). Schmid (1988) found two basic conclusion thar cven we ear lots of mites. Oribarid mites are intermediate
rypes of arrack in adult scydmaenid bcerles. In the can-opener technique, bee- hosts of rapeworms because chey like to eat little animals and because thcy in
t l a capcure mites, turn them ovcr, hold chem wirh thcir legs and use their turn are eaten, inadvertently, by vertebrates. AnimaL that g a z e vcgcrauon do
mandibles to puncrute the anal d v e s and ream open the ventral shield. Other not stop to flick offthe l i d c running bits, bur ingest the lot. Grooming bchav-
beetles hold their prey with labial suckers and usciheir mandibles m plane and iour by vertebrates usually consists of licking or pecking off the dim and itchy
- .
saw throueh the dorsal cuticlc of the mire. Beetle larvae curl around rheir DICY, birs - and both are likely to conrain mitcs. So, accidcnd acarophagy must
to subdue &em bur use rechniques similar ro adults to puncture thcir cuticle. be common.
Each type of armoured mitc requites specific capturing and handling methods Some vertcbrata are exceptional in that they like to car mires. Thc oxoeck-
which are reflected in various modifications of the mouthparts and legs of the cr o r tick bird is one obvious delibcratc acaroph&e. Many small birds that for-
specialists. For example, only oribarid mites with smooth cuticles can be cap- age on the ground orobably also eat at least the lareer " mites and chis is surelv
~ ~~
I
cured by the planer-cutters: those wirh a thick, waxv cerotegument or rough true of ski& and other small lizards. However, it is the amphibians that a;
s u r f a c c ~ u t i ccannot
l~ be held by labial suckers. SO& beetle species are the mite gluttons of the vertebrate wodd. Frogs (Pcngillcy 1971, Simon &Toft
alisrs, however, and require relatively
prey (up to 4 hours).
- -
, lone handling times for some armoured
1991, Donnelly 1991, Stovart & Woolbright 1996). toads (Flowers &Graves
1995) and salamanders (Norton & MacNamara 1976, Maiorana 1978) all
T h e scydmaenid beetles in Australian rainforests that have been invcsri- feast to cxcess on mites. Commonly reported patterns among litter amphib-
gated to dare are more generalist in their prey preferences (Molleman & Waiter ians are that mitcs an: the most abundant prey in stomach contents or second
in press, Walter unpublished). Individual bccdes often capture a variety of
armoured adult oribatid, uropodid and mcjorrigmaric mites (Figure 6.6).
only to ants. Not sumriringlv, -
-. small frogs arc most likclv to feed on mira. For
aamplc, Pcngilley (1971) found that four of five spec& of frogs <35 mm long
Modified hairs on the tarsi of thc beetles allow rhcm to hold the mira as they in chc souchcrn highlands of New Sourh Wala had fed on mica ( 6 1 0 0 % of
flip them ovcr, prune off the legs and puncrurc the body through the p a t h o - the gut contents). 21feeding subadults, but only 54% of feeding aduln, of the
soma (ofcen forcing the chclicerae and hyporromc deep into the body).
Although many different familics of oribatid mites are attacked, those in the
Oppioidea arc the most common victims. The primary weakness of these
mites is the long legs which arc not able to be withdrawn into protected recess-
es of the body. So, cven the well-armourcd species arc easily captured and
eventually penetrated.
Two small (2-3 mm) species in the ant genus Mynnrcina rake a high pro-
portion of armoured mite prey including oribatids and mcsostigmarans
(Matsuko 1994). Mitcs are captured by workers and carried back to the nest,
where they adopt a curled posrurc as thcy manipulate the mite with their legs
and mandibles before finally tearing a hole through the anterior portion of
che ventral shield to one side or the other of the midline. The mite, resem-
bling an opened can of food, is then given ro an ant larva whore head fits
neatly into the opening. Larvac of a species of A&bmynncx in the ncorropics
have similar elongate heads and also appear ro feed on armoured mitcs
(Matsuko 1994).
Based on observations of live cxrractions from Australian rainforests, ants,
especially the smallcr species, are important rnorraliry agents of soil mites
(WHltcr, unpublished). Ants ofcen attack, maim or kill the larger mites but
ignore those thar are rclarively small. Unique-headed bugs (Enicocephalidae)
and larval dusky wings (Neuroptcra, Coniopterygidac) take weakly armoured
and soft-bdied mica. Other small, predatov insects that inhabit litter also
should be considered potential acarophages.

Vertebrate acaropbages
Although extending chc derrital food web beyond arthropods mighc ar first
rcem unlikely, anyone who has paid close attention to their morning bowl of
cereal or rheir dinner salad would have to come to the somewhat disturbing

Australian Corroboree Frog (Psrudophryne corroboree Moore) had eaten mites.
Similarly, a l l 109 females of the Costa Rican Strawberry Poison Frog
(Ddmbutespmilio) sampled by Donnelly (1991) conrained mites, which
accounted for 38% of their diet.
Oribatid mites are those most commonly reported from vertebrate gut
contents; however, other heavily sderotised mitcs superficially resemble orib-
atid mites and we suspect that some of the 'oribatid' mites reported in gut
contents may represent a more diverse diet. In any case, although armour is
obviously little protection against being swallowed whole by a much larger
animal, it does resist digestion and allows these mites to be readily identified.
Whv small anurans are so fond of armoured mites. however. is lcss easv to
understand. Because of their small size, mites have a very high surface-to-vol-
ume ratio, i.e. they have more shell and less meat than do larger arthropods.
Each feeding event takes time and energy, but brings relatively lcss reward for
each armoured mite than for similar sized soft-bodied prey.
Well-sderotised oribatid, uropodid and mesostigmatic mites arc often
extremely abundant on the forest floor and will be encountered commonly by
small vertebrates foraging on the ground, low vegetation or tree trunks. For
example, Maiorana (1978) fbund that oribatid mites accounted for about
27% of the potential prey of California Slender Salamanders (Butruchoccpz
attenrutnu) living under logs. Since oribatid mites accounted for 35% of the
" .
stomach contents of these salamanders.- a slieht oreference for oribatid mitcs
could be infkrred. However, laboratory tests showed that the salamanders
dropped oribatid mites from their diet more quickly than soft-bodied
sminthurid springtails of similar body size (Maiorana 1978). Presumably,
salamanders balance their p references with what is available and with dietarv
requirements. For example, oribatid mites often have high levels of minerals
/ soil organic h o r b n s the structural diversity of microhabitats has been shown to
such as calcium and phosphorus (Seastedt 1984) that could be important to
s m d vertebrates.
THE ENIGMA O F SOIL BIODIVERSITY
In tbe c o m p k f i d world of the soil environment, thew is
&mrlygrrum niche puseJ5r the mtlrllcr organism
(Giller 1996)
Soil interstices and their sheltering accumulations of decaying organic matter
probably represent the ancestral habitats of mites and these are still the habirats
where the greatest divusiv and abundance of mites can be found. Generally,
spccies diversity increases with stage of decomposition (Whihrd 1996) and stage
of plant succasion (Scheu & Sch& 1996). Probably both of these patterns result
ftom an int~ccionbenvcen changing miuohabitacs and colonisadon lags. Also,
llmv tbidcnar is positively correlatedwith soil mite diversity thick organic layers
have more individuals and species than t h i i e r layers (Gi1969, Sranton 1979,
Curry 1994).The ancient age of the mite-soil associadon may help m explain why
so many soil-litter mia species &, but how these species coexist in a uniform
layer of litter is unclear. Traditional ecological theory assumes that communities are
usually near equilibrium and that most available resourca are used to support
respiration and population growrh. Since litter does not accumulate to grrat
I
,
I
depths on the surfice of the soil,the dccomposcr system must be fbod limited and
its members must regularly compete h r resources (Hairston et aL 1960).
{ However, micmbi~re&tritivorcs, the most species rich hnaional group
I of the soil-mite &ma, have a high level of aophic overlap among species (see
j page 104). They also tend to have long developmental times and stable popu-
lation structures (Norton 1985). Thcrefbre, there is l i d e indication of tunvo-
I. ral or trophic partitioning by so3 mites on two of the three major niche axes
' assumed to be important in the coexistence of funaionally s i m i species in
equilibrium communides (Anderson 1975%Gillu 1996). Since oribatid mite
populations appear to be stable, there is no need to hypothesisc non-equilibri-
urn conditions whcrc diversity is maintained by predation (Paine 1966) or an
intermediate level of disturbance (ConneU 1978). In fict, predator populations
also appear to be composed of many general predators and to be r&&ely sta-
ble. Predators may undergo seasonal bouts of recruitment or respond to fluctu-
ations in prey populations but, at any one time, a diverse communiry of general
predators is usually present (eg. Luxton 19GG).
Oribatid species normally have aggregated distributions and population
growth tends to be within aggcptions, rather than from increasing numbers of
aggregaaons (Usher 1975, 1976). This may reflect rather narrow niche-widths
and, iforibatid mites tend to be microhabitat specific, then uophic overlap could
be ef&ctidy reduced. Surhce litter may form a &ly homogeneous habitat.
home to distinct assemblages of oribadd mires (Crossley & Bohnsack 1960,
Hammer 1972), but on doser inspection even seemingly u&rm anas of the
forest floor contain a variety of mite habitats, e.g. dumps of cryptogams, rocks.
, tree trunks, stumps and other woody debris, inhabited by mtriaed subsets of the
, species pool (Hammer 1972. Lindquist 1975, Wallwork 1983). Even within the
:
have a strong positive efiim on the diversity of oribatid mites (Anderson 1978%
I
Abbott etaL 1980). Some level of mphic partitioning related to rniuohabitat dif-
fkrences also has been shown (cg. Anderson 1978b, Siepel 1990).
Soil is a solid matrix infiltrated with a maze of spaces and pores. These pas-
sageways and blind alleys provide a large amount of habitat space for small
organisms. This is usually interpreted, in terms of hcd geometry, as implying
that a diversity of habitats also exists (Lawton 1984, Giller 1996). However, h c -
d scaling results in similarityof patterns at Merent scales so that, although the
absolute amount of habitat space may change, habitat diversity may be similar
at difhent d e s (Fenchel 1993). In either case, the soil is &redimensional
and scaling in a strictly two-dimensional pattern (cg. Morse er al 1985) seems
inadequate. Surprisiiy, there arr fkw studies that addrcss the e k of over-
storey species on soil mite diversity and none that show suong c f f w of indi-
vidual plant species (Curry & Ganley 1977) or litter type (\Walter 1985).
Forest floor habitats
In temperate forests with a low fire frequency, leaf litter and ochcr orga&c
debris accumulare on the forest flooc Surface litter layers tend to be rather
sparsely inhabited, probably because of their large pore spaces and tendency to
dry out, but deeper organic layers have high diversities and abundance5 of
mites. Many oribatids burrow inside leaves, small stems, cones and other suuc-
 turd components of litter - actively increasing the su&ce area for microbial
decomposition and inoculating detritus with microbial spores. In coniferous
forests, especially under acidic conditions, a mor soil profile usually develops.
In these soils, thick layers of needles accumulate and slowly degrade forming a
thick covering of organic matter on the forest f ( o o ~The resulting orpnic hori-
-
zons are dominated by small pore spaces - ideal for mites that decrease in
size range, median size and complexity with depth. Freshly Wen litter overlays
a thick fermentation layer of pardally decayed humus that o h contains
extraordinary densities of mites. Under the fermentation layer is a thinner layer
I26 of fine humus parrides and arthropod b, especially those of oribatid mites.
The organic horizons overlay mineral soil layers variously aflFeaed by leaching
and deposition fiom above. In mor profiles, the average body size of mites ofien
decreases sharply at the organiomineral soil h e & , as species composition
changes and the reduced average pore size restricts the access of the larger mite
species (see Swifi et aL 1979, Wallwork 1976, Eisenbeis & Wichard 1987). The
deeper m i n d soils in conifierousforests are rarely sampled but mites undoubt-
edly occur at least as deep as the roots penetrate.
In neutral to alkaline soils, ofcen associated with deciduous forests, rela-
tively rapid decomposition and high levels of activity by soil macroFauna (espe-
cially earthworms and millipedes) tend to result in a mull profile with a
relatively well-mixed layer of soil and organic material under the litter. This rel-
atively sparse litter layw has a laminar arrangement of fieshly M e n and par-
tially decomposed leaves that provide fewer hiding places fbr mites than a mor.
However, burrows made by the macroiuna or I& by the rotting of roots pro-
vide major highways for mite traffic through a mull profile and mites follow
smaller passages along the rhizosphere into deeper soils. Typidy, mite species
assemblages are drastically different in mor and mull profiles, even when the
forests are adjacent. The major input of organic matter is usually with litterfill
in the autumn, and much of the initial decomposition of litrcr may occur under
a blanket of snow.
Tropical rainforests can be similar to temperate deciduous forests in that
litter auumulation may be highly seasonal, although associated with dry,
rather than cold, periods. In seasonally dry tropical forests, litter arthropod
populauons may flush in the early wet season as accumulated leaf fill is
degraded k i n g s & Windsor 1982). Other aspects of soil structure and
dynamics, however, are strikingly different. When s&cient moisture is avail-
able decomposition is very rapid, little litter accumulates and nutrients are
quickly cyded. Wlth l i d e litter available on the surfice, mite densities tend
to be low and mineral soil is so densely packed with roots that sampling to
any depth is difficult. Litter pockets can be found in the buttresses of trees
and on the uphill side of trees and logs but more humus can be found hang-
-
ing in the canopy in treeholes deep crotches and among the roots and rhi-
wids of large epiphytes. Similar accumulauons of suspended soil can be
found in the cool coniferous rainforests in the Pacific Northwest of North
America. Stanton (1979) found a higher rate of turnover among uopiml
compared to temperate litter mites, and suggested that tropical mites tended
to be more habitat restricted and had higher proportions of rare species.
Based on the few studies that exist, soil mite diversities can be very high in
tropical and subtropical systems (Lasebikan 1974, Chiba et aL 1975, Stanton
1979, Wdter er aL 1998).
Ephemeral vs. stable soil-litter habitats
Humus layus, rotting wood (Fager 1968) and nests (L,indquist 1975) are rela-
tively stable, pusisant habitats fbr soil mites. Other components of the soil-lit-
ter system, howew, can be fPI less predictable in time and space. Patchy,
ephemeral habitats, such as dung, decaying fiuit, rotting f w and carrion, have
charaauisac mite fiunas that depend on phoretic associationswith insects. For
example, phomic species of Mru~ocheI#,Wolocekzeno, Holoskupe~Neopo-
docinurn and G&~tholl.upis(all Mamchelidac) and Parasitinae (Parasitidae) are
the most common and abundant mites in herbivore dung (HaMier & Matthews
1971, Kranu 1983); in con-, soil-inhabiw Parasitidac typically belong to
the s u b M y Pergamisinae and soil-inhabiting Macrochelidae to genera
(GchoLqoiz, Ahzovpis) or species groups of MmchcIcr chat ate non-phoretic
(Manning & Halliday 1994). However, genera and species-pups characteristic
of herbivore dung tend to have dose relatives in other ephemeral habitats. For
example, phomic species of Mmchclis are common in carrion 1983),
rotting caai (Pobk & Markow 1995), under the bark of beetle-killed pines
(Kinn & Witcosky 1977) and in romng fungi (Walter, unpublished). Fungal
sporocarps, b m fleshy to woody, are home to an extraordinarily diversity of
mitts melou & V'1968, Matthewmann & Pielou 1971, Okabe & Amano
1992, 1993, O'Connell& Bolger 1997, Walter & Proctor 1998b).
Body size patterns
We must d e itfir g r a n d chat a &wpart of the mite fiuna
of tbe WO& will m i n umzmp&d unnamed and unclirrnfid
[not to mention unwept; unbonound, and unsung/& & c d s ta come.
(Mayr 1969, interpolated by May 1978)
G. Evelyn Hutchinson and his students were responsible for generating many
hypotheses to explain general patterns in community ecology from trophic
levels to body size differences among congeners (Hutchinson 1965). Two of
Hutchinson's ideas about the importance of body size, both published in The
American Naturalist in 1959, arc especially relevant to soil biodiversity. First,
Hutchinson & MacArrhur (1959) suggested that an animal's perception of the
habitats in an area was basically two-dimensional and size dependent. The
number of available habitats, and species occupying those habitats, should
climb rapidly fiom the smallest size class to the modal dass, and then decline
less rapidly with increasing size. At the large end of the size spectrum, the
number of species (S) should decrease with the characteristic length (L) of the
animal (s-L-~).This model was the basis of May's (1978) influential specula-
tion that insects were highly diverse because they were small and that the
diversicy-size s h o d d l below the modd size class was due to taxonomic igno-
rance of very small species such as mites.
May's speculation, which ended a symposium on insect diversity, has been
honoured with a pyramid of publications on the relationships between size
and diversity. Although those who try to climb that monument may be in for
 a very rapid descent, 20 years later the quest for the perfect slope continues
(I-oder et al. 1997). However, Hutchinson's second paper (Hutchinson 1959),
his presidential address to the American Sociecv of Naturalists, has been treat-
ed with anything but reverence (e.g. Simberloff & Boecklin 1981). Although
much challenged, - Hutchinson's basic observation is all too commonlv true. H e
noted that when two closely related species, typically congeners, are found liv-
ing together in the same habitat, one species is usually twice the size of the
other. If the linear dimensions of the animals are considered, either body
length or the length of an appendage used in feeding, the ratio of the larger to
the smaller species is typically about 1.3 (range = 1.1-1.4, mean = 1.28),
which in animals of similar body shape implies a two-fold difference in body
mass (Hutchinson 1959, 1965).
Hutchinsonian size differences are a common, but difficult to explain,
phenomenon. Although Hutchinson interpreted the size differences under the
prevailing dogma of character displacement through competition, this seems
inadequate. For example, Hutchinsonian size differences are generally present
between instars in arthropods (i.e. Dyar's Constant) and anlong series of musi-
cal instruments and other objects of human manufacture (Horn & May 1977,
Maiorana 1978). Eadie et al. (1787) have suggested that I-lurchinson's rule is
7 an artefact of arbitrary sampling
from animals or objects with a log
normal size distribution and a low
variance, and that no biological
causc needs to be invoked.
Body size displacement con-
forming to Hutchinson's rule is
corn!non among some assemblages
of soil mites (Figure 6.7). For
example, Walter and Norton
(1985) analysed the size distribu-
tion of the oribatid mites in radiata
pine litter at three sites in
California. When 46 species at one
of the sites were arranged in a size
sequence, the ratio of the larger to
the smaller mite ranged from
1.00-1.14, with 83% of the values
falling below 1.05. Therefore, as an
assemblage, these 46 species filled
the available size space with no sign
of regular two-fold displacement in
Figure 11.7 mass. However, 13 congeneric
%dLFaibudons of adult females of four species of species pairs occurred at the three
SdKkKiborts I i n g sptpatrically in radiata pine liaer
In 'California. Uniform size differences eauhralem m a sites and their body size ratios
doubling of mass (linear increase of ab& 30%) are ranged from 1.20-1.39 and
Arirdc of sympacric congeneric spmes averaged 1.28, exactly as observed
pairs in oribadd mrtes.
(Modified from W t e r & Norton 1985.)
by Hutchinson (1957). Whatever
the cause, when congeneric pairs of
oribatid mite species are sympatric, the adult female of one tends to be twice
the mass of the other and the doubling of mass berween instars during
ontogeny suggests that these size differences are maintained among equivalent
life stages.
SENSITIVITY A N D DIVERSITY - SOIL MITES
AS ENVIRONMENTAL INDICATORS
T h e small size of most soil animals and the dificulry of observing rhizosphere
interactions in situ have impeded the understanding of their importance in soil
systems. Most studies have been restricted to com&uing the ibundances and
diversities of soil mites to rates of decomposition and nutrient cycling, the
effects of disturbance and the concept of sustainable agriculture (see Anderson
& MacFaydcn 1976, Wallwork 1976, Swift et al. 1979, Petersen & Luxton
1982, Seastedt 1984, Moore ct al. 1988, Behan-Pelletier et al. 1985, Hendricks
et aL 1990, and Wolters 1991). In most analyses, counts at the subordinal level
are the limits to resolution but a few studies have attempted to tease out finer
taxonomic patterns.
Also, most studies have concentrated on the easily sampled upper 5-10 cni
of soil, ignoring both vertical migrations by the fauna in the upper soils and the
deener soil fama. In drv soils. or those exoosed to environmental stress, corn-
muting to a deeper soil level may be a means of avoiding desiccation. Soil com-
paction and vegetation removal by catde can cause a decrease in small oribatids
that usually avoid drought by moving deeper into the soil profile. Larger
drought-intolerant oribatid species that are less able to move into the soil pro-
file can be eliminated by even a single cutting in grassland (Siepel 1996). Soil
mite communities also may be negatively affected by burning (Yeates & Lcc
1997) or clear-felling (Abbott er aI. 1980).
Mites have seldom been exploited as bioindicators in soil (or in water, sue
Chapter 7); however, oribatid mites may prove especially useful indicators
(Lebrun & van Straalen 1995, Stamou & Argyropoulou 1995). The oribatid
mites Rhysotritia duplicata and Nothrus silvestnj have been shown to quickly
accumulare and retain heavy metals (Lugwig et aL 1991). Since these mites have
relatively long life cycles, they may prove useful indicators of heavy metal pollu-
tion events. The relative proportion of thelytokous oribatids has been shown to
increase in response to heavy metal and to pesticide pollution (Siepel 1995) and,
given that the taxonomic correlates of thelycoky in oribarid mites are well estab-
lished (Norton et aL 1993). this life-history characteristic may prove useful. In
contrast, pentachlorophenol (PCP) pollution had little effect on large oribatids
in microcosni experiments and small oribatids and astigmataris increased in
abundance at the highest concentrations (500 mg kg-' PCP). Only
Mesostigmata appcnred to be negatively affected ( S h i n e n & Iiaimi 1996).
Other studies have shown species-specific responses by mesostigmatans to soil
compaction (Heisler 1975) and pesticide contamination (Koehler 1992).
Many oribatid species have distinct pH preferences (van Straalen & Vcrhoef
1972, van Straalen 1997) and, therefore, may make good indicators of acidifi-
cation caused by acid rain and other air pollutants. For example, Steiner (1995)
found that oribarid mite communities in moss cushions on walls decreased in
 species for morc s p d c study- However, it is important to remember that hnc-
species richness and became more uniform in composition along an tional p u p s , guilds and the like are artificial constructs - user-defined units
urban-rural air pollution gradient in Switzerland Bdellid predators of oribatid
mites also decreased. Air pollution explained the relative abundances of
of study - not pre-exkhg components of nature. As such, they should be
dearly d&ed by the user as to which caxa arc included and which excluded..
Zygotr'B& exih extremely well, suggesting that this widespread specieswould Pradaaon is the best studied of the soil mite functional roles and it is per-
be a good indicator. Since lichens are strongly affected by air pollution, reduc-
haps one of the most important. Applied use of soil predators against pests is a
tion in lichen cover may have been an important factor in the decline of these
mites. However, the nitrogen and sulfur components of acid rain can act as recent, but rapidly developing, branch of biological control. Because of the
nutrients in soil systems and mite populations tend to increase with simulated diversity of predatory soil mites and the ease with which they can be reared and
acid rain pollution in some experiments (Hencghan & Bolger 199&, b). Soil observed, they make excellent subjects for the study of predatory behaviour,
130 hod-web dynamics and the adaptations of prey to avoid b e i i eaten. Mites are
mite populations also can respond positively to above-ground perturbations
such as herbivory - directly through increased input of droppings and indi- eaten, not just by other mites, but by many soil invertebrates and by numerous
small vertebrates. Because mites tic together so many components of the soil
rectly through effects on root chemistry (Seastedt ct aL 1988).
food web, they may make excellent indicators of human disturbance.
Well-sdcrotised mites, such as Oribatida and Mesostigmata, are often fos-
silised (Erickson 1996) and this tendency has lead to the recent development of
pal8c0acaro1ogysi.e. the study of fossil and subbssil mites. Although we rarely
notice those that do not bite us, human habitations have always had their own
acarofiuna and many of these unnoticed companions have tales to tell about
our early habits. For example, although fbssiliied human scats can be identified
fmm the eggs of our characteristic parasites, fossiliscd Mesostigmata are more
d fbr the identification of domestic animal dung (Schelvis 1992). Fossil
and subfossil oribaad mites are especially usefid indicators of vegetation, mois-
ture regimes and salinity around ancient human habitations, at least where the
modern fiuna is well known (Schelvis 1990).

SUMMARY
The enigma of soil mite biodiversity is that even-a handfid of fbrest soil and lit-
ter may contain dozens of species that coexist with seemingly )liew adaptations
to avoid trophic or habitat overlap. Outside of the soil-litter layers in any for-
est, numerous microhabitats with specific assemblages of species can be recog-
nised but, within these dumps of moss, shelves of ftngi, piles of dung and the
like, the riddle is endlessly repeated. Typically, each microhabitat contains suites
of species with extensive withii-suite trophic overlap -or at least so it seems.
The true enigma is that although decomposition is the equal of photosynthesis
in ecosystem importance and half or morc of all rerrestrial biodiversity may be
tied to the soil-litter system, the study of soil biology has been neglected.
In spite of this neglect, certain patterns are dear. Most importantly, because
the diversity and abundance of soil animals is dominated by the h i , any true
understanding of the soil system must include understanding the mite fiuna.
Even in deep soils or in extreme climates, mites are major constituents that
interact with other components of these systems in a variety of ways. Mites link
together many components of soil food webs and the study of their behaviour
can shed light on M - w e b dynamics and stability.
Seven general hctional roles of mites in soil art outlined in this chaptec
comminuting miaobivoteaeaidvores, piercing-sucking microbivotcs, filter-
feeding microbivorts, direct plant parasites, indirect plant parasites,
nematophages and predators of arthropods. Thii is a general functional
dassification and any of these p u p s could be subdivided to identifjt dustus of
I
f one goes back far enough, all terrestrial arthropods are the descendants of
marine ancestors. For some groups, such as isopods, emergence onto dry land
was evolutionarily recent and these animals ofren appear imperfectly adapted
to solid ground. For most other groups, however, the split between marine
and terrestrial lifesryles happened hundreds of millions of years ago and all traces
of aquatic adaptations have disappeared. So for the many taxa that have since re-
invaded water, ancestral structures that would have been useful (e.g &) had long
since vanished and mechanisms for respiration, feeding, and even mating, under
water had to evolve de novo.

TAXONOMIC DISTRIBUTION OF SECONDARILY

AQUATIC ARTHROPODS
O f the terrestrialised arthropods, insects are the most obvious practitioners of
h i s new aquatic habit, although only in certain families in the Hemiptera (e.g.
Corixidae, Bclostomatidae) do a l l life stages living subaquatically. In other m a ,
pupae or adults remain terrestrial. Most aquatic insects live in fresh water; only
a very few groups have rerurned to the ocean and most of these live on the sur-
face film (e.g. water-striding bugs) or intertidally (beetles, flies). Just one species
of caddisfly, Phihnisuspkbcius, two species of chironomid midges, Clunio mar-
inus and Potomyia natans, and one genus of beetles, Haemonia (Chcysomelidae).
spend their larval scages completely immersed in the salty brine (Cheng 1976;
Wtnterbourn & Anderson 1980).
Life under water has not atcraaed many myriapods. Centipedes, symphy-
lans and pauropods are invariably terrestrial. A number of species live in the
rocks and wrack along beaches but do not willingly enter water (Roth
& Brown 1976). Only a few species of Australian millipedes have invaded
fresh water.
Arachnids for the most part seem obstinately landlocked. Even though the
ancestors of scorpions wcre aquatic (Chapter I), extant members of this group
have gone to the opposite exueme and are now classic desert dwellers. There are
no aquatic amblypygids, uropygids, schizomids or opilionids. One genus of
palpigrades has been reported to be able to swim in sea water (see Chapter 2) but
this is unlikely to be its normal habitat. However, many of these arachnid groups
indude species that make their livings beachcombing at low tide and hiding in
wrack or rock crevices when the tide comes in (Roth & Brown 1976). Some spi-
ders and pseudoscorpions are exeptional in that they do not hide from the salty
water but rather remain in their silken nests on the undersides of stones or in
cracks at high tide (Harvey 1998). AIthough many fishing spiders (Piauridae)
and wolf spiders (Lycosidae) can run across the surface of Fresh water and may
submerge briefly to chase prey or avoid enemies, only one of the more than 30
000 named species of spiders spends an appreciable portion of its life under
water. T h e European water spider Argyronrta aquatica (Agelenidae) swims about
and catches prey in Freshwater ponds but it requires air for respiration. The spi-
der builds an undenvacer bell of silk and ferries bubbles to it, thereby crating a
handy store to replenish the layer of air that encases its abdomen. Arlqyroncta
must also construct diving bells to eat its prey, to moult, to transfer sperm (both
from the male's genital opening to his palps and from his palps to the female's
genital opening) and to lay eggs (Braun 1931, Crome 1951).
 So much for non-aerine ancbnids; what ahour rhc mires? As in mmy other
arachnid groups, thcrc arc rcrrcsrrinl mires rlv~rlivc in rhc intertidal zone (see
I.uxron 1990 for a review of rhcir biology). According to Rorh and Brown ( 1 976).
at leur 15 Families of Mesordgmata, Oribarida, Asrigmaw and I'rosrigma~~ hll
into chis ecological category. lnrcnidal mites often occur in grmt numbers: Ernsr
(1996) observcd densides of nculy 200 000 mireslm2 on rhe mckv shore of rhc
- ~ ~ ~~~
presumably open their spiracles ro exchange g a t s only when their hosts are on
land or (for chose clustcrcd around the head) when their hosts surface co breathe.
Aquatic spccics of Mesostigmata have been reported from the Ascidae
(Cheirostiur and Pkqwiiur spp.), Dithinozcrcondac (Gminella pnaphora) and
Uropodidae (Phauhdinychw mini) (Table 7.1). One species in the Phytosciidae,
Macroreiur birnrrarur, has been collected from pitcher plans (Chant rtnL 1959)
but it is unclear whcrher it is subaquatic. Ir may be like PIatyrriur iralicur, which
inhabis wet vegerxion where it L likcly to be occasionally submerged and has
~

l u n g and nasal pasrages of their hosk and so arc not aquatic rnuu strict~,and it is
~~~- cvolved a plastron to dcal with gas exchange under rhese circumstances (Hinron
1971). Many predatory mesostigmatans inhabit the marine lirtoral zone bur 1
also possible chat the crab mires live in air spaces. Thcrc arc many spccies of mica, thcy typically retreat to air-filled crevices ro avoid drowning (Luxron 1990) or
especially prostigmatans like Homouligidae and many members of the Cohort can survive for only a few days under warer (Pugh 1996a).
Parasitengona, char cnwl across rhe surhces of frerhwnrer ponds and bogs but do
do not submerge rhemselvcs. Among the oribnrids, many species in rhe Camisiidae
and Mycobaridac inhabit soggy arms in moss and lirrer next to water bodies hut
rhey are rarcly completely immersed (R Norton, pers. comm.).
Are them any truly sub-aquatic acarines? By now you should nor be sur-
prised to find char, unlike their lcss versatile arachnid relatives, many thou-
sands of spccics of mires are crur permancnr residenrs of aquatic hahirars. In
f x r , almost every freshwater and marinc liabitar imaginable is home to one or
more of rhere adaptable arachnids. Mitcs live in the wzrcr that accumula~erin
rreeholes, pitcher plans, bamboo inremodes, bromeliads and leaf axils -
scrucrures collectively termed 'phyotelrnnta' (c.g. Fashing 1994, 1998;
OConnor 1994). They inhabit standing and running frcsb water oF all rypcs,
from near-freezing glacial melrwatcr to steaming hot springs, from rhe mossy
margins of bogs co thc dcprhs of L-kc Baikal. from tcrnparary ponds ro rhe
srygcan pcrmancncy of dccp groundwater. Marine mites live in ridepoolr,
interstitinlly in sandy beaches and ar abyssal deprhs grcarer rhnn 4 krn. Within
rhesc habitats mites act as prcdarors, parasircs, bcrbivores, fungivorcs. i.c.
everyrhing thcy do on dry land. Now let us explorc rhc cvolurion and ecology
of rhc aquaric mires in mom derail.

REPEATED INVASIONS O F WATER

Them have been ac least ten independenr invasions of warer by difrercnr lincag-
es of mires. In somc wses, cnrry appears quire recenr in that chcrc are only onc
or a few rpecies in a family living undcrwarer while chc rest are land-dwcllers
(e.g. hccidac: Mesostigmnca). In others, whole supcrfamilics comprising hun-
dreds or thowands of spccics are obligatorily aquatic.

Parasitiformes
Very few parasitiformans have venrurcd below the watcr's surface. There arc no
aquatic opilioacarids or holothyrans. There arc w o species of sea-going
Amblyornma tick (Ixodidae): A. nitidurn parasitises sea snakes of the genus
Laricau&, and A. &mini parasitises the marine iguana AmblyrJyzchns rristarus
(Hoogsrral 1973; J. Keirans, pets. comm.). Little is known of their biology
except char the ricks initially infest the reptiles on land; iguanas spend a great
deal of time hauled our on rocks and, whilc most sea snakes spcnd their entire
lives submerged, Lzricau'a spend the day outside of the warcr and only hunts
subaquarically at night (Audy ct r d 1960). Ticks of these n~nrinereptiles
MITES: ECOLOGY.E V O L U T I O N AND BEHAVIOUR
Oribatida
Oribatids have been more adventurous in their exploration of wacer (Behan-
Pelletkr 1996; R Norton, pcrs. comm.) (Table 7.1). Numerous spacics fcad on
sodden algae in the marine littoral zone (Lwton 1990).All 20 or so species in the
Hydmzecidae are subaquatic in ponds, lakes (Kranu and Baker 1982) and
streams (pers. obs. Proctor), and numerous fmhwater inhabitants are: scattered
through the FamiliesTrhypochthoniidae and Atneronothridae. A number of other
taxa are fbund in aquatic systems but appear equally at home in damp moss and
other sodden vegetable matter. These 'amphibians' include Limnozetidae, some
Trhypochthoniidae and one genus of Malaconothridae. Zetornimidae are also
associated with shallow warm but anecdotal literature suggests they may live on
the water's s d c e rather than beneath it. There are a number of other members
of the Ameronothridae and related f2unilies (Selenoribatidae, Fomyniidac) that
are intertidal or estuarine. These are active only when heir environment is wet
but they do not spend their entire lives submerged (R Normn. pers. comm.).
The sub-hearctic species TtimalvOmnbr~~~gcUi~rmir (Mahconothridae) and
EdwanizcteS elongatur (Ceratddae) can survive more than 30 days submerged
but they cannot complete their I& cycle under water (Pugh 1996a). Because their
cxoskcleton is resistant to decomposition, t e r d oribatids arc ofcen found in
aquatic samples after having tumbled into the water and drowned (Schau &
Geredrc 1996; Proaor, pen. obs.).
Astigmata
Although their thin integument would seem well suited for aquatic gas
exchange, there are few families of astigmatans with aquatic species (Table 7.1).
The algivorous Hyadesiidae inhabit tidal pools and mussel beds (Roth & Brown
1976, Luxton 1990). Members of the Histiostomatidae, Acaridae and
Algophagidae are common inhabitants of phytotdmata (OComor 1994).
Histiostomatids and acarids have also been fbund as associates of freshwater fish
and leeches (Proctor c t d 1997). Some Acaridae are amphibious, e.g. T ~ p b a p
p m c r n t h seems equally content feeding on fungus in mouldy grain or d-
lowing through culnrres of aquatic algae (Widtcr, pen. obs.).
Prostigmata
It is among the prostigmarans that one finds the greatest number of aquatic
species, concentrated in two major taxa. The Halacaroidea, with cwo or four
famiies (depending on the author) has about a thousand mostly marine species
(Bartsch 1996), and the 'true' water mites, the Hydracarina, includes about 5000
mainly k h w a t e r species in more than 40 W e s . Halacamids are thought to
be related to the Bdelloidea, a group of free-living terrestrial predators. Newell
(1984) considered the Halamidea to be polyphyictic but Harvey (1990) dis-
agrees and describes several synapomorphies uniting the halacacaroid families.
Water mites are members of the Cohore Parasitengonagwhich are characterisad
by a complex lik cyde with parasitic larvae and predatory post-larval stages.
Although earlier researchers considered the Hydracarina to be grossly poly-
phyletic (e.g. Pennak 1978). studies of larval morphology (I.M. Smith, pas.
comm.), structure of the male snifalia (Barr 1972) and sperm ultrastructure
(~lbe* 1980) support the m&ophyly of six superfamili& Hydrachnoidea,
Eylaioidea, Hydryphantoidea, Lbertioidea, Hygrobatoidea and Arrcnuroidea.
ACARIUNDERWATER, O R . WHYD I D M I T E S TAKE T H E PLUNGE?
Until reccndy there was -anent about whether two other superfsmilies
of aquatic parasitengone mites - che Stygothrombidioidcaand HydrovoMoidea,
each with one M y - are water mites KNU mjttO or if they represent inde-
pendent invasions of k h water (e.g. Cook 1974). R#mt scandng demon
microscopicstudies show that the HydrovoLjidac possess sou- &eriscic
of watw mites (genital acetabula) that were previously thought missii (Alberti &
Bader 1990);this observation has removed much of the rationale for excluding the
p u p h m the Hyd Srygothrombidiidaeare a harder case. Although they
have the rwo defining characters of water mites that arc lacking in temsmd
Parasitengona (two setae on larval palpal genu, combitions of skin glands and
trigger hats d e d glandularia), they retain aichobothria in the adult -a char-
acteristic that has been lost in the water mites ~ ~ JtriCtOl -rand they have a well-
developed empodia claw in the adult, a feature not present in any orher water
mite. The ~ g u c n c s sabout which ~ x should
a be included in the water mites is
rrfleacd in the number of names that have been applied to this p u p :
Hydrachndlae. Hydrachnidia, Hydrachnida and Hydracariaa We prefer the last
name because it l i 4 y means 'wacu mites' and we will use it generously ro refix
w all eight supcrfamilies, including Stygodvombidioidea and Hydrovolzioidca.
NUMBER OF INVASIONS INTO DIFFERENT
AQUATIC HABITATS
ThL is a -cult number to estimate, in part because it is h a d to delimit habitats.
Keepii in mind that these habitats can easily be subdivided into smaller units, let
us considcr thc following Lisc phytotdmara, remp0m-y fresh wacer, sranding fresh
watrr, running k h water, deep inmurial ficsh water, brackish water, &e inter-
tidal, marine deep intersritiai, marine subtidal (iduding abyssal). Another nason
why it is difEculr m enumerate invasions is that in many there have been repeat-
ed independent invasions of the same type of aquatic habitat h m land or tiom
another aqueous habimt So the tallies below should be taken with a grain of salt.
Phytotelmata
A phytotelm is a water-holding cavity formed by a plant, such as traeholes,
pitcher planrs and leaf arils. Phytotelmata are popular subjeas of study for com-
munity acologists because their boundaries arc relatively discrere, can be easily
replicated and the contained wmmunitics tend to have manageably low diversi-
ties (e.g. Naeem 1988. Jenkins & K i t c h i i 1990, Clarke & Kitching 1993).
Phytothata have been independently colonisad by the astigmatan W i e s
Acuidae, Histiostomatidae and Agophagidae, by mesostigmatans ( C . k ~ ,
Asddac).and by the water mites h u w kitchingi and an undescribed species
in the fgnily Anisitsiellidae (Harvey 1998) (Table 7.1). All p h y t o t h mites dis-
perse by waking (eg. to nearby pitcher plants, OConnor 1994) or by attaching
to insecrs. The Cbeimsn'us specics appears to bc amphibious, as we have observed
it walking under water and on the dry side. of containers (pers. obs., Walter,
Proaor).
Temporary freshwater bodies
Ephemeral ponds have been invaded by members of several families of
Hydracarina (Hydryphantidae. Eylaidae, Hydrachnidae, Piersigiidae.

MITES: A N D BEHAVIOUR
ECOLOGY. EVOLUTION
Arrenuridae, Pionidae) (Smith & Cook 1991). Water mites escape desiccation
in the dry season by burying themselves in the mud or when their larvae para-
sitise flying inseas that leave the pools. Smith & Cook (1991) suggest that tem-
porary water bodies am the an& habitats for most of the water mite M i e s
listed above and that only the Arrenuridae and Pionidac saoonddy invaded
temporary ponds fiom permanent water.
At leas three species of Oribatida in the Amuonothridae inhabit rock pools
that evaporate completely. When this happens, the mites runain in the arid silt
fbr days or we&, until the next rains arrive (Norton eta! 1996). Although the
three amemnorthrid species share an unusual morphological charaarr (a Light-
sensing lentidas), they arc widely separated geographically with one species in
South Africa, one in Ausualia and one in North America. It is thuctbre unclear
whether their morpholo~calsimilarity indicates convergence or common deri-
vation from a kngaean ancestor.
Standing fresh water
Permanent ponds, lakes, swamps and bogs have been colonised by many lineag-
es. In the Oribati4 d u M y Hydrozetidac k composed mosdy of spccies that
Livc,on macrophytes in standing k h water. The a n d hydrozctid may have
been a mite that fed on bkc-shore wrack and gradually got its faet wn, evolu-
tionarily speaking. In the Astigmaca, some species in the Euniy Hyadtsiidac
have been described f k m algae in ficshwater habieats (IGann.1978). As most
hyadesiids are marine or brackish-watcr inhabitants. the invasion of k ~ h water
-.
may have been scamdary. In the Prostigmata, smith.& Cook (1991) list 33 sub-
families of Hydracarina with representatives in these habicao but it is unclear
how many invasions this represents.
Also within the Prosrigmafa, the normally sea-going Halacamidea have
repeatedly invaded k h water. In some cases this may have been a passive in=-
sion. Bartsch (1996) hypothesises that many lakedwelling habcaroid species
originated from brackish-water mites whose habitats bccame land-locked and
slowly Vansformed into fiesh water. For example, the ancestor ofAstaropsiphap
p-tinrr. which Lives in the gills of the Australian freshwater crayfish Euart~~s
pint*, probably parasitid a crayfish that inhabited saltwater lagoons during
the Mesozoic Geological activity cut off the lagoons from the sea in the Tatiary-
Both crayfish and mite gradually became adapted to fresh water as their lagoons
became less and less bmddsh The same origin is possible fbr anothu associate
of fieshwatu crayfish in Australia, P '&ps (Paidae) (Harvcy 1990).
Other lineages of haacaroids may have invaded standing water by gradd-
ly moving up estuaries and adapting to the lower salinity in a leisurely way.
Sicmcr (1996) examined the distribution of halacarid species dong the salt
water-fresh water gradient in Weser estuary in Germany. Although more
numerous near the ocean, I r o b u~n b a w w occurxed at all salinities, while
0 t h species (eg. HirhcanUIlz htm) were restricted to hi$ salinities.
Running fresh water
Krana (1978) describes the mesostigmatan mite C h i n e & pmphora
(Dithinozuconidae) as b e i i 'virtually aquatic' in wet moss fiom mountain
streams in Oregon. Howam, as he managed to culture this species on wet Mter
paper, it seems to qualifjr more as 'amphibious' rather than 'aquatic'. Among the
II
i
I
ACARIU N D E R W A T E R , OR, WHYDID MITES TAKE T H E PLUNGE?
Oribatida, two species of Murronothnrr in the hmiiy Trhypochthoniidae are
benthic in cold running water (Norton ct rrL 1988). Most other trhypochthoni-
I
ids arc terrestrial with a kw species being amphibious in water and in sodden lit-
, toral vegetation. For these oribatids, it stuns reasonable to suggest a mode of
invasion from terrestrial to amphibious to obligatorily aquatic Murronotbrus
narnlis has been fbund in streams, springs and the boaoms of very cold lakes
throughout the wodd As M.naJalis has no way of actively d i s h this dis-
tribution indicates that its ancestor invaded water bcfbre the b d - u p of
Pangaea 200 million years (Norton etd 1988). In a survey of springs in the
Bavarian and Italian Alps, Schau and Guedrc (1996) fbund that M. MFlrlk
occupied only permanent springs where it made up about 45% of all oribatids
colleaed. Many of the oribatids they fbund were dearly accidental specimens
from nearby terrestrial and arboreal habitats; however, Pkztynothnrr p e h i
(Camisiidae) was also extremely common in their samples (34% of individual).
They concluded that it, too, was a m e subaquatic denizen of springs. Unlikc M.
&, l?pch#k occasionally occurred in intermittent springs.
Halacamid species from many genera arc found in cpibenthic substram of
springs and rivers (Bartsch 1996). Them have probably been mulaple invasions
of these habitats when mites m o d up estuaries into riwrs and perhaps via inva-
sion of springs through byprhcic hab'~tats.Smith & Cook (1991) list 25 sub-
&lies of water mites with representatives in runningwater. It scuns l i y rhar
many of t h e taxa arc recent invaders from standing water (e.g. some Unw&&
species) while others am ancient taxa that have been in lotic habitats since
Pangaean times (c.g. P r o a i i e ) .
Interstitial fresh water
I
Interstitial freshwater areas, including groundwater and the hyporheic regions of
standing and running water, are home to many hydracarines and h h i d s .
Them are about 540 species of water mites known tiom groundwater. Most of
these arc from superficial substrates but a fgir number, around 80 species, haw
been collected from well water that originatesseveral metres underground (Cook
1991). For both water mites and halacaroids, there have Likcly been repgtcd
invasions of interstitial areas from the sediments of springs and rivers and, fbr
some halacaroids, from sandy marine beaches. Ancient invaders can be recog-
nised by their lack of body and eye pigment, while more recent invaders and
inhabitants of upper interstitial areas may retain pigmentation. Another mor-
phological characteristic of many lineages of interstitial watu mites is a vcrmi-
fbrm idiosorna (cg. Stygothmmbidioidca, WanMinae) (Smith & Cook 1991)
or strongly flattened legs (see illustrations in Cook 1991, 1992), both pmurn-
ably adaptations for movement through substrates. Mom recent invaders may
show no morphol~gicaldivergence from their non-interstitial relatives. Cook
. (1991) mentions that nothing is known of the lifk history of deepinterstitial
water mites. He hypothesises that, because aerially dispersing insect hosts would
be difficult to find in these habitars, many species may produce non-parasiac br-
vac that transfbnn immediately into predatory dcutonymphs.
Brackish and saline inland waters
V . ionic gradients in brackish waar make adapting to such
difficult for most organisms. Among mites, halacaroids are the only regular

inhabitants of brackish water. Perhaps the greatest diversity occurs in the Black
Sea, which has a saliniry range of 18-22%. in which 34 species of halacarid have
been recorded (Bamch 1989). They also arc common inhabitants of brackish
water sand
~ - - flats.
..~ . .
With the exception of the Pontarachnidae, water mites appear to be par-
ticularly averse to salty water. A k species of Eyhis (Eylaidae) are able to deal
with brackish marine water but appear to have no special osmorcgulatory
adaptations (Olomski 1991). T i (1993) recorded six genera of water mites
from Ausvaian lakes ranging in salinity from 0.1-19.3 g/L. Species of
Amnutus, Diplodontus, @his and Hydmbna were recorded from mildly saline
lakes (3-20g/L), while Limnesia and P i o species
~ did not occur at salinities
greater than 0.3 g/L. T i (1993) states that Eyhis and Hydrrvhna were
the most salt tolerant but were abundant only at relatively low salinities
GzO.5 g/L).
Marine intertidal zone
S& submates of the intertidal zone arc home to a rich and diverse assemblage
of tenxxd mites (Pugh ct aL 1987,Emst 1996). Some of these species can survive
submusion in sea water for severaldays. With rrgard to auly aquatic mias, it seems
Likely that the intertidal zone is the a n d habitat of halaovoids. Many species
spend their lives in sodden shore algae in the splash zone (Bartsch 1989). An even
p a r number of halacamids dwdl in mom constantly submerged algae as welI as
among crevices in bamade colonies. Although numerous species inhabit the water-
loggad crevices of sandy beaches, they are very rare in silty flats ( B a d 1989).
Marine subtidai zone (including abyssal)
Many species of halacaroids that occur in the intecridal area also occur in and on
substrates in the permanently submerged subtidal zone. Here, as well as in the
intertidal, halacaroids are ofien associated with sessile invertebrates. Species in
the halacarid genus Bdyagauc live on colonial hydrozoans and have hind legs
adapted for grasping the stolons of their cnidarian hosts (Barrsch 1989).
Although halacaroids are most common on the continental shelf to about 200
m, nearly 50 species have been collected at ocean depths greater than 1000 m
(Bartsch 1989). The deepest record is fbr Batbyhalacatusquadtirumis at around
7000 m (Bartsch 1994). Although living kilometres beneath the ocean s&
would seem to require a very specialid physiology, few of these species arc
restricted to the deep sea. In somc cases, mites may have b a n washed into the
deep sea from their n o d subtidal habitats. However, there are two monospe-
cific genera (ColobocetlXSidCI, W&Clo&) and a scattering of other species that
are rcsuiaed to abyssal depths. AU truly abyssal halacarids lack eyes (Barcsch
1994). A p v i d female of one riftdwelling species. Copidogurkbus &nw, con-
tained an egg that enclosed a welldeveloped larva. This suggests that C &nu
may give birth to live young; larviparity has also been stggesd for some species
of littoral s u b - A n d c halacarids (Pugh 1996b).
Members of the water mite Family Pontarachnidae occur only in the littoral
tone of marine waters (Cook 1974). Pontarachnids arc unique among water
mite families, both in occupying completely marine waters and in lacking geni-
tal acetabula (see Osmoregulation, page 154). The hosts of pontarachnid larvae,
ifany, are unknown.
ACARI U N D E R W A T E R , O R . WHYD I D MITES T A K E T H E P L U N G E ?
I
I
(PRE)ADAIJTATIONSTO SUBAQUATIC LIFE
At the beginning of this chapter we pointed out how few arachnids other than
f
mites had taken up aquatic lifestyles. One explanation for this lies in basic phys-
iological and morphologid difkrences h e e n mites and other arachnids.
Perhaps most important among these are difkences in modes of gas exchange
and fi?eding, with spurn transkr also playing a role. In many casts, modilica-
tions that evolved in tcrteruial mites appear to havc allowed their descendants
to exploit wet habitats. This prc-adaptation hypothesis, applicable both berween
mites and non-mites and within mite lineages, explains why some ararinc groups 1
have been more succesful under water than others.
Gas exchange
The ancestral mode of gas exchange for chclicerates is the book gill, as exhibit-
ed by atant horseshoe crabs (Xiphosura). The extinct euryptcrids and ancicnt
marine scorpions also possessed-these external leaf-like +itory structures.
The invasion of land by scorpions was accompanied by the invaginadon of the
book gills into the ventral cuticle and the n m w i n g of the respiratory opening,
protecting the moist interior from the desiccating external aunosphere.
Liphistiomorph, mygdomorph and somc other primitive spiders exchange gas
solely through book lungs but more derivd spiders have rubular ~ c h e a sys- l
tems in addition to book lungs. In general, large-bodied arachnids have book
lungs (e-g. Arnblypygi, Uropygi) while smaller ones havc an insect-li mchd
system. Palpigrades are the odd arachnid out, in that they appear to h a y no gas
exchange system other than their integument. The Acari display a range of res-
piratory struccufcs that characterise the major lineages. No mites possess book
lungs. Rather, they have tracheal systems whose openings (= stigmata) W r in
number and position. The Opilioacarida havc four pairs of do& stigmata, the
Holothyrida two or three pairs of lateral ones, the Mesostigmata one pair of lat-
eral stigmata, Prostigmata one pair of prodorsal openings, and the Astigmata and
Oribatida (previously called 'Cryptostigmata') lack obvious stigmata pores
(although they are indeed present, albeit well hidden, in the latter). Very small
mites o h n have no obvious structures f$r gas exchange.
Why do stigmatal/uacheal systems allow mites to exploit water? Alone, they
do not, but combined with their overall smaller size, they do. If an air-breathing
arthropod is submerged, its respiratory tubes will fill with water ifthe openings
to these tubes arc large.Small animals, having a smaller mass of respiring tissues,
can make do with vuy small openings. The smaller the opening, the higher the
ratio beweem the s&u tension of the airlwater interface at the spiracular
opening and the external water pressure, and the less Likely it is that water will
enter the respiratory tubes.
Spiders that rtgularly spend time under water avoid drowning by maintain-
ing a layer of air around their respiratory openings that is supported by special
hairs. This layer serves as a compressible physical gill. Oxygen dissolved in the
water diffuses into the air layer and thence into the s p i r a c u l a r h k lung opcn-
ing, and C 0 2 diffusa out, as does the remaining nitrogen in the layer.
E v e n d y the nitrogen is depleted and must be replaced, either by the spider
returning to the s& or to an underwater supply in the case of Argytonrta.
Because of the small size and low oxygen requirements of most terrestrial
mites, their respiratory systems often a a as physical gills evcn without special
 MITES:
ECOLOGY,EVOLUTIONA N D BEHAVIOUR
modificationr (Hinton 1971). This allows temruial mites a few minutes grace , Relative to co-occurring insects and crusmceans, water mites are highly
to escape from flooded areas before their oxygcn supply expires. Many marine
littoral mite have no clear morphological adaptations to their soggy environ-
ment (Luxton 1990). For example, littoral arneronothrid oribaads rely on air s influence of different oxygen levels on several vital parameters of one lentic and
held in their extensive tracheal systemswhen submerged (Kranu 1978). Ifa mite
wishes to remain s u b m q d h r long periods of time, it would seem a simple
matter (evolutionarily spoking) m make the air-holding cuticular s& wider
to provide a grcatv d c c area fbr gas exchange by the physical gill. Thii
appears to be just what several aquatic and semi-aquatic mesostigmacans and
oribatids have done.
Hinton (1971) describes the physical gill of Phyci1u &(hcidae), a
mero~rigmvicinhabitant of marshes and other damp situations. The peritmcs
of most mesostigmatans are circular in ~ t ~ ~ ~ - s e c with
t i o n only
, a narrow slit
running dong the mrernal s& to connect the perinemad d u a to the out-
side atmosphere (as if one had & a long thin strip from a tube). Hinton
(1971) suggacs that the narrow aperture prevents large panicles fmm dogging
up the stigmata1 opening. In the semi-aquatic E italinrr, a cross-don of the
p e r i t m e appears semi-circular; so the d c e area available fbr gas exchange in
this mite is much larger than in its ternstrial relatives. A lining of micromchiac
presumably helps to keep the layer of air attached m the periaeme. Krantz
(1974) describes a very similar physical gill in the intertidal uropodid
Phaulodinychzu miti. Pugh er d (1987) suggest that the strucnue of the leg base
of Phaulodittychus 'tplcks and the coarsely sculptured integument of Thitt~anron
mkhucli (Thinozuconidac) may capture air bubbles that act as tempomy phys-
ical gills when these liuonl marine mites arc submerged. The aquatic oribatid
Hydmzes also has an armgement of micropapillae near the stigmata that
appeat to retain a thin layer of air. Krantz and Baker (1982) note that unsdero-
tiscd juvenile Hyhzzta lack this physical gill, and praumably ex&angc gws
through their thin integument.
k a n a (1974) noted that submerged PhaulodinychuJ mi* raise the dorsal
s&ce of their bodies to contact the airlwater int&ce and called this behav-
iour 'plastron capture'. Strialy, however, a p b n is an amqcment of fine
hairs that holds an incompressible physical gill that does not require replenish-
ment (D. Craig, pers. comm.). Hinmn (1971) states that Physn'w itnlinu can
say submerged indefinitely; this suggests that the physical gill borne by I? it&-
rr3 miaotrichiae is incompressible, making the mite more legitimately a phs-
tron-bearer. But many aquatic mitts either have not been observed to make
regular trips for Pir or else live in places where such journeys would be impossi-
-
ble (interstices or abyssal). These species asdgmamns, water mites, and halac-
aroids - undoubtably respire dermally.
Some of the larger waux mites such as Hydraclb~and &fa& have compkx sys-
tuns of dosed gas-filled tradleoles that lie unda the epidermis and swaddle maa-
bolidy active tissues like the brain and kg muscles 1984; Plocmr, p.
o h ) . In highly derotised water mites such as Anrnury the armour is puoauat-
ed with thinner arcas of intc&ument that allow loops of tracheoles to lie mom prm-
imately to the surface of the mite Thick-skinned water mites o& f' fin theit hind
legs aver their dorsal sucfkcs, presumably to 'fieshed the arygen supply. The ua-
chcal system of these wam mites doer not cornea functionally with the stigma-
ta, which are dosed and nonoperaave (Mitchell 1972, Wdes 1984). PreSucnably~
the same holds true h r the sagmatal opening of halacatoids.
ACARIUNDERWATER,
OR, WHYD I D MITES TAKE THE PLUNGE?
resistant to low oxygen levels; nevertheless, they may exhibit adaptations to the
0 2 content of their normal habitat. Young and Rhodes (1974) compared the
two lotic species of water mites. They found that the lenac mite Hydrvphanta
tmuabilir (Hydryphantidae) was an 0 2 regulator (i.e. had a metabolic rate that
was constant over a wide range of 4 concentrations). The lodc mites, hmia
mzchu (Limnesiidae) and Lebmtk quiqUCtlUZnJO~15(Lebertiidae), appeared to
alter their 0 2 consumption when the environmental concentration of the gas
changed (i.e. wexe 0 2 conf$rmus). The activity rate of L qru'qIKntlLCILIbmwas
g d y slowed by low OD L unAulntd was a&cted to a lesser d w , and H.
muabiCis did not alter its behaviour at alL The authors felt that these c W k n c e s
may result fiom H.tnnrrrbicrj' evolution in ponds that txperiena radical changes
in O2 concentrations compared to the more un&rm conditions of the streams
the other two species inhabit.
Feeding
With the exception of some harvestmen (Opiliones), all non-aCatine arachnids
fitd on liquefied prey that they have digested d y . Usually this prey is
macerated with the chelicerac and bathed in salivary products, and the resulting
goo is sucked in through set& that strain out unliquefied matter. As Preston-
Mafham and Preston-Mafham (1984) point out, this mode of external digestion
is unsuited to subaquatic habitats. D i t i v e enzymes would be diluted to
insipidness and the s& tension of liquefied prey (which allows turestrial
arachnids to 'sips the fluids) would not hold the dinner together. So the only
cnily aquatic spider, Agymncta aguarica, must drag prey into its air-filled diving
bell to eat it. The only way fbr an arachnid to eat under watu is to swallow
whole pamdes or to somehow avoid dilution of its digestive enzymes and dis-
persion of digcsud prey. Mites do both.
:Particl~nsult;ngis the normal mode of fixding in the Sarcop~rmes,so it
is not surprisii that many sarcopfirmans live subaquatic Lives. In contrast,
prostipatans are fluid f;ccdm that externally digest their food, usually liqueft-
ing it without macerating it Mrehand, and then sucking the soup through a
puncture hole in the epidermis of their prey or host. If the puncture is small, the
prey's body can act as a protective bag h r the digestive fluids of the mite. Below
we describe in greater detail the feading behaviour of aquatic mites, with the
, exclusion of mesostigmatans, as their diets are poorly known.
'
L i i their land-locked relatives, aquatic oribatids f d primarily on h g u s and
decaying plant matter. Hydmacm are ofien hund inside stems of aquatic plants
and on damaged and deterioratingleaves but it is not known whether their M-
ing causes the damage or if they simply exploit decaying wounds (K.rantz 1978,
Norton 1994). Norcon et aL (1988) examined the gut contents of the widely dis-
tributed springawelling species M w n o t b f w d Muls and immature
mites h m Canadian, French, A u s d i a n and New Zeaand populations con-
tained a mixture of filamentous algae, diatoms, hyphae, decayed vascular plants
and the occasional bit of arrhropod cuticle, s u g g d n g tbat these mites graze on
the periphyton growing on benthic substrates. An interesting exception to the
typical vegetable diet is shown by a species of ameronothrid that includes
 bdelloid rotifers in i t s meals (Norton et aL 1996). These mites have no obvious
adaptations for capturing moving prey and it is likely that the hapless rotifers are
engulfed along with detritus as the niites graze.
Most aquatic asrigmatans have also maintained diets similar to those of their
terrestrial progenitors, feeding on Fungus, decaying plants and bacteria. Fashing
(1994, 1998) compared the feeding methods of three treehole-inhabiting
species. Naiadacarw arboricokz (Acaridae) uses its powerhl chelicerae to bite off
chunks of decaying leaves and ingests them whole. Algophagus p t n ~ f u a n i n c r
.4
(Algophagidae) uses its more gracile mouthparts to scrape fungus from leaf sur-
faces. Honnosianoen~~ mallotae (Histiostomatidae) has serrate chelicerae that fil-
ter suspended bacteria and bits of detritus that it stirs up using its whip-like
palps. Judging by their gut contents, hyadesiids and other species of freshwater
and marine algophagids are algivores (Fain & Synnot 1981, OConnor 1994).
There are numerous records of aquatic acarids and histiostomatids collected
from the bodies of fish, both wild and farmed, and one report of these mites
inhabiting the integument of leeches (Proctor et aL 1997). Although this may
appear to represent parasitism, in the u s e of the leech and in many of the fish,
the 'host' animals were diseased and it appears more likely that the mites were
feeding on bacteria and fungus associated with necrotic flesh.
(6) Predation by water mites
Let us leave the slime-sucking and vegetarian mites behind and investigtte the
diets of predatory aquatic mites, beginning with the Hydracarina. Do their diets
differ much from those of their terrestrial relatives? Water mites belong to the
cohort Parasitengona. Terrestrial parasitengone species are parasitic on arthro-
pods or vertebrates as larvae and predatory on arthropods as nymphs and adulrs.
Insects, particularly the egg stage, are the main prey, while mites arc consumed
by some species of terrestrial parasitengones (Putman 1970; Chen & Zhang
1991; Wohltmann 1996). Often a younger life-stage of the larval host serves as
prey for post-larval stages (A. Wohltmann pers. comm.).
Figure 7.1
Water mite palps: (a)
Eudrps (Hydryphodae).
@f Huddma
(ttydrodromidae). (c)
Hydmdrno (Hydrachn~dae).
(d) Armnutus
(Ammuridae). (e) &fats
(+id=). (9 Rm'7
(Ptonidae). (g)
Notospcrchormpsts
(Sperchontidae), (h)
Lknnaio (Umnedrdae),
(1) Udnilmcypocom
(Uhidarrygacaridae).
(After various illumations
in Cook 1974.)
Altliough there is controversy about which lineage of terrestrial parasiten-
gones is most closely related to water mites (e.g. Witte 1991 vs. Welbourn
1991), the earlier dcrivative groups of water mites have retained the egg-eating
habit and, like their terrestrial relatives, often prey on the eggs of those insects
they parasitise in their larval stage (Proctor & Pritchard 1989). This diet is
reflected morphologically in the chelate palps of egg-eating mites in the families
Hydryphantidae, Hydrodromidae and Hydrachnidae (Figure 7.la-c). Palps with
a claw formed by a dorsal extension of the palp tibia (the 'palpal thumb-claw
-
complex') are also a characteristic of many terrestrial parasiten~onesand this fea-
cure has presumably been retained in primitive water mites, although it is also
I
145
possible that the structure has independently evolved. More derived water mite
cam have lost this chelate tip, although similar-looking uncate palps (Figure
7. ld) have evolved in Arrtr~urur(Arrenuridae) to grasp the slim appendages of
their crustacean prey. For those species with linear palps, the presence of sharp
spines or tubercles on the ventral side of the second palpal segment (Figure 7. lg,
h) is correlated with a diet of insect larvae and lack of such tubercles (Figure
7. le, fJ with a diet of small crustaceans such as Daphniu.
Even among closely related mites, palp morphology may indicate different
diets. Ullrich (1976) found chat Spcrchon set& (Sperchontidac) can prey on ver-
tically oriented simuliid larvae because i t can spread its palps sideways, whereas
other Spcrchon species must turn their
bodies sideways to gain purchase.
Another spcrchontid, Sperrhonopsis v r m -
cosa, is a sit-and-wait predator that stands
with its disproportionately huge palps
spread and lifted, waiting for dipreran lar-
vae to crawl underneath (Ullrich 1976).
This ambush behaviour is similar to that
shown by terrestrial mites in the family
Cunaxidae (see Fibwre 6.2). Not all pdps
can be readily correlated with diet, how-
ever, and direct observations are needed
to explain the function of odd srrucrures
(Figure 7.1, i). As well as eating dlc eggs,
larvae and pupae of aquatic insccts, water
mites prey on small crustacuns, indud- Figure 7.2
ing dadocerans, ostracods and copepods, Hydmdma (Hydmdmidae) reaching into rhe
on other water mites and somerimes on jelfy coar of a chimnomid egg--.
non-arthropods such as rotifers, nema-
-
todes and oligochaetcs (Table 7.2).
How do water mites catch their prey? Egg-eaters are probably attracted to
the surface chemical of the jelly coat surrounding their food (Figure 7.2). Wiles
(1782) found that Hydwdroma dcspicicm (Hydrodrornidae) repeatedly probed
glass beads embedded in the jelly of a chironomid egg clutch but showed no
interest in chironomid eggs removed from their gelatinous matrix. ffydrachna
(Hydrachnidae) feeds on insect eggs including those that are laid endophytical-
ly (e.g. many Odonata) and avidly investigates small wounds in plant stems by
inserting its long, curved rostrum. This behaviour led early investigators to
assume that I-fidrachna was herbivorous (see Bottger 1970). Davids and Belier
(1974) found that male Hydrad~naconjecta ate 2-4 corixid eggs a day.
 Strongly swimming mites in the families Eylaidae and Pionidae are voracious species appear to prefer cladocerans as prey, whereas Ncromznia prefer cope-
predators of small planktonic crustaceans (Figure 7.3). Ellis-Adam and Davids pods (Proctor, pers. obs.).
(1970) observed Piona alpicola (Pionidae) as it hunted and fed. The mites r e h e d Crustaceans killed by mites are easily differentiated from those that died
to eat ostncods or mayfly nymphs. Daphnia, however, were accepted. They occa- another way. Ellis-Adam and Davids (1970) found that mite-killed daphniids
sionally caught copepods but these prey items oken succeeded in escaping from were totally transparent save for the dark-brown gut. Riessen (1982) also
their grasp. Mires that had not been fed for several days swam about actively and found some dark para undigested in Daphnia, while Bosmirra was rendered
grasped any floating particle they came upon. Once a Daphnia was captured, the totally transparent. All prey showed characteristic puncture marks from the
mite manipulated it with its lcgs until its palps achieved a good grip behind the chelicerae. Eggs and embryos in prey animals appear to be undigested, as
dadoceran's head. Immediately after assuming this final position, I! alpicokz Riessen observed juvenile Daphnia escaping from the brood chamber of their
injected digestive juices into the .prey
. throush a hole torn in its canoace. Mitchell mother's empty husk.
(1962) felt-that incomparison with terrestrral mites, the great dcvel&xnent of the Many water mites are fond of dipteran larvae for supper (Table 7.2).
oral digestive glands in water mites, togetl~erwith the reduction in musculature Gerecke and Smith (1993) report that Nifotonia longipora (Anisitsiellidae) feeds
in the pharyngeal pump, suggests that hydrachnids have extremely effective exter- only on freshly killed larvae and make no attempt to capture prey themselves;
nal digestion. Ellis-Adam and Davids (1970) estimated I!alpicoks consumption however, the vast majority of mites that feed on dipteran larvae kill their own
of daphniids to be up to 10 a day. prey. The mode of prey capture depends in part on where the larvae live.
Kiessen (1982) outlined a similar
series of wents for prey capture by Piona
Exposed prey (e.g. mosquito larvae and
pupae) are encountered and attacked in
-
consm'r*~Riessen postulated that I! con- ;he water column apparently by chance.
stricra had a low preference for Once they are attacked by one water
Mesocycfops because of the copepod's mite, long, thin larvae such as chirono-
ability ro generate brief spurts of speed mids or chaoborids may be swarmed by
(up to 50 cmls) that allow the prey to hungry hydracarines until there is no
easily outdistance the water mite (whose space free for another pair of chelicerae
top speed is 2.5 cmls). Unlike Ellis- (Davids et aL 1981, Proctor pers. obs.).
Adam and David's observation that Tube-dwelling chironomids re-
copepods often escaped l? alpicola's quire a bit more finesse to extract.
grasp, Riessen found tllat once caught by Limnochares aquatica (Limnocharidae)
I?corummcta,Mesocyrlops never escaped. is a large, red mite with extrusiblc
Ricssen (1982) determined that nvo mouthparts that has a unique method
Figure 7.3 of the favourire prey of Piorza conshicta of preying on these larvae. The mite
An Eyfols (Eylaidae) mite feeding on a adults (and the only prey of the slowly approaches a chironomid tube
daphniid crustacean. nymphs) were Bosrnina and Chydorrrs. and walks towards the head end (Figure
He felt that the 'dead-man' response of 7.5). Presumably, ventilatory currents
/ Figure 7.4
these crustaceans (sinking pasively through the water once disturbed) makes xreated by the encased larva indicate to
, UnMnicola cmhsrpes (Unionicolidae) in
them ideal prey for the mites, especially for the smaller and slower nymphs. the mite which end is which. Once at nec-zrance posture,orienting to the
Chydoncr was slightly less preferred; this could be due to its thick carapace which the open end of the tube, L. aquarica vibrations of a swimming m h n i a .
may withstand puncture by Pionds cheliceme. waits ~atientlvfor the larva to extend its
Mites in the family Unionicolidae also prey on small crustaceans but, head to graze (Bottger 1969). The mite
rather than the above 'bump-and-grab' technique, they employ a subtler style then shoots out its extendible gnathosoma and grips the larva's head capsule with
of prey capture. Species of Unionicola and Neumania adopt a special posture its short, hooked chelicerae. A wild thrashing then ensues but the mire rarely
termed 'net-stance' when hunting, in which the first two pairs of legs are lift- loses its hold. T h e larva's struggles weaken and eventually cease as its brain is
ed from the substrate and held outstretched (Figure 7.4). With the exception digested, allowing Limnorhares to slurp its supper in peace.
of endoparasitic Unionicoh (see Parasitic water mites below), the fore legs of Encased chironomid larvae are difficult for less stealthy water mites to
these mites are armed with a battery of spines similar to those of other sit-and- extract. However, such mites sometimes have unwitting vertebrate allies. Ten
wait acarines (e.g. Caeculidae). T h e vibrations of passing prey cause the mites Winkel and Davids (1985) observed that the density of Ckzdotaryranus mancus,
to orient towards and clutch at the stimulus. Proctor and Pritchard (1990) a chironomid that builds a sturdy sand tube, was significantly lower in areas
found that Unionicofiz crassiprs would respond to the vibrating tip of a glass exposed to bottom-feeding cyprinid fish than in areas protected by fish exclo-
probe as if it were a prey animal. Male Nrurnanrtl appear to have taken advan- sures. They ruled out direct predation by fish bcc~usethe qprinids' ability to
tage of the female's predatory sensitivity to vibrations by incorporating leg sort the small larvae from larger bits of substrare was very low (about 1% effi-
vibrations into their own courtship (see page 69). Free-living Unionicokz ciency). The only other predatory animals in the man-made lake were two
 spccies of warcr mircs. Hygrobarer nigrornacukztus and H. rrigoaicrrr
(Hygrobntidnc). Laboratory studies had shown that thesc mites had difticulty
preying on the well-prorecred larvae and caprured, on avcragc, only onc larva
every 14 days. But when ten Winkel and Davids imitated the feeding behaviour
ofcyprinids by sucking up and expelling the substrate with a piperrc, rbe ratc of
prey capture by lab-held mires doubled. The authohors suggest that in the ficld,
where botrom-feeding fish son through 300400% of the lake's substrare annu-
ally water mites rely upon chironomids shaken from their tubes by fish as their
primary food source in the winter. During the summer, daphniids and tubclr;\r
chironomids (Srici,rochironornw hirmmo)are also fed upon by H. nipmnnrkzriu
(ten Wtnkel mar! 1989).
How do Hygrobara hunt for chironomids when fish are not aiding them?
Ten Winkel tt aL (1989) observcd an interesting behaviour exhibited by these
mircs: burrowing. H y p b a n r mgonicur was found to burrow to depths of up to
15 mm in quest of buried chironomid larvae, while H. nigromanrkzrur burrowed
to a maximum of 5 mm in the smdy sedimenrs. The chironomid specialist, H.
wigmicur, burrowcd irrespective of the presence of prey but H nigromcuhrw
only burrowed under certain circumsrances: if alternative prey (Daphnia) were
unavailable and if chemiul cues (from real prcy or crushed homogcnare) indi-
cared that chironornids were prescnr. T h e tubeless chironomid Sti~hwtczn~tariw
is favoured by thcse mires. Similarly, P~terson(1970) found thar Piona camea
(Pionidae) had difficulty attacking Glyprorrndiper larvae when rhey were in rheir
silken rubes hut readily fcd on those that had been cvicted.
I Water mites occasionally prey
on each other, especially in crowded
conditions. Davids (1973) observcd
adult Pionn roccinea (Pionidae) caring
nymphs of Eyiais (Eylaidae) while
leaving those of Hydachna (Hydra-
chnidac) alonc. Thc author felt char
this discrimination was bazed on rhe
much softer and more easily pierced
skin of Eykir. Elron (1923) mentioncd
that Piona bngipalpk attacks Lintnrsia
jirl'da (Limnesiidae) and Hydrachna
furcaw and that L./ulgida in turn will
prey on Eykzir.
What effect docs water mite feed-
ing have on prey populations? As
Proctor and Pritchard (1989) note,
there has been link resarch on the
role of water mires as predaron in
freshwater communities. However, a few studies of simple benthic and plank-
..
tonic food webs have indicated chat water mites may often be the coo orcdaror.
Tcn Winkel rraL (1989) estimate chat Hygrobatrrspp. in the Dutch man-made
Gliwia and Bieradka (1975) discuss the ralc of Piona limnmm (Pionidat) in
the planktonic food web of a neotropiwl man-made lakc. These mitts rcachcd
densities of about 1501m3 in the plankton. Laboratory studies showed thar feed-
ing rare on dadoceans was about 3-4 prey/mite/day; at that rate, the mite pop-
ulation would concume about 50% of the standing crop of cladocerans per week
However, this latter smdy did nor have a ficld component in which the actual
decline in prey numbers in mite-present and mite-absent enclosures was deter-
mined. Other evidence of high rates of prcdacion come from similar
srudies of field densities andlor laboracoty obsemtions of prcy consumption
4.
aces. Riesscn (1982 determined that Piona cornmi-rn (Pionidae) reaches densi-
ries of a b p 100/m in a Canadian lake and consumes up to 10 daphniidslday.
l i r d (194?) describes Limntsia jarnurmir (Limnesiidae) as eating 6 8 l m e and
of mosquitoes per day. Rajendran and Prasad (1989) calculare the
daily ?
up topredatlo
l8 rare of Encenrridophom rimilk (Unionicolidac) ro bc 40 mosqui-
to larvaelday. Davids rtaL (198 1 ) found thar at 2 4 C both Hygrobnrrs lorrgpalpu
(Hygmbatidae) and Limneria undukzm (Limnesiidae) arc o w chirooomid larva
every nvo days. They observed that Unionicokz marrips (Unionicolidae) would
kill on avcnge 18 copepodslday. Other observations of (i. cms;Pes found rhat
mites would kill up ro 20 cladoceranr equal to thcir own body size in G hours (=
801day) (Proctor. ;npublished dam). -
Egg-ating mites have also have large appetites. Davids (1991) mentions thar
an adult Hydrachm conjccra (Hydrachnidac) consumed about 200 corixid e m in
its lifespan, which is greater than the total liferimei cgg production of a female
corixid (140 eggslfemale). He suggested char thc c o d loss of corixids to egg pre-
dation would be at least 30%. Wiles (1982) observed one fernale Hvdrodrorna
&,picicnr(Hydrodrornidae) consume 235 chironomid eggs in I2 hour; The high
rates of predation on insect rgSs and larvae have led somc to consider rhcir use in
biological wnrrol of mosquitoes (Smith 1983, Rajendran 81 Pmad 1989).
But for several reasons, laborarory studies of prcdarion rates must be taken
-
with a wain ofsalt. First, mitcs may .
. be provided . . t h ~arc
with prey t normally nor
encountered (e.g. planktonic prey presented to a benthic mire), prey rhat are nac
allowed their normal anti-predator behaviour (e.g. chironomids removed from
rheir tubes) and thar are often oresenred in unredistic demirics. It is likclv that
in such situations, much of rhe prey mortality is 'wasteful killing', in which
,.
many "rev, arc killed but only . .parridfv consumed (lohnron
- cr aL 1975).
Certainly, if the (I. mrsipcr in the above example fully consumed the contents
of 20 cladocerans in an hour, ir would explode. It is also necessary to maintain
.,
(1985) indirectly achieved) are necessary before watcr mites can be considctcd
major controllers of prey populations. However, mites have one wcll-studied
characreristic that suggesrs they may share top predator m k with large piscivo-
rous fish: almost nothing will ear them (see page 155).

Lakc Maarsreveen reached densities of up m 1000 mireslmZ ofsubstrate. In win-
tcr, whcn no other prey arc available, Hypbatcr fecding reduces thc density of
the chironomid Cbzdomnvran~from28 000 to 12 5001m2. In contrast. in wecd
a r m (where dislodgcment of chironomids through fish feeding did nor occur)
CL?doranytarrw densiry incmscd.
(c) Pffrasirismby post-laml water mites
A fuw groups of water mites have eschewed their anccrrral predarory behaviour
" and become paasites in their posdarval as well as larval stages. Gravid female
Pamrirnlbia r u m m m k (Aturidae) attach ro the aquaric naiads of an ephcmerid
mayfly where rhcy become greatly engorged (Cook 1974). Armcorroton moflr
 EVOLUTIONA N D BEHAVIOUR
MITES: ECOLOGY,
(Asacocmtonidae) appears to be parasitic in the gill chambers of an Australian
cayfish (Cook 1974).
AU other water mites parasitic during postlarval stages have molluscs as
hosts. In the Pionidae, Najadicola i a p is parasitic in the gills and pericardial
cavity of a wide range of fteshwatec mussels (Simmons & Smith 1984). Both
adults and dcutonyrnphs inhabit the hosts and they cannot survive when
removed. When numerous mites inhabit a single mussel, the suprabranchid
chamber is occupied by a reproductively mature mde-funale pair and non-
reproductive mites skulk near the gill margin. Simmons and Smith (1984) sug-
152 p t that larval N. ingens may transform to deutonymphs without an
intcrrnediate parasitic phase on an insect host; if it does indeed lack an aerially
dispersing larva, then the geographically distant records from North America
and Thailand indicate that this species may have been present when these land
masses were contiguous.
The rype g e r k of the Unionicolidae, Unionicokz, is so named because
many species inhabit the mantle cavities of freshwater mussels in the fimily
Unionidae. Approximately 40 species of mussel-dwelling unionicolids are
known, and six species from mantle cavities of freshwater snails (Wets 1980.
Gledhill 1985). Not all Unionicoh species are parasitic; rather, some species
merely use the tissues of other animals (mussels, sponges) as safe, well-oxy-
genated places in which to deposit eggs and to pass calyptostatic insmrs
(protonymph, uitonymph) (Hevers 1980). Three other unionicolid genera
parasicise bivalves from the Unionidae (Irutsatar. AtnceIla) and Hyriidae
( Unioniiohpsis) ((Cook 1974, Viets 1980). Unlike Nc~jadicokaand host-
inhabiting halacaroids (see (d) below), there is good evidence that
Unionicoh species act as parasites (i.e. damage their hosts). Using histologi-
cal stains, Baker (1976, 1977) showed that U.interne& feeds on the blood
cells and mucus of its host mussel, Anohnta anatina, and that gill tissue at
the site of mite attachment becomes ruptured and swollen. The palps of
mussel parasites are highly modified relative to free-living Unionicoh and
seem to be adapted for rearing rather than for clutching and restraining
small prey).
Inhabiting mussels appears to have drastically altered the sex life of parasitic
unionicolids. All free-living Unionicoh for which mating has been observed
d r sperm without copulating; in contrast, direct sperm transfer has
evolved repeatedly within mussel-dwelling taxa (Proctor 1991). It is possible
that the slimy su&x of mussel flesh is a poor substrate for spermatophores;
perhaps this has selected for sperm-trans& through copulation in parasitic
species. Another dramatic change in tcproductive behaviour is in maltmale
interactions. Among non-parasitic unionicolids, male sexual competition is
directed against spermatophores, whereby males trample or deposit their own
spermatophores on those of r i d males (Proctor 1992). But many species of
mussel-parasitic Untonicokz have highly aggressive males that attack and
attempt to kill r i d males entering their mussel (Dimock 1983, Davids et aL
1988. Edwards 8r Dimodc 1991) (stc page 78). This behaviour can result in
dramatically female-biased sex ratios; fbr example, Dimodc (1983) b u n d an
average ratio of 30.8 female (I.@nnosa per mussel to 1 male. Thii aggressive
male behaviour not only excludes conspecific males from the harun-master's
mussel but it may also kp out other more peace-loving species of Unionicoh
(Davids ct al 1988).
ACARIU N D E R W A T E R , O R . WHYD I D MITES TAKE T H E P L U N G E ?
, (d) Halacaroidr will eat anything
The aquatic mites discussed above, although they may have expanded their diet
, relative to that of their terrestrial anwtors, have not made any major switches
between tbod types. Hahcamids, however, have been more adventurous in their
choice of cuisine. The presumed terrestrial ancestor of the Halaamidea was a
member of the superfamily Bdelloidea (discussed in Harvey 1990). This taxon
is composed entirely of free-living predators that feed on eggs, larvae and adults
of small arthropods (Kranu 1978). In striking contrast, h d o i d s a a as every-
thing from fungivores to predators to parasites.
1
Members of the halacarid subtgnily Rhombognathinae are solely algivorous
and live only within the marine phoac zone (MacQuitty 1984. Barrsch 1989).
They have long, fine chelicerae appropriate fbr piercing algal cJls and sucking
up material that 'has presumably been subjected to pre-oral digestion' (Barsch
1989). The genus PombaLacrlm in the subCgmily Halacarinae is also l i y to be
algivorous, judging by their o h green gut contents (Bartsch 1996). and some
species of HalacawUw and A c t u ~ m a h wnsume algae, although perhaps only
incidentally (Bartsch 1989).
Most halacaroid species are thought to be predators, although chii is based
on a limited number of direct observations. Bactsch (1996) lists protozoans,
oligochaetcs and other small metazoans among their diets. MacQuitty (1984)
observed cwo marine species of Agauopsis (Halacaridae: Halacarinae) feeding on
copepods. Agauopris nrmata preferentially fed on the earliest instars (nauplii) at
a maximum rate of 10 naupliilh. Agauopsisfltvssrrir preferred the larger adults
at a lower rated of 2 an hour. The first pair of legs of both species have modified
raptorial spines used to cage and restrain captured p q . The fim pair of legs of
A filirostrir arc about mice the length of A. nrrvatds, which sukgests that prey
references are based on the ability to handle copepods of diffkrent sizes.
AcamcheCopodia, Hakzcaarrrs and HaCaurmCCuF also have a spiny first pair of legs,
suggesting similar predatory habits. It is interesting to note rhar nrvo genera of
water mites with s i m i i modifications to their fim pair of legs, Nnrmania and
Unwnicola (Unionicolidae), indude copepods in their diets (Table 7.2).
A number of halacaroids are parasitic inside larger invedrara. Bartsch (1987)
lists marine species known m be parasites. Two Cbpithpuhs species are parasites
in decapods, one in the giU c h a m k of the slipper lobsur Parrib- antllntinu
and another tiom the egg packm of the spider crab Maja s q u i d -Another species
bund in the gill chambas of a marine decapod (Peltarisan zpinulo~~ll)is
Vchzuhbmu gmni Bamch (1987) poinu out that all three Spacia have d-
developed eya and w o n k whether the mites use light as a cue d e n s c a d i n g fbr
hosts. Certainly, warn mitts of the genus I/iridnicoka thar are parasitic inside fresh-
water mussels use a combition of host chemicals and light to sense when they are
safc inside a mussel (Welsh, 1930. Edwards & D i d 1995). In the hakcarid sub
family H a b d h x , h!i&ds *nis lives in thc gill and mande cavities of chitons
and gastropods. -P -appears to be an eaoparasite of the nunattan
Cmbmfu&u h q a h k . Bans& (1987) &%I that species in the genus B*gaw ate
parasites of hydrozoaas.Anotha probable parasite is EnProhalacanrr midpai)iz
(Enterohaacarinac)).It lives in the gua of sea urchins ( P a hindbm).
There arc a fcw species of frahwatu halacaroids that appear to be parasitic.
Rztacopsiph~~gur pamiticur is a gill parasite of the frahwater crayfish E u a ~ ~ u s
MITES: ECOLOGY,EVOLUTIONA N D BEHAVIOUR
~pinzjhin Australia (Bamch 1996). This is a very large halacarid - up to 2 mm
long -that has ban pIaced in its own subf$mily,the Astacop~ipha~inae. Another
hakcarid, fimnohalacdtus wackcri, has been co1lmed fmm the gill charnbem of the
European crayfish AWCW but it has also been found in aufaoc-and groundwate~
Bartsch (1996) suggao it m y be an accidental inhabitant of crayfish gills. On
firmer ground is Harvey's (1990) identification of P a d z p (Pezidac) as a parasite
of the gill chambers of tbe Ausuak cnyfirh Engan~zjC3toniIn addition to its
habitat, I? &s kdrr eyes,sqgesting a cloistered and potentially parasitic Litr. On
the other hand, Eirgtzcruspccier are bumming crayfish that dig tunnels up to a
metre in depth u the margins of swamps and streams Uona & Morgan 1994); so
it is possible d u t I? depr is a non-parasitic mite normally inhabiting inamirial
areas that is accidentally 'breathed in' by E $.&mi The exact diet has not been
determined fbr any presumed 'parasitic' speciesof halacarid, fkshwater or marine,
nor has the dfkt of haIaaroid pansitism on hosts been investigated.
Osmoregulation
Moving from Iand, where prevention of water loss is a priority, to fie&water,
where loss of soluble ions becomes a problem, has resulted in changes in the
osmoregulatory s m n u r a of aquatic mites. Aquatic astigmatans in the M y
Algophagidac have a porous Yrillnry pkte between their filar and second pair of
legs that appears to fimaion in the same ion-absorbing way as the chloride ccJls
found on aquatic insect larvae 0:ashing & Marcuson 1996). Similasly~the
urstigmata and acetabula bund in N~~ arbot.ico&z (Acaridae) and in
water mites also have the structure of chloride epithelia (Alberti 1977).
Urstigmata are ancestral in the Acariformes; pamitiform mites, in contrast, lack
them. The absence of these 'preadapted' structures may be one reason why par-
asitihrmans have so rarely invaded khwaccr habirats.
At the opposite extreme of ionic concentration, salty water is anathema to the
vast majority of water mites. The Poncuachnidae is an obvious rrrcepaon, as water
mites in this M y are rrstricted to che marine Littoral (Cook 1974). In a survey
of the water mite assernbhges of Sicily,Gerecke (199 1) found that in streams with
conductivities greater than 5 mSIan, only one of approximately 100 species -
DipIb&ntw snnrlp~nznrr(Hydryphantidae) - was common. Thc water boat-
man ~ c 0 r r j u cL x p k (Corixidae) appears to escape parasitism by water mite lar-
vae because it ouxpies inland waters too saline fbr the mites (Smith 1988).
Why are water mites, otherwise so robust to environmend extremes, so sen-
sitive to salt? The answer may be in the genital a d u l a . If they are des'ied to
efficiently take up ions fiom fieshwater, then an overabundance of Na+ and other
ions may 'overload' a mite's haemolymph. The marine Ponmrachnidae have lost
their a d u l a , which supporn this ionic werload hypothesis. However, Olomski
(1991) huad no mtistical evidence that &jlais tanti& (Eyhidae) fiom saline
ponds had any k m r @taI acetabula than individuals from Iess salty waters.
Sperm transfer
Spematlna of temmial a n i d do not respond wcll to being immersed in
hypotonic water. A p n c t a aputJca, the onIy spider that spends a major amount
of time unciefwater, transfvs sperm while in the air supply of the female's diving
bell (Bristowe 1958). (199 1) suggests that adaptations to keep sperm moist
in terrestrial habitats may have helped the ancestors of water mites to avoid
osmotic damage to their sperm when they invaded fresh water. Terrestrial para-
sitengones typically uansfkr sperm in a very iadirea way. Males deposit sper-
matophores (of& in the absena of U e s ) and f d e s may come across the
spermatophores at a later b e , at which point they may or may not take up the
sperm packet Dissociared &also occurs in some other prodgnatam and
oribatid mites (see Chapter 5). The temporal disjunction between deposition and
up& means that sperm cells are exposed to low humidities prior to being taken
up by fhales. The osmotic stress placed on sperm of dissociated terresaial para-
sitengones has selected h r very clever packaging. The sperm cells are wrapped in
coats that are impervious to water and the fluid surrounw these packets h
hypphilic (Witte 1991). spermatophores of these mites 'osmoregulate' inde-
pendently, keepii the sperm cells surrounded by a liquid.
The impervious wrappings of the sperm not only prevent water b m leav-
ing the cells but also they keep ex- water fiom entering. Witte (1984, 1991)
suggests that it is this characccristic that has allowed the ancestor of water mites
to&vade water while rrraining external sperm 4. The spermamphorer of
terrestrial oribatid mites also appear' to have some osmoregulatory ability
(Albem n d 1991), that this may also be a 'prtadaptati~~ for inva-
sion of aquatic systems m onbatids. Astigmatans uansk sperm directly through
an aedeagus, thus sperm cells are not exposed to external conditions. Sperm
transfix in mesostigmarans typically involves a d c introducing a sperm packet
into the fkmaleSssperm receptacle. Thii mode of uansfer is unlikely to select for
osmoreplatory abiiy in spermatophoresand may be one reason why there are
no mesostigmatans known to spend their entire &-history under water. Little
is known about sperm aansfkr in halacads, although fiee-scanding sper-
matophores have been described k r Halacadus bastct.i.
Although the r e d relatives of water mites show no inchation to dkect-
Iy uan& sperrn, copuladon has evolved repeatedly within the 5000 species of
water mites. Using a comparative method, Proctor (1991) tested two hypotheses
about why direct transfClr has evolved so o h in the hydracarines. There was no
evidence that disruption of phcromonal communication between spermatophores
and females was the selective krce, as lineages inhabiting running water showed
no greater tendency to evolve copulation than those in standing water. However,
lineages of swimmhg mites did show a significantly gtxcer number of independ-
ent evolutions of direa spenn tradk than did lineages of crawlingmites. Proctor
(1991) suggests that movement of M e s into the three dimensional water col-
umn decreases the pmbabiity of contact between f;emalesand subscratedeposited
spermatophorcs. In thissituation, males that captured fknales in the water column
and tmdkmd spennatophores directly would be fivoured.
PREDATION ON WATER MITES - THE
CORRELATION BETWEEN FOUL TASTE
AND BRIGHT COLOUR
Water mites are only occasionallyfound in fish stomachs and it has been assumed
that they are seldom preyed upon. Eriksson a aL (1980) report &at of 21 635
food items identified from the gut contents of perch, only one was a water mite.
ICeeley and G m t (1997) found that although lentic water mites made up 14.9%
of all individd invertebrates driing in a suwm, they represented only 0.4% of
 items in the stomachs of resident salmon. In contrast, other organisms in the drift Kerfoot wanted to test Elton's hypothesis that rcd colouration enhances
appeared to be fed upon in proportion to their abundance. Modlin and Gannorl learning in fish, as well as the hypothesis that red mites are especially unpalat-
(1973) examined the stomach contents of 157 specimens of alewife (Alosupsc~o- able relative to non-red hydracarines. He found that guppies learned to avoid
barengus) from the Great Lakes in North America and found that fewer than 2% black balls of food mixed with powdered Linrnocbures (a distasteful red mire) just
of the stomachs contained mites. These mites were not noticeably digested, even as rapidly as they did similar red-dyed balls. Thus Elton's first hypothesis was
when found in the lower intestine. Cupp and Willis (1982) removed 36 living rejected. But, in general, powder from red mites was rejected at much lower con-
Lebeka mites from the upper and lower intestines of a single green sunfish, centrations than powder from dully coloured mites. Kerfoot felt that these
Lepomis ryanel'. The mites first moved freely about but expired 10 minutes after results confirm 'that large size and bright-red coloration are serving an apose-
removal from the gut. It appears that water mites not only are rarely preyed upon matic function in mites and suggest that the mites generally found in the stom-
15G by fish, they are also extremely difficult to digest. achs of fishes are more poorly protected species'. As predicted by Kerfoot, tlle 157
Pieaynski (1976) summarises a 3-year study of the effects of increased fish numerous Lebertia found in the green sunfish intestines (Cupp and Willis 1982)
stocking on the animal communities in a Polish lake. Tench, carp and crucian and those in alewife guts (Modlin and Gannon 1973) were non-red species.
carp all contained water mites in their guts, making up respectively 0.5%. 0.4% There can be little doubt that red water mites are particularly distasteful to
and 2.2% of the biomass of all gut contents; however, the assemblage of mites fish. However, the claim that water mite assemblages are more biased towards
in the guts differed considerably from that in the habitat. Consumed mites were red species in water bodies containing fish has been called into question. Kerfoot
smaller (500-1000 p m vs 1000-2000 p m ) and more dully coloured than tile (1982) collected mites from only eight water bodies (six with fish, two without):
mites that were common in the habitat but rarely found in [he fish guts. a rather small sample size. To test the generality of Kerfoot's observations, Garga
Piecsynski suggests that these small, dull mites are probably 'caught by the fish (1996) collected more than 6000 water mites from 2 6 fish-present and 2 0 fish-
accidentally, together with other representatives of the invertebrate Fauna, con- absent water bodies in southeastern Ontario and classified each mite according
stituting the basic components o f their food'. to colour. Contrary to Kerfoot's findings, she found that assemblages of mites
This semi-immunity from fish predation has puzzled biologists for many from sites lacking fish were much more skewed towards redness than those from
decades. Especially disconcerting is the fact that even hungry fish will ignore sites with fish (Figure 7.6). These results make the hypothesis of fish-driven evo-
large, brightly coloured water mites. Elton (1923) was among the first to note a lution o f redness unlikely.
correlation between the co-occurrence of red-coloured mites and fish in the same Rather than redness repeatedly arising within the hydraurine clade (as the
body ofwater. O f the nine species of t~~dracarines he collected from a ditch occu- Miillerian mimicry hypothesis of Elton would hold), it seems more probable
pied by stickleback, eight were scarlet. He found that hungry fish would mouth that redness is a holdover from water mites' terrestrial relatives. Terrestrial para-
the water mica but would spit them out immediately; chis occurred w e n if the sitengone species are ovenvhelmingly orange or red in colour. T h e related cohort
fish had been starved for 10 days. Elton speculated that the dorsal skin glands
(glandularia) common to all water mites were the source of a foul exudate. The
release of this secretjon would be triggered by bending of the large sensory hairs
found near the openings of these glands. T h e fish, when mouthing a mite, would
be punished by spurts of noxious chemicals and would hastily release the unpleas-
ant mouthful. Elton evoked Mullerian mimicry to cxplain the prevalence of red
among mites associated with fish. He also thought that the colour red may have
a more striking effect on piscine retinas than d o other colours.
More recent research has had similar results. Kiessen (1985) states that Piona
consmkirr is distasteful to fish, as he observed that after a few tentative attacks on
the mites, fish tend to avoid consuming them. Kerfoot (1982) took an experi-
mental approach to explaining his observation that red predominates among
assemblaga of large-bodied, fish-associated mites. In bodies of water containing
fish, he observed that most zooplankton use transparency to solve the problem
of concealment against a background that continually changes in brightness and
colour. Water mites, however, seem to advertise their presence in open water.
Like Elton, Kerfoot found assemblages of 3-9 species of red water mite.. in fish-
inhabited ponds, while fishless ponds contained more yellow-brown species.
Using laboratory trials, he found that if a fish is truly naive, e.g. aquarium-raised
individuals, introduction of a water mite almost always attracts the attention of
the fish. Often it will completely swallow the mite or, more commonly, mouth
it and reject it. Rejected mites seldom showed damage. Subsequent trials indi- I rhos* wid, h e largest (Modified from Garga. 1996.)
. .
I
cared a rapid drop in interest as the fish became more familiar with the mites.
 ACAKI ~ N I > I ~ R W A T E O
KR, . WliY IIIU M I T E S T A K E T H E P L U N G E ?

Anysrina also contains primarily lnrgc, red, activc predators. Thosr warer mircs white to red, depending on d ~ espccia) ro W lighr, to determine whether red-
char are considered 'primitive' are also rypiully red (c.g. I-lyJryphnntidze. pigmcnted eggs arc more likely to produce healthy larvae.
Limnocharidae) and it seems likely thar red pigmentation is an ancesrral trait in In conuasr to pr&don on warer mica by fish, lidc work has b a n done on
the warer mites. inverrebrate predators. Uron (1923) sated rhat an adult A g a h beetle (Dpcidae),
Bur whar of the foul flavour associarcd wirh red warer mitcc? Garga (1996) which had never been exposed ro mites before, artackcd and ate a red Hydwhm
rested the hypothesis that disrasrefulncss as well as redncss is a wrry-over from Pennak (1978) says that water mires fall prey ro numerous invertebara including
the terrestrial ancesrors ofwater mires. Using Kerfoot's (1982) mcrhodology, she Hydra but does not provide referenas for rhis claim. Apparently the foul exudate
presenred sunfish with flour balls made with varying proporrions of powder so distarteful to fish does not bother those water mites rhat prey on other
from dried vclvcr mites, Dirrorl,rornbium magnz/imrn (Trombidiidae). a large hydnwrines, as borh Elton (1923) and D a d s (1973) mentioned that && idcn-
desert-dwelling paasirengonc. She found char fish rcjecred the flour balls at con- dfied by Kerfoot as a particularly potcnr red mite, was earen by other mite species. I
centrations of mite powder as low as Kecfoor had found for rcd warcr mires
(95% rejection ar 15% mire by weight).
Garga hypothesised thar red pigmcnrarion had initially cvalved as
m o t e n o i d - b a ~ dphotoprotecrion in chc rcrresrrial anccsror of warcr mites.
Among the various Functions proposed for wrotenoid pigmcntr, the b a r undcr-
scood and most researched is protection against photodynamic injury
(Goldstrohm & Lilly 1965). Thc phocoprocective role of carotcnoids has hem
observed in organisms as diffcferenr as bacteria (Marhews & Sisrrom 1959). Fun-
gus (Goldsrrohm & Lilly 1965) and copepods (Hairston 1976. Ct~alkcr-Scott
1995). Carorenoids have been found in many species of red warer mites and rcr-
rcstrial parasitengones (Manunra 1939, Green 1964, Czccruga & Czrpak
19G8a, b, c, Meyer & Kabbe 1991). Garga proposed char rcdncss has been
rerained in chore hydrawrincs living i n shallow, olicn temporary wnrer bodies
(which are also typically fishless) bur h a repcaredly been lost by groups inhab-
icing deeper water where damage by lighr is less likely. Photoprorccrion by pig-
ments wn occur nor only at rhc ndulr srage, bur in rhe egg and larval rrages.
Indirecr evidence for wrotcnoid-bared pboroprorcction in rerresrrial parasircn-
gones is thac chiggers (larval Trombiculidar) dwelling in rhc ncsrs of rheir hosrs
are typically pale yellow, whcrca those rhar roam about in scarch ofhosrs (and
hencc are cxposcd to lighr) arc brillianr red ( K n n ~ z1978). There is olro cir-
cumstanrial evidence from ocher mite r:ua. Norron rr rrL (1996) describe orib-
arids that are active in shallow (2-5 c m ) cempocwy puddles of warcr on rockc
outcrops (see page 138). Thcy consume orange-coloured bdelloid rotifers and
themselves produce e m thnr arc bright orang", 'a color nor previously reporred
for eggs of Oribatidi.
To cxplplain h e zsociadon between rednns and disrastcfulncti, G a p ruggesrs
that once redness evolved in terrarial pansitcngones, it pur these large active mircs
at risk from visual predxon such as reptiles, amphibians and birds. DLmtcful cxu-
dares evolved to counter this higher visibiliry and werc likewise maintained in the
still visible red water mice, but to rebuff prcdarion by aquatic rather than by rer-
resuial vcrtebares (Fi'igurc 7.7). Viual vcrtebntc prcdarors in rempomry warcr bad-
ies would mosr likely be amphibians. Donnelly (1991) found thar mites composed

-
up to 40Yo of the stomach conrcntr of poison arrow fmgs m d Flowen and Graves
(1995) observed mites in 70% of w i n e d toad sromacl~s;unfnmnately, in bath
of t h a c mites wcrc not idendficd ro anything marc specific than 'Agri'. To
our knowledpe, there is no information about whether vclvrr mites and rheir kin
are eaten by Kwrds, Frogs, s h a n d e n or birds. It would be very inreresring to resr
the palaahiiity of rcd terrestrial and aquatic pansitcngones on potenrial tcrresrrial
predators. As weU, it would be valuable to test the 'photoprotecriori hyprhc+ of
Garga (1996) by subjecting diff&cnrly mlourcd watcr mice eggs (which range horn
Bottger (1962) found that hydra would grab I'ioruz nu&& (Pionidae) but would Swimming
release them almost immediately. Afcer a few minutes the stunned mites appeared
Swimming has evolved indcpcndently in many lineages of aquatic insects, e.g. in
to recover and swam off normally. Notonecrid and naucorid bugs would not eat
them. Larvae of dytiscid beetles would release the mites after gabbing them bugs, beetles, caddisflies and true flies. In contrast, few of the major lineages of
(although ofien the mites were mortally wounded). Other species of Piom as well aquatic mites have evolved nacatory locomotion. There are no examples of swim-
as conspecifics would eat I?nodata, as would zygopteran larvae. Bihger speculated ming species among the Parasitiformes, Halacaroidea or Oribacida (but see
that water mite glandularia release unpleasant chemials that deter predation, but Levitation, below). Among the Astigmata, only a few species in the genus
he did not explain why damselfly larvae were unaffected. Proctor (1992) found that C r a m r i a (Histiostomatidae) have exchanged walking for swimming. Fashing et
males of the small blue mite Neumaniapapihtor (Unionicolidae) were more likely aL (1996) describe the behaviour and morphology of a Creurzrria species from
than females to be eaten by odonate larvae ((schnura, Libellufa) and by the water Australian pitcher plants. Nymphs, males and females have highly modified legs
1
mite Limnesia sp. (Limnesiidae). She postulated that males were more susceptible bearing long whip-like setae at their tips. The male bears a remarkable likeness
to predation because their active mate-searching behaviour increased their to a planktonic copepod nauplius. However, this crustacean-like morphology is
detectability by or encounter rate with predators.
Like the interaction between Hypbates spp. and bottom-feeding fish
described above, in which fish increase the number of prey available to the mites, Figure 7.8
The effect of srocking
there are examples of fish presence helping mites by reducing predation on a reservoir with u o u t
them. Eriksson et al. (1980) noted a strong positive correlation between lakes on the popularion size
that contained fish and lakes that contained the water mite Piona carnea of the water mite
(Pionidae). In a field experiment they divided a fishless lake in half with a net h a amea .- &
barrier, and introduced perch to one part. In the second year of the srudy, they
found that water mites were present only in the half with fish. Co-occurrence of
(M,.(Mdiied
from Puncochar and
Hhacek 199 1 .) More Piona carnea
&-
d~esetwo taxa due to a similar preference in abiotic surroundings could be ruled
out, as condirions in the divided lake were similar on both sides. Eriksson et al.
performed a series of laboratory experiments in which perch were kept together More chimnornid
with water mites and a number of potential insect predators of the mites. hosts for water
Lericorrbinia, Coenagrion (both odonates), Notonecta Glaenocorixa, Sigara (all mite larvae
hcmipterans) and C h b o t u r (Diptera) fed on the pionid water mites. Aciliurlar-
vae (Coleoptera) did not. The perch also ace water mites but preferred the avail-
t
able insects in all but one case (that of Leucorr\~inia).The authors explain the Fewer small
higher abundance of water mites in lakes containing fish as follows: in lakes benthic insects eaten
without fish, 1? carnea are kept at low densities because of the predation pressure
from aquatic insects. In the presence of fish, predatory insects decrease in num- Fewer Hemiptera Fewer cladocerans
(predators of water mites) eaten
ber because of increased predation pressure from fish. This implies decreased
pressure from aquatic insects on water mites, which is not compensated for by
an increased predation from fish so long as alternative prey arc available.
A similar phenomenon and hypothesis were described by Puncochar and
Hrbacek (1991) to explain the co-occurrence of trout and Piona cantea in a
Czechoslovakian reservoir. When trout were present there were high numbers of
P carnea (and other mites); when trout-stocking ceased the smaller fish species
that the trout normally consumed increased in number and the water mites (Z?
carnea in particular) decreased dramatically. The authors suggest thac predation
by trout on large insects reduced predation on mites, and that the trouts' con-
sumption of small plar~ktivorousand benthivorous fish kept the mites' prey and
host populations (cladocerans and chironomids) high (Figure 7.8).

LOCOMOTION
Aquatic mites have a grcxer variety of options with regard to locomotion than
do their land-bound relatives. They may crawl, burrow or swim - the last
being the equivalent of flight for terrestrial organisms.
 MITES: ECOLOGY,EVOLUTIONA N D BEHAVIOUR
1
I
the d t ofa wmpromise beween sex and swimming. The male uses his strong
brelcp to grasp the female whiie mating, and the second pair of legs are used
both for swimming and for holding onto a substratewhen the first pair arc con-
nubially occupied.
It is among the Hydracarina that we find the greatest number of swim-
ming Acari. Water mites show a gradation of competence in swimming, from
crawling and burmwing forms completely incapable of natatory locomotion to
pe!agic water mites that spend much of their lifi in the plankton. Bottom-
dwelling water mi- generally lack the long, slender setac rumad 'swimming
i2 hairs', which are found in more natato'y forms. Swimming abiity seems very
labile, having arisen and disappeared repeatedly in d i f k n t lineages. The inva-
sion of fist-flowing warn or interstidal habitats is often associatedwith a d u c -
tion in size and number, or total loss, of hairs. Using the pmence of
swimming hairs as a prory. Proctor (1991) exammod thc diJtniution of swim-
ming abiity among 343 genera of water mi=. She fbund that 89 genera (26%)
were composed entirely of swimming species. I92 genera (56%) war entirely
non-swimming, and 62 genera (18%) contained both nvimmhg and non-
Swimmingspeciy
Bam and Smth (1979) examined the bbdclilcc s w h n + ~hairs of the mite
Limmckum (C$&thtrj;) mmhma Thcy Mt that the swmming mat of L.
.
rmLniuuta probably lose some efficiency duough their structural draraacnsa.a.
especially whcn compared m the sti&r setac of natatory inseas. Barr and Smith
pe&rmed depilatory expuirncnts on these mites and hund that swimming
abiity was eliminated whcn 80% of the swimming hats wmc removed. Even
though n o d swimming mwunents occurred, & mites could not generate
enough lift to move off the boaom
1; the same study, the sctae of L amrrirana were fbund to be almost uni-
form in width fiom base to tip with no particular morphological elaborations.
The more pelagic mite, Piona rodckr, has more complicated natatory setae
(Riessen 1982). These are widened and flattened at their distal ends to make
them spoon-shaped. As well,the setae themselves are fringed with short hairs,
structures that probably add to swimming efficiency. Cuticular structures
other than setae may also be involved in open-water movement. Hdik (1924)
proposed that pelagic Unionirola species (Unioniwlidae) could erect thick
setae on their legs while drifting to serve as a sort of parachuu. However, as
many species of Union&& and other unionicolids in the genus Nnrmrrnia
employ these collapsible setae fbr capturing prey (Figure 7.4), it is not dear
whether locomotion or predation was the primary selective fbnc behind their
evolution.
Among swimming mites, habicac choice is often corrrlad with swimming
abiiry. B6ttgcr (19624 cornparad three species of Gcnnaa waw mites.
Anrnurw globarur (Arrenuridae) was che weakest swimmer and was most o b
captured in ncas-shore vegetation. &j& i+dbult% (Eylaidae) was the
strongest and most penevaant swimma of the thnx and was most commonly
b u n d in open watet. PioM wubz (Pionidae) between the orhcr two in loco-
motory &acncy. Prediaabb it was f b u d boch among litcoral macrophytes
and in open arras. Picaynski (1964) wd trapabiity in stationary traps vs. d i p
nets as an estimator of wata mite motility. As a whole, watcr mites ranked
between cuatopogonids and mayflies ip motility, with beetles and corixids t o p
ping the List and isopods being the least motile. Withii the water mites,
Hjpbarcs nipmaculatus (Hygrobatidae) was the most motile, followed by
Hydro&uma a!zpin'nrr (Hydrodromidae); poorly motile species included
Mk%opsir irr6incl;lris (Midsopsidae) and PioM conglobatu (Pionidae), which
Pieaynski ranked as sluggish as kopob. Of course, this all depends on whether
all taxa arc similarly 'traphappy'.
Barr and Smith (1980) b u n d the swimming veloaty of Limnocham -
UIM to be about 1.6 d s . Riessen (1982) fbund that the adult stage of the
pelagic water mite Piona mmtnkta could swim at speeds of 2.0-2.5 a d s . These
open-wafermites typicallyswim tbr short periods of a fkv seconds on one wursc
and then switch direction. Ricssen states that swimmingspeeds of various poten-
tial prey of I? are usually less than 2 mmls. Proctor (1988) determined
that U n h k o h etawipes (Unionicolidae), when prodded by an observu; swam at
an average rate of 0.84 a d s .
Smith and Barr (1977) fbund that Limmchmaprknarilyuses light direction
to orient i d w h i l e swimming. Botcbm lightinginan aquarium caused the mite
to swim in loops with the v e n d &i d Runoval of the eye capsule of
fimmrhamrrsulted in normally oriexid s i j (dosum upwards), regard-
less of the direction of lighting. This indicates rhat some cue other than light is
a h used for orientation. Wngcr (1962b) hund that when presented with light
from below, artcndmz (Eybidae) wodd try to swim upside down but,
begusc of the shape of its body, it would end up swimming in Imps.
H g v i r y p ~d m (Hydtyphantih) behaved as &&is, except that when it
contacted tbe substrate the tactile suw omrode the visuaI and the mite would
orient so that its k g tips touched the surfkcc. B8ttgcr bund that P ~ mdata M
(Pionidac) initially went into a series of wild rolls until it crashed into the side
of the container but that over time these mites became acclimated to the invett-
ed light and c v e n d y 'learned' to swim in a normal fashion. Berrgcr suggested
that the trailing fourth pair legs of many species of water mites act to generate
lift when the mire is swimming normally but causes looping when the mite is
upside down.
Positive phototaris is common in water mites, as evidenced by mites' greater
activity during the day than at night (Pieaynski 1964). Among lentic taxa, the
tendency to be day active is stronger in littoral than in open-water. species.
Similarly, lotic mites ofien have their peak drik during the day (Schmidt 1969).
PioM &(Pionidae) and Limneshz undula*r (Limnesiidae) are very strongly
a d m Light, which B(lctgcr (1962b) s is an adaptation to avoid oxy-
8-
gen-poor deeper waters. He introduced C -laden n t e r to the bottom of an
aquarium and the mites responded by ssrimminra' to the &but d e n he lit
tbe aquarium from below they swam to the bottom and suffocated, suggesting
that it isL.icbt iiberAlt& even when it does not make sense. However,this atuac-
tion to lighc does not hold LCall species. An illurninad Hya5yphantes d m
(Hydryphantidae) will crawl ceaselessly until it ma&& shadow (Biittger 1962b)
and most intczsatial taxa ace also photo-negative.
Levitation
Aquatic oribatids of the family Hydrozcadae do not look much different from
tenrstria oribacids and move at the svae sedate waking pace as they a w l
among water weds but Hydro- makes w of air in a novel way. Newel1
(1945) noted that H.larumir and perrrrnkcvitchi often contain bubbles of gas
in their midgucs and that by releasing their grip on the substrate, they would
 MITES: A N D BEHAVIOUR
ECOLOGY, EVOLUTION
float up to the water's surface much more rapidly than they could crawl -
rather l i k underwater ballooning. He called this activity 'levitation', and
em~hasisedthat '[tlhis most appropriate term is used in its preferred sense, and
is in no way intended to sugest the unhrtunate connotation applied to it in
spiritism'. Newell noted that agitating mites would induce the fbrmation of
these bubbles, suggesting that this may be a form of rapid escape response.
Levitation occurred, however, not only a f c a the mites were agirated but a h
whenever ambient light conditions M low enough. Hydroatk.shas pigment
spots that would allow it to deucc light Keeping mites in a thoroughly dark-
ened aquarium did not induce levitation; it appeared that the mites responded
only to a change fkom high to low intensity. Newell suggested thar levitation
would allow animals that had been dislodged h m their normal home on
plants in the photic zone to escape starvation and death by the anoxia that
would occur at the dark bottom of a pond. He was uncertain about how
Hyckozetes generates and regulates the gas bubble.
SENSITIVITY AND DIVERSITY - WATER MITES
AS ENVIRONMENTAL INDICATORS
Organic and inorganic pollution of fresh water is often monitored by subject-
ing individuals to water containing a suspected pollutant (bioassays) or by look-
ing at the species richness and composition of invertebrate assemblages in a
water body (Rosenberg & Rcsh 1993). Biodiversity is o h also used as a meas-
ure of the nebulous quality termed 'ecosystem health'. Mites have been
employed as bioindicators in terrestrial systems (e.g LagedZif & Andrtn 1988,
Koehler 1992) but water mites are typically ignored in studies of ficshwater
health (Resh & McElravy 1993). Promoting one's fivourite taxon as an indica-
tor of pollution is a popular pastime among freshwater ecologists. It is therefore
-
disappointing to find that -physiologically water mites do not appear par-
ticularly susceptible to contaminants. We have observed water mites swimming
energetically through a soup of decomposed zooplankton and insects. As well,
along with beetles, water mites tend to be among that last invertebrates to
expire in collecting jars filled with ethanol. Pieaynski (1976) lists studies that
show water mites to be insensitive to long periods without oxygen, changes in
temperature and dehydration. He suggests that physiological robusmess may be
particularly common in lentic littoral species whose habitat naturally presents
greatly varying abiotic conditions.
Lotic warer mites may be more sensitive to such extremes. Gemke and
Schwoerbel (1991) state that almost all studies of lotic mites show that thcy
dedine in polluted w. unpolluted sections of screams. But regardless of whetha
mites are 'beteer' than other taxa at identifying stressed water bodies, it is dear
that physical factors play a great role in determining the distribution, abundance
and variety of water mites in a body of water. The temperature, chemical con-
scicution, depth, substrate and water velocity in an aqueous environment affbct
the nature of its hydracarine population.
As well, because water mites depend on a diversity of other organisms fbr
prey, hosts and even oviposition sites, the presence of certain mites may be
used to indicate the presence of t h e other organisms. For example, if
Unionicoia masipes (Unionicolidae) is present, then its oviposition and trans-
fbrmation sites - freshwater sponges - must & be present. Below is an
ACARIUNDERWATER, OR. W H YD I D MITES TAKE T H E PLUNGE?
outline of abiotic and biotic factors that may correlate with the diversiry and
abundance of water mites.
Temperature
As a taxon, water mites have a broad range of thermal tolerance. Active mites can
often be & e n from the firinid waters of icc-bound bka (Pennak 1978; Pmaor,
pus. obs.). Conversely, some species of mites are very tolerant of high tempera-
tures. Young (1969) found 2 spbcies in t h e d springs: ThmMMlu nmathris
and TynrClia eirnrLzriswued u n from water with a temperature of 49. lac,near
the upper level of tolerance for most arthropods (Chapman 1982). It is this abii- 165
icy to live in hot pools that led Philip (1953) to pen this apocalyptic wfiimsy:
rib of
'...in the htilely protective shadow of a protruding bit of
...
a long-since artina whale. in this shimmering shadow in a now bleak
and almost lifeless wodd steaming in the writhing heat of a memless
expanding ball of fire in the heavens and beside the ever boiling cauldron
springs of the North Pole, crouches an anxious, solitary water-mite, the sole
survivor of animal l i upon chis agonized, liquidating planet. There will be
no chronicle of her life cyde, and the validity of her scientific name will be
a matter of great unimportance.'
Depth
Water mites tend to be more common in the littoral zone of lakes and d d o m
venture into deep water. As samples are taken at progressively greater depths.
hydracarinc populations become scanty and diversity deueases (Pennak 1978).
Modlin and Gannon (1973), in a study of Great Lakes water mitts, fbund that
only 4 of 32 species were bund in the pro&ndal zone (21-40 m). Ricradcrall
and G i (1993) found no water mites in w e samples h m lake substrates
deeper than 13 m, whiie from 5-12 m mires made up at most 0.39% of the ben-
thic fiuna. Mites arc also scarce in the pelagic zone of deep water. The plankton
community is usually dominated by comparatively few species from even h t
genera, usually in the famidies Pionidae and Unionicolidae. Modlin and Gannon
(1973) found two species of Piow and one each of Fotrlia, N'mania and
Unwnicola in the plankton of the Great Lakes. Riessen (1982) found three
species of Piona, HuicJkhk mnw and Unwnuola E*PW;OCS in the open water of
Heney Lake, Quebec. In North America Unionirokacnwipu o h dominates the
pelagic zone; Conroy (1974) found that 90% of all plankconic mitts in a British
C o l u m b i lake were U.rr~~lpu.
Moving &m the plankton to the substrate, the phreatic zone may contain
lower numbers of mites but it &rds more variety. Cook (1969) says that 33 of
the 48 fimilics of Hydracarina are known to have at least some representatives
in the ground waters. Only the superkmily Hydrachnoidea goes unrepresented
in the phreatic, possibly because the generally rounded shape of hydracbnoids is
ill suited to life in gravel interstices. I. Smith (pa. w m . ) has collected more
than 20 species of interstirial mites from a single stream site in Alberta. Much of
the subsurfice fauna seems to have evolved from rheophilic ancxston, as the
interstitial waters associated with lakes and ponds are almost completely ladring
in water mites (Cook 1969).
MITES: ECOLOGY.EVOLUTION
AND BEHAVIOUR
Substrate
The majority of water mites remain in dose proximity to some form of sub-
strate, either vegetable or m i n d . It has o h been recnacked that water mites
are rare when there is a lack of mauvphytcs (Pennak 1978. Young 1969, Modlin
& Ganaon 1973). A comprehensive study of biotic and abiotic &tors deter-
mining water mice assemblages in Ppnean mreams showed that the presence
and type of moss in a s a r a m was one of chc most important f e a (Angtlier~
et d 1985). In his study of Colorado water mites, Young (1969) found that 42
of the 48 lakes that yielded no mites were either alpine bkcs or fluauating reser-
voirs. He postulated that repeated exposure of the lake bed or scouring by ice
would d u d e both plants and invertebrate bottom kuna. Hence, he tilt that
the mutual absence of plants and mites was due to harsh environmental condi-
tions rather than any vegetabl&unal i n r e d o n . Rooted aquatic plants are not
essential to a l l wata mites, although H y k h n a requires plant stalks in which to
lay its eggs. Many species happily exist in treeholes and temporary bodies of
water that lack such flora.
Nevertheless, when maaophyns are available, water mites sometimes show
djstina p h c c s b r cemin~pl&rs.Cyr and Downing (1988) observed more
mites on the broad-I& IJot~lopr~ n on Mvriovhllrrm or VaClintcria both
than
of which have finely dissected I&. In c z c c h o s l carp
~ ponds. Puacochar
(1971) h u n d the k t hydracuines in stands of %&a, while three times as
many were collected from Pomnogcwn Young (1969) found rhat both
Potmwgcton and Myriohyllrrm were fivourite plants fbr water mites and bund
hhydracarines near either A!%& or Cbam Even though large populations of
several species were r a l in other parts of a lake, submerged meadows of these
rwo macrophytcs wue o k n devoid of mites, possibly indicating active avoid-
ance. Young did not investigate the cause of this avoidance, which could be
based on a lack of prey or a surfiit of predators.
Mites &o seun to show preferences for certain types of mineral substrates.
Sand or gravel shores of lakes ace genetally poor places to collect water mites
(Modlin & Gannon 1973, Pcnnak 1978). In streams, sand and gravel are pre-
h a d to silty bomms or subsuatcs consisting of large boulders voung 1969,
Freundlieb 1979). Snram velocity seuns to iduenct mite populations through
its & on the substrate. Young (1969) found that the greatest diversity and
abundance of water mites o d at sawm velocities of 0.34.5 mls, when the
saeam bed was mainIy gavel. F m d l i c b (1979) also n o d that rhe sand and
g r a d subsctate of fast-moving streams had the highest densities of hydmchnib.
Standing (lentic) vs. running (lotic) water
In his three-yearstudy of mites in Colorado, Young (1969) compared the lentic
and lodc b. He b u n d three major difkences beonreen these two p u p s .
The most obvious was the brger number of lentic vs. lotic species. Of the 99
species he coUected. 44 occurred in Iotic situations, 66 in lenric, and only 11
species were found in both habitats. Young felt that three things could acmunt
b r this phenomenon. F i i y , environmend conditions in a series of lakcs arc
much mom diverse then the conditions accurring throughout a stream qmxn
and this provides a greater variety of niches for those hrms with proper adapta-
tions. Secondly, the opportunity for speciation to occur is greater in laka and
ponds than in loac situations; the isolation of populations in bodies of still water
I O R , WHYDID MITES TAKE THE PLUNGE?
ACARIUNDERWATER,
results in genetic isolation more frequently than in continuous stream systems.
Finally, it seems likely that lentic situations provide a greater variety of insect
horn and a bemr supply of dadoecran prey. Thii finding that the lotic fauna is
less diverse than the lentic is probably partially an a& of Young's sampling
method He seems to have coUectcd fmr genera of interstitial mites, although
thcse can be very diverse in montane smams.
1
A second major difference between these two bunas was the much higher
between-site frequency of common stream mites. For example, S p d o n g&&-
j &nu (Spuchontidae) was b u n d at 90% of the stream stations, whereas the most
common & species, LimMia nranrlzrcz (Limnesiidac) ocarmd in only 30% of
the lenac habitats. This difference probably reflects the greater ease of dispersal
I
in sacam systems as compared w the passive mode of parasitic d i s p e d that
lentic mites must rely upon.
The third diircnce cited by Young was the high ratio of 'euryzonal' (i.e.
widespread) species to species with rcsuicud altitudinal ranges in thc stream
&ma as compared w thc & fiuna. This l i y results from the more d m
conditions throughout a stream system, permitting even narrowly adapted
species to inhabit a broad altitudinal range.
Acidity
The pH of a body of water may correlate with the diversity of water mites prcs-
ent but there is l i d evidence thac acidiry affecFs mites directly. Pamak (1978)
says that acid lakes contain kw water mites. Bagge and M d e n (1985) bund
, rhat of 30 species of mites prescnt in the estuary of the River Kflnjoki in
Finlands only L i m n o c h ~qsratiea
~~ (Limnocharidac) seemed able to survive
highly acidic river waters. Eriksson tt A (1980) bund that in acidic lakes where
fish were absent, water mites were absent as well; however, they felt that this was
, due, not to the acidity, but to the lack of fish which would otherwise eat the
I insect predators of hydracarines. In a laboratory study, Rousch ct d (1997)
; b u n d that survivorship of Amnurus manubrkmr (Armuridae) was una&cted
by acidity until it to pH 3 or lower - a Level unlikely to be encountered in
most nacuraf water bodies. Mites were entirely unaffixted by high iron l m l s
(added to simulate acidic mine runom. In Colorado, several species of water
mites seem Limited to non-alkaline waters but only a very few species of
Anmvrus show a prcf;erencc for high alkalinity (Young 1969). However, it is
hard to determine if these prdcrences arc physiologically those of h e mite or
those of the mite's hosa or prey.
Organic pollution
'' Organic pollution may virtually diminate the water mite fiuna of a stream. In
Young's (1969) study of Colorado mites, he found that very few spscies inhab-
I
ited water even 8 miles below the o u a l of sewage from a Boulder treatment
, plant. Ge& and Schwocrbcl (1991) campre water mite assetnbhgc~from
the upper Danube in 1959 with those present in 1984. They bund that in zones
where pollution from domestic sewage had i n d , species richness had
d d drastically,whereas in arcas where purification plants had impmved
'
water quality compared to 1959, species richness had increased H p b m f i -
uirrtiflis(Hygrobatidac) emerged as an indicator of pollution, as its dominance of
rhe water mite assemblages increased with increasing pollution. At the most
MITES: ECOLOGY,EVOLUTIONAND B E H A V I O U R

polluted sites it made up more than 90% of all individuals. In studies of streams
in central Italy, Cicolani and Di Sabatino (1991) observed that diversity of water
mites declined with decreasing water quality. Like Gerecke and Schwoerbel
(19911, their study indicates that H. fiviatiiis is extremely tolerant of organic
pollutants. It is also interesting to note that Bagge and Merikinen (1985) found
that of 30 species of mites present in a river estuary, H. J7uviatilisand H. longi-
palpis were the only ones to have their highest densities in the saltiest reach of
the estuary. This suggests that H.fluviatiIis, and perhaps other congeners, are
exceptionally resimnt to environmental extremes and may be good indicators of

With the exception of these and a handful of other European studies, there
is essentially no work on the effects of man-made disturbances on water mite
assemblages. This is mainly due to the tendency of freshwater ecologists either
not to report the collection of mites at all, to lump them as 'mites' without fur-
ther taxonomic resolution or to place them with nematodes and oligochaetes in
the extremely uninformative group 'other'. D o water mites provide information
on water quality that other organisms do not? Do they intensify a signal given
by other macroinvenebrates, or run counter to it? T h e species richness, abun-
dance, demonstrated sensitiviry to organic pollution and salinity and potential
as holistic representatives of benthic communities are strong reasons for the
inclusion of water mites in biological assessments of aquatic systems.

SUMMARY
In contrast to other arachnids, mites have invaded aquatic systems at least ten
times, with some lineages giving rise to thousands of water-dwelling species.
Every possible rype of aquatic habitat contains mites, from temporary puddles
on rocky outcrops to the stygean permanency of marine rifts. Some acariform
lineages, parricularly the Hydracarina and Halacaroidea, have radiated into
many different aquatic habitats. This switch to an aquatic lifestyle was made
more feasible by the respiratory systems and 'waterproof feeding methods of
these lineages' ancestors (and probably explains why parasitiformans have not
been successfd in water). Aquatic oribatids, astigmatans and water mites have
not altered their diet drastically from that of their terresuial relatives but halac-
aroids have been more adventurous in adopting vegetarian and parasitic habits.
Some water mites share top predator rank with venebrates in freshwater systems
because they are almost immune to predation by fish Although they are likely
to be useful as indicators of organic pollution, salinity and general ecosystem
'health', water mites have very rarely been included in freshwater assessment
studies.

ondering imponderables can stimulate scientists much as red flags are
alleged to a f k bulls. A good example of this phenomenon is the current
controversy over the number of living species.Terry Erwin's estimate of 30
million living species has elicited much snorting, pawing and charging of
bioestinlators. Acatologists have mostly taken a ringside seat at this display
because the flags have been flying f h m the canopies of tropical minbrcsts and fkw
mites were thought to be arboreal. Rather, rhe cmacs of mite diversity have long
been known to be in the soil and in symbiotic association with animals. Even with-
out a mite component, however, dsuggess that rainhest canopies arc filled
with a previously uhmgined diversity of arthropods, especially insects, and in
particular, beetles.
- of mices to form hssils. However, when co&rous trres with &dry sap
Although the C ~ t omay r have had a particular fbndness fbr beetles, he also
&cted chun with quite a few mites, many of them parasites (see Chapter 9).
Nor were other arboreal animals or plants spared. Because of their economic
importance, mites parasitic on crop plants have long k n known (eg. Jeppson
ct al 1975, HeUe & Sabelis 1985, Lindquist et aL 1996). Almost any orchard or
field crop is Likely to be infested with spider mires, fslse spider mites, erinose
mites, rust mites, e a d mites or any of a host of other pests -and this is true
of rainhest plants as well. More surprisingly,mcnt studies in native forests and
plantations throughout the world have demonstrated that trees are aswarm with
fi-ee-living mites (e.g. h k i 1973, Hijii 1986, Costa & Crossley 1991, Willson
1991, Coy et aL 1993, Etching ct aL 1993, Walter ct aL 1994, Wdter &
O'Dowd 1995a, b, Wdter & Proctor 1998b Recher a aL 1996, Guilbert 1997,
Watanabe 1997, W~nchester1997, Watanabe 1997, Walter & Behan-Pelletier
1999). In fict, a 6ne patina of acarines adds its lustrt to the outermost layer of
fbrests and a cornucopia of Acari thrive between the outer canopy and the
&rest floor.
MITES ON PLANTS - WHERE DO THEY COME
FROM?
The sufkce and interstices of soil, and the decaying vegetation that accumulates
in this matrix, are the a n d homes of mites and still contain the most impres-
sive acarofiunas (see Chapter 6). Except in the driest or most fiozen of soils,
mite densities in the tens to hundreds of thousands per square metre are com-
monly reported (Petersen 1982), and a handrl of &rest humus ofien contains
dozens of species of mites. This detritus-based diversicy is known to extend into
the canopy in the suspended soils that collect in d o l e s , crutches and among
the leaves of epiphytes (Nadkami & Lnngino 1990, Paolcui ct aL 1991).
Although some sol mites wander up tree trunks and colonise these patches of
hanging humus, most of the mite spacies hund on tme trunks, branches and
leaves are truly arboreal and only descend to the hrtst floor through mischance
(Walter & Behan-Pelletier 1999). Patterns at the M y and generic levels indi-
cate that relatively fkw lineages have made the transition to living on the d c e
of plants but some of these have undergone speccaaJar radiations.
In the rich Bdtic amber h ssils of the mid-Terdarg,many of today's charac-
teristically arboreal mite taxa can be kund. However, these fbssil assemblages do
not mirror the common view of arboreal.mitesderived from agricultural ecasys-
tcms. Relatively fiw are predators (e.g. J+y&AErythraeidae, Anystidac, Cheyletidae,
Phytoseiidae, and Digamasellidae) or herbivores (e.g. Eriophyidae,
Tecranychidae) (Selden 1993, Labandeira ct aL 1997). Instead, most mites in
amber have living datives that fked on firngi, scavenge dead plant matter or graze
on algae and lichens growing on plants the grazers, browsers and piercinpuck-
ing microbivore functional p u p s so common in soil (see Chapter 6). The line-
ages in canopy habitats, however, axe taxonomically distinct fiom those fbund on
the hrtst floor (Walter ct al 1994, Water & Behan-Pelletier 1993, 1999).
One of the most characteristic fsmilies of modern bliar oribatid mites is the
Cymbaeremaeidae. At least one species in this Emily, Jajnrmur16ycoLrrus, is
known fiom h ssils in the late Jurassic. Other characteristically arboreal oribatid
W e s , such as Catniiidae, Oribanrlidae and Platerernaeidae,are known &om
Crttaceous hssils.AU of these are armoured mites, perhaps the most likely kind
appeared, even sofi-bodied mites could be preserwd as fbssils in amber. For
example, tydeid mites are ubiquitous on modem plants and one &Ml tydeid has
been hund in Cretaceous amber (Selden 1993). Many other arboreal mites
trapped in amber (Zacharda & Krivolutslsy 1985, Krivolutsky & Druk 1986,
Selden 1993) are known Erom the Cretaceous.
In agriculture systems that rely on chemical control of insect and fungal
pests, outbreak of plant-parasiac mites are common and f;cw mites. in oothu
firnctional p u p s survive. But in modem mesic to humid &rest canopies,
although plant-parasitic mites are diverse, their populations tend to be restrict-
ed in time and space. For example, Australian rainfbrest canopies ofien have
densities of 1000 to 10 000 mites per metre of leaf area - populations that
might temfy an orchardist -but tbe vast majority of these mites are fun%ivores,
especially sarcoptifbrmans and prostigmatans (Water 8c O'Dowd 1995a).
Free-living sarcopciform mites with pincer-like chelicerae f k d on fungal
hyphae, algal strands and dead leaf or woody material. Except fbr pollen (usually
windblown), sarcoptibrm mites rarely ked on the living tissue of green plants,
probably because chelatedentate mouthparts are not usem b r puncturing the
epidermis of plants. It is mites with needle-& movable cheliceral digits that gave
rise to mites parasitic on higher plants (Kranu & Lidquist 1979, Lindquist
1998). Obtaining the leverage to krcc cheliceral stylets through the epidermis of
a leafwas probably the main problem that these mites had to overcome. Most of
these minute herbivores stab individual plant cells and suck out their contents,
providing a ready source of moist^^^ and allowing them to avoid localised plant
chemical d&cts (eg. fkcding around vacuoles). Plant parasitism has evolved
rtpeatdy in d.if?knt lineages of mites so that today most species of conif;ers,
monocots and dicots, and many &ms,are attacked by one or more species of mite
(Jeppson ad 1995, Helle & Sabelis 1985, Lindquist ct aL 1996).
PLANT PARASITES
Mites parasitic on the leaves of vascular plants belong to che order A c d r r n e s
and primarily to the suborder Prostipara. As in all Prostipam, plant-parasites
f'red only on fluids: modified stylet-like mouthparts are used to puncture indi-
vidual host cells and drain their contents (Lindquist 1998). Phytophagy has aris-
en within at least seven dades of Proscigmaca, including w o major radiations of
obligate plant parasites (Eriophyoidea and Tetranychoidea) and several Less m-
lutionarily successful experiments within other lineages (Erythraeidac,
Eupodoidea, Stigmaeidae, Tydeidae and Tarsonemidae). Tarsonemid mites arc
 MITES: ECOLOGY.EVOLUTIONA N D BEHAVIOUR
especially interesting example because at least four independent evolutions of
plant-parasitism from mycophagous an-tors seem to have occumd (Lindquist
1986, 1998).
Rust, gall and erinose mites
Most of the more rhan 5000 described species of plant-parasitic mites belong to
the rhrec families of the Eriophyoidm: Phycoptidae, Diptilomiopidae and
Eriophyidae. The association between eriovhvoid mites and vascular ~lants
app- to be an ancient one (Lindquist 1596), which may help expl& the
172 extreme diversity of this group. About 2900 species of gall and rust mites are
described but three-fourths of these are from temperate regions. Arnrine &
Stasny (1994) estimate that this is less than one-fihh of the temperate fauna and
that perhaps only one-twendeth of the tropical fauna has been described. All of
these mites arc tiny, most less than 200 pm in length, all post-egg scages (larva?
nymph, adult) have worm-like bodies with only two pairs of legs and all are par-
asites of plants. Most woody dicots, and many herbaceous dicots, monocots,
conifers, and ferns, are atracked by eriophyoids (Amrine & Stasny 1994,
Lindquist et d 1996) and the vast majoricy of these mites are host-specific
(Oldfield 1996). Hosts arc located by aerial migration (Zhao & Amrine 1997).
The mouthparts of eriophyoid mites are complex and have not been com-
pletely homologised with those of other prostigmatans. The stylets (7-9 in num-
ber) are encased in a U-shaped channel of the subcapitulum but do not form a
W i n g tube (Lindquist 199Ga). Two methods of attachment to the leaf surfice
during feeding are known. Most eriophyoids have the apices of the palp tarsi
modified into a suction pad that allows them to anchor their mouthparts to the
leaf epidermis. The muscles of the pdps then contract and fbrcc the stylets into
the epidermal cell of the h o s ~ In these mites, the paps usually telesoope during
penetration (Nuzzaci & Alberd 1996). In contrast, citrus russet mites anchor
themselves to the leaf with anal suckers, arch the body and force the srylns into
epidermal &;palps are reffexed away from the plant surface. Stylets are short
(20 urn or less), penetrate only about 2-7 pm into host tissue and therdore
mites fked only on epidermal cells. No feeding rube is brmed by the stylets and
thcy appear to be withdrawn befbre cell fluids are sucked out (Wgtphall &
Manson 1996. Oldfield 1996).
Gall, erinose, blister, witches'-broom and big bud mites cause galling and
deformation of leaves, petioles, stems, buds, flowers and fruia (Keiir rt d
1982). Only plant roots appear to be safe from attack Perhaps the most unusu-
al of these cancer-lii growths arc rhe felt-like pelts of hair-like pnwxsses called
ecinea (because they ofien nun a bright red to rusty colour). Mites live among
the hairs and appear to fcad on them (Westphall & Manson 1996). Predators
can be seen wandering over the surface of erinea and probing for mites but the
erinosc mites appear to be w d protected by the growth of hairs. Finding mites
in erinea is no easy task either (especially since erinea persist afier the mites have
gone), making diagnosis difficult for a non-specialist. However, if a leaf with a
fresh erineum is picked and placed under a light, hordes of tiny erinose mites
will come scrambling to the surface as the leaf dries.
Mites arc easier to find in discrete galls (variously d l e d bladder, finger, nail
and galls) and other swollen tissues that can be cut open, often to dis-
dose hundreds of tiny worm-like mites. The exaa mechanism causing the
galling response is not well understood but appears to result from the rdcasc of
some component that the mite introduces (or induces) during teeding. The
three glands (an unpaired median &d and a pair of lateral glands) that unpty
into the feeding tube are a likely source of this component (Nuaaci & Albem
199G). The cell initially punctured by a gall mite dies but surrounding cells
begin to proliferate to hrm the protective gall, while differentiation of nutritive
cells also occurs (Westphd & Manson 1996). Considering the economic impor-
tance of these mites and their diversity and commonness, understanding the
galling process should be considered &imporrant area of futurc research. Since
about a dozen eriophyid mites arc known to vector vlant viruses or Lirus-like dis-
eases (Oldfield &-~r&eler 1989). the hypothesis-that microbid associates are 173
involved in gall production merits consideration.
The ability to gall plant tissue has evolved several times in acarifbrm mites
(e.g. some Tenuipalpidae and Tarsonemidae cause @-like growths) but it is
most strongly developed within the Eriophyoidea However, mom than half of
all known eriophyoid species do not live within deformed plant tissues (Amrine
& Seasny 1994). These mites are called rust mites, nrsset mites or leaf vagrants.
Some species arc brightly coloured in orange or purple, some are covered with
waxy plumes, and a few spin small silken webs (Manson & Gerson 1996). Rust
mites wander the leaf s h c e puncturing cells and causing a silvery to rust-
coloured damage (Keifer et d 1982). Like all eriophyoid mites that have been
studied, these mites arc b i d and arrhenotokous; the haploid males produce
scaked spcrmatophores (see Chapter 5). Current evidence suggests that erio-
phyoid mites are closely related to tydeid mites (Lindquist et d 1996) and pre-
sumably plant feeding evolved from scavenging or hgus-feeding leaf vagrants
that were oppommistic leaf cell feeders (as some modem tydeid mites are
thought to be). This switch to obligate plant parasitism may have occurred in
the Palaeozoic The most primitive known eriophyoid mite, P m arau- ~ ~
a&, fbrms galls on the needles of a Chilean species of Araucariaceac, a family
that originated in the Permian period more than 250 million years ago ( B o d
& Shevchenko 1996).
Earth mites
In contrast lant paasitism appears to have arisen more recently withii a group
*9
of soil-inhab~tinghgivores in the Eupodoidea (Qin & Halliday 1997). Earth
mites (Penthaleidae) are relatively large, long-legged and soft-bodied mites that
are usually found on low-growing herbs or in the soil under them. Generally
their integument is orange to red but this colouration is obscured by the black,
--
blue-black or dark green internal colouration of the body- Since the dark pig-
ment is absent or reduced in the legs, these ofien appear ;ed.
One of the best known penthaleid mites is a major agricultural pest in the
Southern Hemisphere: the red-legged eatth mite (aka black sand mite)
h%&&us dcrmrrtor. Annual broad-leaved plants and grasses are attacked, usu-
ally on the upper &ce of the leaf, and large populations can cause extensive
damage to pastures in the cool seasons in Mediterranean climates (Ridsdill-
Smith 1997). When fkding on the leaves of higher plants, earch mites brace
their bodies by gripping the leaf s d c e with thdr tarsal claws and then punc-
ture and flatten the convex surfice of leaf epithelial cells during feeding.
The needle-like movable digits in thcse mites are 9-20 pm in length and thii
appears to determine the depth to which thcy are able to feed (Ridsdill-Smith
et at! 1996).
 MITES:
ECOLOGY,EVOLUTIONA N D BEHAVIOUR
Red-legged earth mites reproduce sexually and both sexes are diploid (Weeks
et aL 1995). Sperrnatophora are a simple silken web on which dmps of sperm
arc deposited by males, even when females are not present (Ann& 1995). Eggs
are laid individually on plants during the cooler months but at the beginning of
summer adult femalesdie with their bodies full of diapausing eggs. These cadav-
erous egg sacs may be blown on the wind and disperse the mite ow long dis-
mar. Immature stages (Lmand three nymphs) appear to be less likely to be
found on plants and the lik q d e may be completed on mosses, f i q i and algae
-
growing on the soil s h c e (Ridsdill-Smith 1997L
- -.
174 Th; blue oat mite, P&&& nujot, is another important pasture pest.
Unlike the red-legged earth mite, the blue oat mite &eds upsidedown on the
underside of leaves. Conveniently, this mite has its anal openine on its back h r -
rounded by an orange spot id live spedmens). ~lso'conv&ent for lohdy
females, the blue oat mite has done away with males and reproduces by M y -
mkous parthenogenesis (Wacks et rrl 1995). The blue oat mite is active during
the autumn and winter and passes the warmer months as aestivating eggs glued
m plant sums (T'ashiro 1987). Although the blue oat mite has a greenish tinge
m the adult integument, it is not blue a n d perhaps, winter grain mire is a bet-
ter common name.
-ThePenthaeidae as presendy defined may be diphyletic and herbivoy may
have arisen twice: once in an ancestor of U a l b t y h and once in an ancestor of
P m d k a n d its relatives (Qin & Halliday 1997). However, interpreting these
transitions is complicated by several other related families of poorly known
mites, the Penthlodidae and Eriorhynchidae. Pentholodid mites are oficn a
bright yellow in colour, strongly ornamented and well armoured. Two genera are
rrcognised: Pcnrhdlily with a boreal distribution and Stclrotyah fiom a d Yamamura 1987, Saito 1997).
regions (Qin 1994). Species of the latter arc common in mosses and lichens in
the Southern Hemisphere, including Antarctica (see Chapter 6). E r i o r ~ h u is z
the only known genus in the recently described Eriorhynchidae (Qin & Halliday
1997). Five species are currently known and all are large, hairy, rapidly moving
mites with v y r long legs. Leg span from the tips of the antennikrm fmnt legs
to the daws of the hind legs are typically 6-7 mm in adult females. E r i o ~ h u s
w&can be found in m o w , leaf litter and in canopy knockdown samples in
rainfbrests in Queensland.
Spider mites, false spider mites and ornate false spider
mites
The Tetranychoidea is composed of five fimilies united by having an eversible
styiophore fbrmed fiom the b e d cheliceral bases and a 10% tecurved, hollow
stylet fbrmcd fiom the movable digits (Hislop & Jeppson 1976). All known
Tetranychoidea are parasices of vascular plants. Because of the damagc c a d to
economicdy important plants, the spider mites (Tetranychidae) are the best
studied. Although only one species has been demonsulud to vector a p l a t virus
(Robertson & Carroll 1988), spider mite fosditg is o h extremely dam-
and can result in death, especially in herbaceous hosts. Spider mites stab in&-
vidual plant &with their mouthparts and suck out the contents. This can lead
to necrosis of leaftissueand leafdrop. Generation times are usually short (10-14
days) and populations rapidly reach damaging levels. Spider mites migrate on
the wind and readily colonise new plants. Many respond to chemical miticides
by migrating, thereby expanding the area under attack. Additionally, spider
mites rapidly evolve resistance to chemicals, perhaps because hvourable mum-
tions become tixed rapidly in haploid males (Crozier 1985). Bebre World War
I& spider mitts were only rarely pests; however, since the use of synthetic insec-
acides and fbgicides became common, spider mites have become major causes
of economic loss.
Spider mites get their common name fiom the silken webbing produced by
some species in the s u b m y Teuanychii however, many of these mites use
silk only t6 protect their eggs and those in the subEmily Bryobiinae do not pro-
duce silk at all (Gutiemz & H d e 1985, Gerson 1985). Master-dass weavers
occur only within che tribe Tetranychini and many of these mites have developed
a subsocial type of colony. For example, species of Schiwtmanychus and some
sped& of Olpttychus (eg. 0. pmem) produce densely woven sheets of s i b
clothhnder which f$milies of mites fkd in relative security. These web nests
(Saito 1985) are as tightly woven as any spider egg case and provide a r d e n t
proteaion against desiccation and predators. As the nests are constructed, small
openings arc lefi and males oftcn guard these entrances and ward off predators
and competitors (Aponte & McMuruy 1997). Immature predators, especially
h e , that attempt to enter nests of a species of Schiwtcmrrych~uon bamboo
are anadced and oficn killed by thrusts of the chelicerac. Male and &male spi-
der mites appear to cooperate in defence, with k d e s finding and pursuing the
predator and males catching and killing them (Saito 1986% b). As in the
Hymenoptera, spider mites are arrhenotokous and species like S. celariw live in
colonies, o h fbunded by a single female, that develop into complex webs com-
posed of many overlapping generations. These mites appear to have reached a
level of subsocial organisation unknown in any other mites (Saito 1987,
Species of Tchvutych produce the largest and most complex spider mite
webs and they ofien form dense entanglements of many layers. Some species,
such as the two-spotted spider mite, Tcttrrnychrrr urticac, are polyphagous pests
that can devastate many crops. The two-spotted mite holds the record, at over
900 species of known hosts (Navajas 1998). However, of the approximately
1200 described species in 70 genera (Bolland et aL 1998), only a fkw dozen spi-
der mites are major agricultural pests that regularly debliate and kill plants
(Jeppson et aL 1975, H d e & Sabelis 1985 a, b). Unlike many agriculturally
important species, most tetranychids appear to have r e s t r i d host ranges
(Jeppson et aL 1975, Hill & Stone 1985). Most host specialists do not attack
economidy important crops and arc poorly studied, that the true
diversity of the Tefl;mychidae is undoubtedly considerably hlgher than 1200
species (see Chapter 10).
The probable sister p u p of the Tetranychidae is a dade composed of the
remaining hur fbilies of Tevanychoidea (Liidquist 1985). The Tenuipalpidae
or m e spider mites are best known, again because of a few economically impor-
tant polyphap (Jcppson rr aL 1975. Mcyer 1979). Most tenuipalpid species,
howcvu, seem to be host specific. More than 600 species have been described in
22 genera (Mcycr 1979, Evans et aL 1993) and, given the diversity of unde-
scribed fbrms in Ausualii, this must be a minor component of the aue diversi-
ty of the group.
The remaining three h i l i e s of tetranychoid mites, Tuckerellidae,
Linotetranidae and Allochaetophoridae, are rarely important agriculturally and
account fbr less than 30 described species in five genera (Meyer & Ueckermann
 1 997). 1-inotetranid mites (Limoretrrrwus, Afiolinonu, and Anopfopalpru) are asso-
ciated with soil collected among grasses and are unique among the tetranychoids
in completely lacking eyes. Possibly they feed on grass roots or within the crown
of grasses. Until recently allochaeropl~orid mites, or rather the one known
nymph of Allochaerophora, was one of the great mysteries of acarology. The fnm-
ily was proposed in 1959 to accommodate one aberrant tctranychoid nymph
from grass in California and for nearly 40 years that was the only known rcpre-
176
sentative of the family. A Full developmental sequence of a second species from
Africa (also associated with grasses) has now been described (Meycr &
Ueckermann 1997).
Tuckerellid mites (Tuckerella) are perhaps the least derived of the
Tetranychoidea and they are certainly arc the most ornate of the spider mites
(Figure 8.1). A peacock tail of plumose posterior setac trails out behind an idio-
soma protected by ornate dorsal shields covered with large, leaf-like setae.
Described species of 7ilckerella fall into two species groups chat segregate
Figure 8.1
An early derivative
member of zhe
Tetranychoidea
(Pmstigmae),the
plant-parasitic
Tuckerella sp.
(Tuckerellidae).
ecologically. One group is found in association with grasses (perhaps feeding on
roots) and the other on stems and fruits. Some species of the latter group are
sometimes pests of citrus (Ochoa & Vargas 1994). These mites seemingly retain
the tritonymphal stage (Quiros-Gonzala & Baker 1984), although trito-
nymphs are suppressed in all other Tetranychoidea and in the closely related
Cheyletoidea and Raphignathoidea (Lindquisc 1998). Paedogencsis has been
- - of Tuckerella knorri (Ochoa 1989).
reported in tritonymphs
Unlike other groups of plant-parasitic prostigmatans, the Tecranychoidea
appear to have evolved phytophagy from a predaceous ancestor in the
Cheyletoidca or Raphignathoidea. Basal cheyletid mites are predators and
derived wxa account for one of the most impressive radiations of parasites of
I
177
insects and vertebrates (Krann 1978, Evans 1992). No cheyletid mites feed on
plants but a number of predatory Cheyletidae are arboreal and perhaps some
ancestor of these mites first began feeding on plant cells. Most raphignathoid
mites are also thought to be predators, including the Stigmaeidae, a well-known
group of biocontrol agents in agriculrural systems. Howcver, at least one genus
of stigmaeid mites, Eurtigmaeur (known as k&rmuel&ria in the older literature),
is plant parasitic, although o n mosses rather than vascular plants (Gerson 1972).
The biologies of species in most families of Raphignathoidea are very poor-
ly known. The Homocaligidae is associated with subaquatic to aquatic plants
and an herbivorous relationship with these plants should at least be considered
a possibility. Also, members of perhaps the most obscure family of the
Raphignathoidea, the Cryptognathidae, have a number of derived characters
(e.g. the ability to withdraw the gnathosoma through a collar-like extension into
the idiosoma) that may indicate a close relationship to the Tetranychoidca. The
feeding biology of cryprognathid mites is not known.
Duckweeed and water hyacinth mites
Outside of the Prostigmata, reports of mites feeding on the leaves of living plants
arc rare and mostly caused by misidentif cations or by facultative leaf feeding by
predators (Porres et aL 1375) or by the depredation of omnivores on seedlings
(Walter et RL 1986). However, some species of oribatid mites seem to have made
the transition from feeding on fungi and dead leavcs to attacking living aquatic
plants. For example, adult Hydozetes (Hydrozetidae) are commonly associared
with duckweed (Lonma spp.) and immature stages burrow within the small,
floating thallus of the plant. Immature stages of another oribacid mite,
Orthogalumna terebrantis, burrow in aquatic plants in the Pontederiaceae,
including the noxious weed, water hyacinth, Eichhomia rrassipes. The eggs are
laid on pseudolaminae (= leaf-like structures) and the immature mites excavate
tunnels in 'leaves'. The mite tunnels become infection portals for a leaf spot fun-
gy, Acremonircm zunatum, that is vectored by the mite. Mite activity stimulates
ov~positionby the weevil Neochitina eichhornicre, causing better control in areas
where the mite is present (Crornroy 1983).
Roming fruit that has dropped beneath a plant can be colonised by soil-inhabit-
ing mites and those phoretic on the flies and beetles attracted to the decaying
fruit. Fruit that are damaged but retained on the plant may acquire a similar
acarofauna and fruit with mildews or ocher Fungal growths may support large
populations of Fungivores and scavengers chat have moved out from the leaves
 I MITES:
ECOLOGY,EVOLUTION
A N D BEHAWOUR
and wigs. Intact fruit may be attacked by species of Tenuipalpidae,
Tudcerellidae, Tksonemidae or Eriophyidae (e.g. citrus rust mites), each of
which may cause characteristicdamage (Jeppson ct al 1975).
One spedaliaad fruit, the fig, has its own specialised p u p of fhgivorous
mites. F i g are complex inflorescences composed of many small unisexual flow-
ers which arc surrounded by a fleshy covering. Within a green fig is a cenml cav-
ity carpeted by the stigmas of h a l e s flowers, each connected to an o d e by a
style of w i o & lengths. Each of the M e flowers can develop into a seed -or
a fig wasp (Hymenopten: Chdcidoidcl: Agaonidae). Entrance to the fig is
178 through the 'eye' or ostiole, an opening that is usually tightly packed with d e s
that rip the wings fmm a W e fig wasp asshe worms her way through the osti-
ole. Once in the central cavity, the W e wasp spreads pollen a m s s the carpet
of stigmas (assuring development of the fig seeds) and probes sryles with her
ovipositor, laying in those ovules she can reach (Janzen 1979). As figs ripen,
wingless male wasps emerge fiom seeds first and mate with funale wasps, ohcn
stilI within their natal seeds.-Female wasps emerge, actively gather pollen that is
carried in spacialised fblds, pockets or groups of hairs, or in the gut and then exit
the fig to search for another developing fig of the same species. Ow 900 species
of figs are known and each is believed to have a host-specific pollinator.
Small tydcid and tarsonernid mites that scavenge or f e d as fungivores can
make their way into a fig through the ostiole; however, one tribe of tarsonanid
mites appears to have a much more specific association with fig.Three genera
of Tvsonemellini are currently known with species that feed on fig ovules. The
mites are phorrac on fig wasps and a high diversity of host-specific mites appears
to be present (Lindquist 1998, Ho 1994, Compton 1993). Although this asso-
ciation has only recently been discovered, it appears to represent yet another
independent evolution of phytophagy among the Tarsonernidae - one poten-
tially represented by many hundreds of species in tropical brests.
Venereal diseases of plants
Although we find many flowers attractive to our sight and nose, only the most
unnatural of commercial varieties produce their flowers solely for our benefit.
As Linnaeus was fbnd of pointing out (to the discomfort of many of his col-
leagues), flowers are the genitalia of plants. Flowers produce female (ovules)
andlor male (pollen) gametes, and in angiosperms and cycads copulation and
fedisation usually occurs as a result of the visit of an animal (the pollinator).
Therefore, parasites that move from flower to flower on pollinators and inkct
the plant reproductive system are analogous to venereal transmission of diseases
in animals.
At least five, and possibly as many as ten, lineages of mesostigmatans have
evolved a specialised life styie that has been appropriately described as a venere-
al disease of plants; they ride pollinators fiom flower to flower, i d s t flowers and
consume significant amounts of nectar and polfen (Colwelf1995,Paciorek aaL
1995). In the neouopics, all species of Rhinosdw and Tmpicoscius, and lineages
of R-octoI;zckzps and tasiosnirr, live within the flowers of a variety of shrubs and
trees and use hummingbirds for phoretic transport between plants (Dobkin
1985, Naeem c t 4 1985, Colwell1986, Hcynernan etaL 1991, OConnor ctaL
1991, Ohmer ct al: 1991, Colwell & Naeem 1994, Paciorek ct all 1995,
OConnor et all 1997, Nasktecki & Colwell1998). A quick dash down the hum-
mingbird's bill is necessary'for prompt disembarkation and the decision to exit
is probably mediated by the olfactory infbrmation in the stream of air generat-
ed by the birds as they breathe (100-300 breaths per minute). The
Rhinoseize~mpicosn'uzline& appears to have arisen in the montane neotropio
and to have diverged in association with di&rent findies of plant hosts
(Naskrcdci & Colwell 1998).
H u m m i n g b i r d - d a d mites are the best studied flower-inhabiting
mesostigmatans but others hitch rides on many insects. For example, flower-
inhabi&g species of hc~okzeLpsand other &d mites (sometim& mistaken
and misspelt as 'orobatids') arc commonly found on b u t t d e s and moths (Treat
1975, Janzen 1983, Boggs & Gilbert 1987). Species of R.octdkzelaps also are
fbund in flowers in South Afiica (Rykc 1964) and Western Australia (Domrow
1979), and it is probable that the flower habitat has been colonised independ-
ently several times. Mites in the ascid genus JLznthippcapparently feed on pollen
or nectar in inflorescences of a palm and may be phoretic on nitidulid beetles
that pollinate the palm (Naskredci &, Colwell 1995).
In Africa, Australasia and Asia ameroseiid mites in the genera
Neoc~pholackzpsand AFocVpholaclapslive in flowers, fkd on pollen and nectar,
and primarily use bees and buttedies fbr phoretic transport (Evans 1963, Baker
& Dffiado-Baker 1985, Eidcwort 1994, Seeman & Walter 1995, Halliday
1996). Additionally, an Australian system analogous to the neompical hum-
mingbird-flower mitcs has evolved between species of the ameroseiid genus
Hat- and birds that visit flowers. The mites k d on pollen and nectar in the
flowers of mangroves, mistletots and fbrest trees and shrubs, and use hon-
eyeaters, spinebii and probably lorikeets, to move h r n plant to plant
(Domrow 1979, Seeman 1996, Halliday 1997). Flower-mite systems are prima-
rily tropical to subtropical and kw species are known fiom the temperate zones.
No flower-specific oribatid mites are known, though species of Scheloribatidae,
Haplozecidae and MochlozetiQe have been collected fiom flowers (Aoki 1992,
Seeman & Walter 1995).
HUNTING ON LEAVES
A forest may seem a climatically benign and protected habitat to large mammals
such as ourselves but the phylloplaue (surf& of a leaf) in a forest canopy is
regularly exposed to intense sunlight, driving winds and pouring rain. This is a
hostile environment to an animal as small as a mite and thii must be especially
true fbr predators that cannot obtain water and nutrition directly fiom the plant.
This probably explains why relatively fiw lineages of predatory mites have
colonised the phyiloplane. Some of those lineages, however, have undergone
spectacular radiations.
Predatory Prostigmata
Few plants in any garden or fbrest arc without f~e-livingprostigmatans and this
is true fbr one h i l y in particular, the Tydeidae. In Greek mythology, Tydeus
,
I
was a murderer on the run who became one of the heroic Seven Against Thebes.
Among arboreal Acati, species of ?j&us and other tydeid mites are one of the
I
spectacular success stories, ailthough their biology is still mostly a mystery. Algae,
, h g i and pollen are known sources of fbod for tydeid mites but at least some
I speck are ficultative predators (Andre 1986, Walter & O'Dowd 1995) and oth-
I ers can be important biocontrol agents of plant-parasitic mites (Hessein &
I

Perring 1976). Similarly, mosr foliar Tarsoncmidae arc fuogivorcs or algivorcs
bur a few spccies are predators of criophyoid mircs or rile eggs of various planr
mites (Lindquisr 1986).
Tydcid and rarsoncmid mires are small, active mites that come in a variety
of pde, beige or greenish shades; however, mosr predarory prostigmatans on the
phylloplane are yellowish orange to bright red in colour, possibly because che
carorenoid pigments char cause these hues prorect from ulrraviolet lighr.
Commonly encountered families include the Adamystidae. Anystidae,
Bdellidae, Cheylctidae, Cunaxidae, Eryrhaeidae and Stigmacidae. As in soil-lit-
rer systems (see Chaprer 6), some are ambush predators and many are cruise
prcdarors (Figure 8.2).
Cheyletid mites are ambush predators and can often be found at the junc-
ture of thc petiole and rhe leaf blade, lying in wair for small arthropods moving
along the stem-periole highways that connecr one leaf to another. Species of
Rubroxiw (Cunaxidac, Cunaxinae) are also ambush ~redatorsbut they tend ro
take up their positions well out on the leaf blade. As wirh related genera in soils,
Rubrmcirvs have snout-like mourhparts and carw rheir .D ~.D reflexed
S over their
bodies when hunting. The palps are thrown
forward to snap-trap prey againzt the snour.
Even relatively large, acrivr prey such as
thrips can bc capcured using these tactics.
Generally, ambush predarors require active
prey bur Australian species of Rubrorcinrr also
are able ro feed on drops of honeydew and ir
is possible rhac they may feed on inactive prey
such as scale insecrs or eggs as well.
Mort prcdarory pr&rigmatans acrively
seek out prey on rhc phylloplane, alrbough
rheir pace varies from a consranr and deliber-
are searching of every nook and cranny ro rhe
dizzy, spiralling dash across rhe leafcharacter-
istic of anysrid mirm. These 'whirligig' mites
are general predators char overrun mires and
small insects, scab rhem with their m o u t h
parts and seemingly paralyse them with a
toxin (Sorenren cr aL 1976). Whirligig mites
occasionally get carried away with themelves
and scramble onto people, where they are
capable of administering a nasty bite. Like d l
prosrigmarans, whirligig mites feed only on
the fluids of rheir prey but, unlike ambush
prcdarors, rhey tnkc a variety of acrive and
sessile prey.
Many cruise predators are able to search
our and feed on d ~ eggs
e of luge insects. For
example, in rhc Brisbane region, a large
(4 mm body, 1 cm leg span) red velver mite
in the gcnus Cl~rlrronia(Erythraeidae) fccds
on thc eggs of rhc Richmond birdwing
(Troi&s richmundia), one of Australia's largest
M I T E SO N P ~ u N ' r s
-
butrerflies. Thc cffects of this predarion on birdwinrr abundance have nor becn
invcsrigared bur opportunisric predation by anarher erythracid mite (Balnwtium
sp.) on the ems of a pierid burrcrflv can bc a major cause of pradulr monaliry
(H~YCS 19857;
Scigmaeid mites seem ro have a predilection for cggs, including those of
plant-parasitic mites and competing predators, and even cannibalise their own
cggs (Clements & Harmsen 1992). For example, ZEnellia mali wander leaves
and feed on the eggs of a variety of plant-parasitic and predatory mites thar they
encounter (Santos 1991). O n apple laves, Z. malispend about three-quarters of
their foraging time on and around d,r midrib, resulring in preferenrial con- I
sumption of eggs ofspecies char oviposir in this area ( M c h & Croft 1996). As
with most planr-inhabiring stigmaeids, Z mali oviposir on leaf hairs or errant
strands of silk, presumably reducing the chance of cannibalism.
Foliar Mesostigmata
In contrast to the diversity of predatory prosrigmarans, only a single family of
mesostigmatans, the Phytoseiidae, is characteri~ricall~ found on leaves in tcm-
perarc forests. This lineage, however, has undergone a specracular adiarion on
vegetation and accounts for abour 15% of rhe known diversity of Mesostigmara.
Most of the 1700 species have been described since World War I1 as a direct
rciulr of their importance as biological conrrol agenu (Chant & McMurtry
1994, Kortianinen & Hoy 1996). They are small ( 2 0 0 4 0 0 p m in length) and
supprccs many of the idiosomd and leg serac found in rheir roil-inhabiring rel-
atives. Tempcrate phytoseiid faunas are relarively well known but tropical faunas
ace cvtrcrnely diverse and have scarcely been rouched (Walrcr & Beard 1997,
Waltcr 81 I'rocror l798b). Borh thc local and regional species diversity ofphy-
tosciid milcr increases from remperarc ro rrapical regions and additional lineag-
es of Mesostigmata (c.g. Ascidac, Olognrnasidae, Uropodidae) begin appearing
in rbc phylloplmc fauna Walter er nL 1994, Walter & Procror 1998b). For
example, in rropical Ausrralia species in the Laiiorciusporulorur group and the
Arca fi[iara group (both Ascidae) are often more abundant on leaves than are
phytosciid mites (Walter er aL 1993, 1994, Walter 81 Lindquist 1997).
Producing a balance between predatory and plant-parasitic mites in agricul-
tural systems is one of the goals of Integrated Pcrr Management (IPM).
However, predatory mires actively search for prey and are much more likely ro
encounter a pesticide droplet than arc more sedentary plant parasires. For this
and ocher reasons, pesticide usc often dismprs popularions of predatory mites.
Before World War 11, phytoseiid mites were a curiosity and few species had been
described. In the post-World War 11 D D T era, however, accounts of damaging
outbreaks of spider mites after the application of such as D D T and
pamthion to control pests became all too common. This is when rhc hunt for
potential biological control agents of spider mires began and in unsprayed fields
and orchards pbytoseiids were the primary group of predarorr encounrerrd.
Development and reproduction of phytoseiid mites
The r o d life cycle of phyroseiid mircs, from egg to egg, usually raker
8-10 days at 22-24'C (Sabelis & Helle 1985b. Sabelis & Janssen 1994)
bur varies wirh subfamily (Amblyzeiinae haw farrer average rates than
I'hytosciinae-Typhlodrominae) and with gcnera within subfamilies (Zhang
 MITES: ECOLOGY.EVOLUTION
A N D BEHAVIOUR
1995). Species in some amblyseiine genera, eg. Pbywseiulus, have generation
rims as short as five days at Summer temperatures and, given enough food.
fkxdes can lay 3-5 a day for several we&. Development and reproduction
can be influenced by the host plant on which the DRY fkcds. For examde,
Pbytozeiulru petsirnil& rearal on -wo-spotted spider kt&grown on
had 10s than half the fkcundity (33 eggs per finale) of those reared on two-spot-
red mites grown on soybean (69 eggs per kmale) (Popov & Khudyakova 1989).
Except Tor a few known thelymkous species (Hoy 1985), phytoseiids must
mate in order to lay eggs. Female deutonymphs near maturity produce a
182 ,pheromone that produces an arrcsanenc: response in males (Rock ct aL 1976,
Hoy & Smilanick 1979). A single mating apparently is sufficient to ferdise a
bale's endre complement of eggs in some species, whereas in others, f;unaes
apparently run out of sperm and oviposition stops until they mate again. Males
develop fiom fertiliscd eggs. but have a haploid genome as adults. The paternal
set of chromosomes is lost or heteroduomatised in the early development of the
eggs destined to become males. This has been termed both parahaploidy and
pseudoarrhenotob (set Chapter 5).
All species studied arc muldvoltine and in warm, tropical or subtropical di-
mates all stages can be found essentially anytime of year. In dry tropical climates,
reproduction appears to be more seasonal. In tunperate climates, the adult
female is the overwintering stage and a reproductive diapause has been demon-
strated for a number of species. Photoperiod is the prime fictor inducing dia-
pause but it ofien interacts with temperature, relative humidity and nutrition.
For example, in some species carotenoids are essential for photoperiodic induc-
tion of diapause and can be supplied in part by the pollen of some plants (Van
et aL 1981, Overmecr et aL 1989). For a comprehensive review of diapause in
the Phytoseiidae, see Veermann (1992).
Feeding biology of ph~toseiidmites
Much of what we know about the fbading biology of phytoseiid mites is based on
the fkw species that arc wfLl in biological control (McMurrry & Crofi 1997).
Preeminent among this small group arc the predators of spider mites in the genus
Tmanychs that produce dense webbing (CW-u type of Saito 1983). One of the
most u s d of all of these biological control agents is &e Chilean predatory mite
Phyt~~ulurpmbstilk. perhaps the most intensively studied of all acarine biolog-
ical control agents. A recent bibliography of the Phytoseiidae (Kostiainen & Hoy
1996) lists nearly a thousand citations indexed to PpmimiCis (21% of the 4634
items). Like its spider mite prey, the Chilean predatory mite hragts for new
rrsources both by h t and on the wind (Charles 8c White 1988), and the pred-
ator responds to chemical signals both from its prey and the prey's host plant
(Bruin e t a l 1995). Chilean predatory mites have elongate dorsal shield setae that
help them to penetau the dense silken webs of Tctnrnychus (Sabelis & Bakkcr
1992) and the predators take up residence in the midst of their prey. Eggs arc laid
on the spider mite silk and the nymphs and adults hunt h u g h the web.
The Chilean p d t o r y mitc and other species of Phytusciulut appear to
require spidu mites that develop in dense colonies with heavy webbing, espe-
cially species of Tctrrutg,cbus.This d- of trophic speciaisation is unusual in
the Phytoseiidae, although species of Phytosrutrrsare associated with folk acarid
mites in the genus Neotmpacarrrs.A few other phytoseiid mites, e.g. G M m r n u r
occidntkslis (Nesbitt), Neosnirlw faCIitciz and Typblodtomus pyl.i, seem to prefer
spider mites but they also cake other prey and fixd to a limited extent on plant
products such as nectar and pollen (digested externally). Most phywseiid mites,
h o w s arc polyphagous and some appear to do best when thy have a high
propomon of pollen in their diets (McMufpy & Crofi 1997). The diet of some
E-us species can be very complex and indude prey, pollen, honeydew and
pknt exudates (Bruce-Oliver n a! 1996). Even species that are usually consid-
ered efkctive predators of spider mites may be mom likely to udise a range of
food types in the wild. For example, TybbdrbarM can obtain enough nuui-
em f b m the conidia of mildews to support development and low rates of ovipo-
sition (Zunek & Prenerova 1997). In natural systems, these generalist
phytoseiid mites ate abundant and relatively unifbrm in their distribution com-
pared to most plant-parasitic mites.
MITES AND LEAP DOMATIA
From the pespeaive of an animal as minute as a mite, the &of a leaf will
seem a c~mplac and variable habirat. Sicc mites arc small, they can seek out small
crevices in which to shelter. But bdngs d also means that even a single leaf may
he an immcclsc distance to aws.The large smooth,rainhedding leaves of many
tropical accs must be especially challenging places to livc.Other leaves are covered
by foreas of hairs (tomenta) and other leafsmrcrures. The difkrmces in fbliar mite
populations between adjacent treeswith di&rences in pubescence can be striking.
Haky leaves in tropical rainfbrcsts in Ausualia typically average three times as
many species and five times as many individual mites as smooth leayes at h e same
site. Faaors such as the density of hairs on leaf veins and in vein axils can be espe-
cially imporrant in the distribution of predatory mites (Karban et aL 1995). Only
mccndy have the responses of mites to leaf architecture been considered but it is
clear that leaf surfice snucnws alur mite abundanccs, iduencc predator-prey
ineradons and arc central to an understanding of the relationship between phyl-
loplane mitcs and plants (Wdter 1992, Wdter & O'Dowd 1995b).
More than a centllry ago a Swedish worker, Axel Lundsui)m (1887), noaced
that tufts of hairs found in the vein a d s on the underside of the leaves of lime
trees o h sheltered mites. He called these & of hairs, and other tiny struc-
tures that protected a small pocket of leaftissue, acarodomatia (mitc houses) and
compared them to the much hger cavities that housed ants (brmicaria or ant
domatia) on the leaves of some tropical plants. Unbrtunately fbr Lundsaiim,
botanists did not take his observations seriously and his hypothsis that mites
Iived in leaf domatia and that plants benefited from the association was consid-
ered crackpot at best (O'Dowd & W h n 1989). It did not help that ,
Lundstr6m mistakenly believed that mites induced acmdomatia. Leaf domatia
are under the genetic control of the plant, unlike the hair-lii erinose patches,
pocket galls and other dehrmities produced by eriophyoid mites. The rolled leaf
margins (orlettes) of some plants appear to be analogous to domatia.
Structure and distribution of leaf domatia
In tempcrate fbrcsts of che Northern Hemisphere, aws and shrubs with leaf
domatia arc very common but the domatia themselves arc mostly unrunarkable
structures: simple & of hairsin shallow pits in vein axils on the underside of
leaves (Willson 1991, O'Dowd & Pemberton 1994).These dumps of hairs may
MITES:ECOLOGY,
EVOLUTION
A N D BEHAVIOUR
be useful for telling one oak or one blackberry species from another but attribut-
ing an adaptive Function to them seems to be straying into the kind of reduc-
tionist storytelling that Stephen Jay Gould and Richard Lewontin (1978)
criticised so effectively with their example of the spandrels in the dome of the
great San Marco cathedral in Venice. The spandrels, referring to the tapering tri-
angular surfaces between pairs of intersecting arches that suppon, the dome, each
contain an elaborate mosaic mural that perfectly fits the space and smoothly
integrates the piitorid story inlaid across the arches and ceiling of the cathedral.
Gould and Lewontin argued that it would be easy to be overwhelmed by the per-
fection of the iconography, invert cause and effect, and assume that the triangu-
lar mosaics induce the construction of spandrels for their display.
In the case of leaf domatia, spandrel may be a particularly apt term because
a domatium fills the triangular space formed by intersecting leaf veins. Veins
often bear hairs, so one might expect the juncture of two hairy veins to have a
high density of hairs - a plant architectural inevitability with no need for an
adaptationist explanation. Most botanists seem to have adopted such an icono-
clastic view of leafdomatia: they are useful taxonomic characters that needed no
further explanation (O'Dowd & Willson 1989).
Figure 8.3
h f domatia of rwo rainforest trees from Queensknd: (left) pit-arfc domatia of Sloanea
(right) pocket domatiurn of Eloeoccupus obavotus (both Haeocarpaceae)
WOOISI;
_ throughout the world has found that small arthropods, their cast skins and their
However, many woody ~ l a n t sin subtropical to tropical forests have leaf
domacia in the form of pits sunken deep within the leaf lamina, igloo-like domes
that rise above the surface or ~ocket-likesheets of tissue that connect the veins
(Figure 8.3). These domatia are very house-like, at least at a microscale, and are
not as easily dismissed a s hair tufts. Even the domatia that Lundstrom studied
on lime tree leaves are striking structures: large cottony tufts that rise well above
the leaf surface. As with our own armpit hair, these tangles seem poorly
explained by traditional concepts of the function of hair.
Given the diversity of structures that have been called leaf domatia, one
might wonder if the definition is too diffuse? Leafdomatia usually occur in vein
axils on the underside of leaves. This is true even when veins are weakly
expressed. Similarity of position is a basic criterion of homology and finding
similar structures in the same location argues for continuiry through descent, at
least among related taxa. In some genera of rainforest trees (e.g. Cryptocarya),
certain species have simple tuft domatia. while others have more elaborate
domes or pockets in the same location: moderately strong evidence for genetic
homology. However, the structures called leaf domatia are found in more than
30 h i l i e s of woody angiosperms and it seems likely that they have been
evolved convergently numerous rimes (O'Dowd & Wdlson 1989). Vein a d s 1
must be predisposed to the production of leaf domatia, much as heads are pre-
disposed sites for the evolution of horns in various animals. Exceptions tend to
prove this rule. For example, the tropical tree Emoniuz timon has pit domatia
that occur on the upper surface of the leaves, but again, in vein axils (O'Dowd
& W~llson1989, Walter & O'Dowd 1995a).
As well as positional similarity, leaf domatia share a basic structural similar-
ity that seems more important than their differences in construction. Most leaf
domatia enclose small spaces, typically a millimerre or less in diameter. h s to
the interior of a domatiurn is via a minute pore, slit or gap. For example, tuft
domacia ofien resemble the tangles of brush ;hat are pullgd-together fo; ternpo-
rary shelter by hunters in many tribal societies (e.g. the wickiup of the Apache
and the humpy or gunyah of Australian Aborigines). Access to the sparsely filled
centre of such a tangle is limited by the space between the shafts of the hairs that
form the outer margin of the domatium - typically less than 100 pm. Pit doma-
cia open through similarly small pores. Pocket domatia consist of sheets of tissue
that roof over the vein junctures. These ofien have relatively broad openings
(1-3 mm) that could be accessible to small, flattened insects but many pocket
domatia sport growths of hairs that reduce the effective size of these openings.
Except for a few very large domatia found on some tropical plants, the size of
the space enclosed and the size of the opening to that space ensure that only very
small organisms, such as mites and minute insects, can enter.
W h a t lives in leaf domatia?
Although Lundstrom first reported mites in domatia, many botanists subse-
quently claimed they were unable to find any arthropods consistently associated
wirh leafdomacia (O'Dowd & Willson 1989). It is certainly possible to find leaf
domatia that are uninhabited, especially on newly flushed leaves, on trees in cirv
p a r k or in vineyards with heavy pesticide use (many grape varieties have welt-
developed leaf domatia). Howwer, every serious examination of leaf domatia
faeces are consistently present.
With a single exception, mites have been found to be the predominant
inhabitants of both t u k domatia and the more elaborate pits, pouches
and domes (Walter 199G). The exception is an extremely small species of thrips
, (Thysanoptera) described from leafdomatia in Costa Rica (Mound 1993). Large
black and red h i p s can be found in some of the larger leaf domatia in
Australian rainforests, but rarely. these thrips appear to be predators. The
nymphs of small bugs (Heteroptera) that may be predatory also are occasional-
ly found in leaf domatia. However, even these small imects are a bit too large to
, fit into most leaf domatia comfortably. In contrast, relatively large scale insects
(Homoptcra, Coccoidea) can be found completely filling domatia. Adult female
scales are bloated, sessile, plant paraites but they develop from a minute crawl-
ing stage. The older leaves of some Australian rainforest trees sometimes havc all
of their leaf domatia clogged with scale insects or their pamitised bodies.
Garden trees and shrubs, such as bay leaf and elms, may also have their leaf
domatia clogged with scale insects. Overall, however, insects are rare in leaf
domatia: mites are commonplace.
Predatory mites and those that scavenge and feed on Fungi and other
microbes usually represent over 90% of the arthropods in domatia (Walter
1996). None of these mites are known to harm plants. In fact, plants with sig-
nificant populations of predators and scavengers are likely to receive consider-
able benefits from reduced parasite load and from the mobilisation of nutrients
sequestered by leaf fungi, algae and other epiphylls such as bacteria, yeasts, liv-
erworts and lichens as mites graze and defecate.
Fungivores are especially common inhabitants of domatia in humid cli-
mates. For exaniple, on a wild grape in Florida, populations of the rydeid
Orthotydnu nr. lina+isti and the asrigmatan Cumpinskirr transvcrsostrifita
increased dramatically during the onset of the rainy season. Individual leaves
oken had several hundred fungivores and domatia were packed with eggs and
moulting mites (Walter & Denmark 1991). Mildews are a common problem on
domestic grapes and one of the main factors limiting commercial production in
Florida; however, this mite-infested wild grape species thrives there.
In another study, leaves of a dozen species of rainforesr plants had leaf donla-
ria blocked with a bitumen paint. Five months later, fungivores were six times
more common on leaves with domacia left open than on adjacent leaves with the
domaria painted shut (Walter & O'Dowd 1995b). Tllercfore, leaf donlaria
appear to elevate populations of Fungivores but whether the plant gains from
having herds of these mites roaming i t s leaves is difficult to test. Fungi vary in
their effect on plants from beneficial to deleterious and the imporrance of cle-
vated numbers of fungivores on leaves with domaria is dificult ro evaluate in
natural systems. A far clearer example of a benefit to plants would be elevated
numbers of predatory mites that are know11 to act as 'bodyguards' ag~instplant
parasitic mites (Dicke & Sabelis 1988).
dornatium significantly increased the chance that a leaf also had a resident preda-
tory mite and the proportion of leaves with predators climbed wid1 the number
of domatia per leaf.
That predatory mites seek out appropriately sized spaces on the plants they
inhabit is not in itself surprising but that planrs produce structures that have no
known function except to liousc mites calls for an explanation. This is especial-
ly true because plant-pamitic mites are at best rare and ephemeral inhabitants
of domatia. Even during outbreaks, when dozens to hundreds of pests occupy
each leaf, few plant-parasitic mites seek refuge within domatia.
Plant-parasitic mites affect plant fitness through reduction in yield (growth 187
and reproduction) and death of plants. The evidence for this in aericultural
"
svs-
terns is overwhelming, especially since the advent of synthetic insecticides eie-
vated spider mites to major secondary pests. Plant-parasitic mites are small, use
stylet-like mouthparts to puncture individual plant cells (and thus can avoid
many plant defences) and have short generation times and high reproductive
outputs, allowing them to overexploit their hosts (Dicke & Sabelis 1988).
Howcver, plant-parasitic mites must run a gauntlet of predators when they
artempr to colonise leaves with domatia.
If leaves with domatia tend to retain wandering predatory mites and these
bodyyards arrive before attack by plant parasites, then domaria can be consid-
ered a type of constitutive defence against herbivores. One ready prediction of
this hypothcsis is that the renloval of domatia should result in fewer bodyguards.

Domatia as a constitutive plant defence

Predatory mites are often active animals that move rapidly and frequently in
their search for food. Therefore, chance alone is a sufficient explanation for an
occasional predatory mite found loafing within a leaf domatium; however, a
more consistent association between predatory mites and leaf domatia would be
more difficult to explain. Mite use of leaf domatia has now been evaluated in
North America, Costa Rica, Hawaii, Australia, New Guinea, New Zcdand,
Bangladesh and Korea (see review in Walter 1996). In all of these studies, preda-
tory mites are common inhabitants of leafdomatia and leaves with domatia havc
more predators than leaves without domatia. This is true even within a spccies
as demonstrated in Figure 8.4. This g a p h is based on about 1200 leaves from
two rainforest tree species that grow in eastern Australia from just north of
Sydney in the south to just south of Cairns in the north. About half of all the
leaves collected were without domatia -and rarely had a predatory mite - but
the other half had from 1-6 (rarely 7-9) domatia per leaf. Even having a single
Walter & O'Dowd (1992 a, b, 1995b) used two techniques to 'remove' doma-
cia fiom leaves. The simplest technique was to shave off tuft domaaa with a
small scalpel. The leaf s&ce below each domatium was suaped with the scalpel
on another treatment to control for any effects caused by shaviq. After two
weeks, predatory mites (mostly the stigmaeid Agistemur &n@m~sand the phy-
toseiid &n'ru elinue) were 4-7 times more abundant on leaves where the doma-
ria had been left intact (Walter & O'Dowd 1992a).
Tufi domatia in shallow pin can be removed by shaving but most lcafdomatia,
even most ruft domacia, a~ complex suuaurrs and cannot be cut away h m plants
without causing sipiticant damage to leaves. Walter & O'Dowd's solution to this
problem was to paint the entrances m domacia dosed with a bitumen paint (thick-
ened with ground ddk)on newly flushed leaves. As wi& the shaving experiment,
an appropriate conpol treatment was needed and in this experiment paint was
dabbed below the domacia on a second set of leaves. To dare, this technique has
been applied to 13 species of sees, shrubs and lianas in Australia and in every case
dosing domatia with paint resulted in drastic reductions in the numbers of preda-
tory mites in comparison to leaves with paint dabbed below the domatia (Walter &
O'Dowd 1992b. 1995b). Laboratory experiments have taken these results one step
f i d e r to demonmate a proteaive effect of leaf domatia (Walter & O'Dowd
1998). Shoots of an ornamental shrub with domatia shaved off had higher nurn-
bus of spida mites and lower numbers of predators than similarly dshoots
with domatia lefi intau Sunilarly,Grostal& O'Dowd (1994) d u n o n m a d thac
predamrs ate more spider mite e&s when domatia were present.
The reverse holds m e as well. In an innovative series of experiments, Shelley
Rozario (1994) added & of polyester fibres to the vein axils of grape varieties
with poorly c x p d domatia and observed the efFecc on the phytoseiid preda-
tor Gahndmmw occidmtrrlrj. Leaves with a d c i a 1 tuft domatia retained more df
the predator and these mites had higher reproductive outputs than on the same
grape variety without polyester &. In the field, results were more variable but
in some experiments rydeid and phytoseiid mite populations were significantly
higher when artificial domatia were present Similar results have been found in
other systems (Agwaral 1997) and the dornatia concept has been applied to cot-
ton plants using relatively large & of cotton (4 mm diameter) glued to leaves
at their juncture with the petiole. These tufts of cotton harboured predatory
thrips and bugs and, as a result, plants with artificial domatia experienced less
damage by spider mites and a 30% increase in fiuit production over cotton
plants without simulated domatia (Agwaral& Karban 1997).
What's in it for the mites?
Given the potential of plant-parasitic mites to reduce plant fimess and the abil-
ity of predatory mitcs to protect plants &om attack, the independent derivation
of dornatia in many lineage of angiosperms is easily understood. Under attack
by plant-pansitic mites, individual plants with leaves having resident predatory
mites would experience enhanced survival, growth and reproduction. Plant par-
asites would be picked off as they atrempted ro colonise leaves and before they
could produce large, damaging populations or have much chance to veaor a
plant disease. But what of the predatory mites?
Predators with narrow prcy ranges or that require large populations of prey
for reproduction are unlikely to h d -leaveswith domatia espeddy fivourable
habitats. If mites gain no particular benefit fiom entering domatia or if
predators are lured away from better hunting grounds by hideaways on barren
leaves, then the mica could be aploitcd by the plants. In the field, specialised
predators such as species of Pi?yf~sn'ulur are rarely found in leafdomatia; they
live in the webbing of their spider mite prcy and enter domatia only at low prey
densities. Most of the predatory mites associated with leaf domatia are " eened-
kt species of phytoseiid, chqrietid, stigmaeid and cunaxid mites that can be
bund on many different plant hosts in a region and have broad prey prderencts.
Many of these mites an also able to persist on pollen, honeydew and fungi;
therefore, leaves having convenient shelters may be especially attractive.
The most obvious benefit of leaf domatia to predators is protection and shel- 189
rer, especially for eggs and moulting mites. Several studies have demonstrated
chat phytoseiid mites preferentially use leaf dornatia b r oviposition and
moulting Wdter 1996). In the field, more than threequarters of all eggs laid by
phytoseiid mitcs were found within domacia In a series of laboratory experi-
ments, Grosral& O'Dowd (1994) demonstrated that leaf domatia b&rcd the
effect of low humidity and when domatia were present the predator
Galenhrnw o c ~ t u f i laid
s more than twice as many eggs as when domatia
were absent.
PHYLLOPLANE SCAVENGERS AND
FUNGIVORES
Burnerworts (Pin+ spp.) are low-growing carnivorous plants found in moist
soils whose leaves arc coated with glandular hairs that secrete drops of adhesive.
Small insms that land on a leaf are ensnared by the adhesive maps, die and are
digested by the plant. The undigested remains accumulate on the s&ce and
can support the growth of fungi that also can attack the leaves. However, a small
oribatid mite, Odatula tibidis, k able to wander among the glandular hairs
without becoming trapped The mites feed on fungi and on the undigested
remains of prey, thereby reducing the resources thar support chc growth of path-
ogenic h g i (Antor & Garcia 1995).
Intuitively, leaves do not seem a suitable habitat for oribacid mites, arche-
typal denizens of the soil, but species in 17 families have been recorded from leaf
su&ces from tow-growing plants like butterwort to the tops of the highest rain-
forest ttees (Walter & Behan-Pelletier 1999). Other mite scavengers also have
colonised the phylloplane, probably in the same manner as oribatid mites -via
a long evolutionary progression from the soil, up the uunk and stems, to the
leaves. Leaves are a good place to start in our consideration of arboreal scavengers
because the phylloplane is as Merent a habitat tiom the soil as one can find in
forest canopies. Temperature fluctuations, light conditions, wind currents,
humidity and water flow all tend to be buffered and predictable in soil but vary
rapidly and extremely on the phylloplane. S& nooks and crannies are at a pre-
mium and on many smooth-surf8cod leaves a small boundary zone along the
midtib is the only refugium.
Scavenging on leaves
Oribatid mites living on leaves are readily identifiable by their morphology, espe-
cially by the short, dubbed to globose prodorsal sensilla that are characcerisd-
cally present (Norton and Palacios-Vargas 1982, O'Dowd ct aL 1991. Hum
1996). As an organism moves, it displaces a volume of air and creates 1 0 4 air
 MITES: ECOLOGY,EVOLUTIONAND BEHAVIOUR
currents. This is especially true in doscd spaces such as exist in the soil. Most
soil-inhabiting oribadds are blind but they have elongate, and ofien plumose,
p r o d o d sensil1.ithat may provide them with a radar-like image of animals mov-
ing in their vicinity. Mites living on leaves, however, must be exposed to an
excess of wind current infbrmation and hence the short, thick sensilla.
Cemtegumcnt, a waxy cuticular seaetion, can be especially thick on arbo-
real oribatids and probably aids in water ~nservation(Alberci et aL 1997).
I
190
Other modificato& to & and secretory organs may reflect arboreal adapta-
tions (Water8c Beban-Pelletier 1999) but perhaps the clearest adaptation to lifk
on the phylloplane is the convergent evolution of adhesive empodia on the tarsi
of many leaf-inhabiting oribatid mites. For arample, AaksozempoIypbyIlbs has
a single large claw on each tarsus beneath which is a large ~eccangularsuuion-cup
Walter & Behan-Pelletier 1993). The daw probably serves both to grip rough
su+ and to lever the suction cup free fiom smooth surfkces.
An interesting, but unexplored, characteristic of arboreal oribatid mites is
that s d dimorphism tends to be well developed. In soils, male oribatid mites
tend to be half the mass of k d e s but are otherwise unremarkable. Males of
arboreal taxa, however, are ofien coverod with bumps, processes or hom-like
serae that are absent fi*omfemales. For atample, the genus Symbwribatcswas first
described fiom a mite living in lichens growing on the backs of weevils in New
Guinea (Aoki 1966). Other species of Symbiorr'bam arc common on leaves in
Australian tainf$tests. The males of these mites have elongate, inflated prodor-
sal s e a that resemble the horns of bulls or, given their heavy armour, ceratop-
sian dinosaurs (see Figure 5.3). Although oribatid mites are thought to have a
primarily indir#x and dissociated mating system where spermatophores are
deposited by males with fkw or no cues fiom firnates (see Chapter 5), it is tcmpt-
ing to speculate that arboreal oribatid mites have repeatedly evolved a more inti-
mate association.
In Australian minfbrests, the oribatid fiuna of leaves has been derived from
numerous independent colonisaaons by mites in various superfbdies. For
example, only the Oriopodoidea and the genus Scaph- within the
Cymbaeremaeidae have radiated extensively on the phfloplane. Other lineages
are represented by f kgenera and species. This pattern holds true fbr the most
impressive of all sarcoptifbrm radiations, the Astigmata. Only two genera of
asugmatans, each from a &rent h i l y , are commonly found on leaves in
Australian fbresrs. Species of Neompauzrw (Acaridae) are relatively large mites
that occur in moderately dense aggregations that suggest a degree of subsociali-
ty may be present. Leaves with smooth surfices seem to be prekrred. In contrast,
specits of Cenrrpit~tkia (Winterschmidtiidae), including the cosmopolitan
thclyrokc C m n s v r n o are ~ hund on hairy leaves, and there is no indica-
tion of aggregation behaviour.
In mesic to humid forests, densities of oribatid mites can exceed seveat hun-
dred per l d , however, over all leaf and b r a t cypes the most charaaerisdc
acarine inhabitants of the phyiloplane are +id mires. Many tydeids are sus-
pected of being opportunistic predators, e.g. species of T M O&ty&u,
h n m t a t u r , especiaty of eriophyoid mites. These rydeids tend to be pale to apri-
cot in colout. Species in other gcncra, however, o h take on deep greenish hues,
presumably from f+ on algae and Lichens. Herbivory is suspected in some
&liar tydeids but we have been unable to find convincing evidence that m y
tydeid mites are plant parasites.
When leaves or fiuit are damaged or attacked by parasitic h g i , rampant
fungal growth ofien occurs on the damaged and dying tissues. Mites that k d
on +, eg. oribatids, astigmatans, tydeids and tarsonanid mites, arc amact-
ed to such areas and can produce large populations. Even healthy leaves ofien
have a fine covering of oppormnisdc fhgi and honeydew h m k d h g by
homopterans often ptoduces dense growths of mildews that can support popu-
lations of scavengers and rirngivores.
Another group of fhgivores that has done well on the phyiloplane is the
Tarsonernidae. One particularly success11 group is fingikuront~us.Many of
these mites have the unusual habit of collecting tiny bits of detritus - pollen,
alga balls, bits of leaf hairs -and gluing them onto their ba&. Presumably this
camouflages them from predators and it certainly can astonish one to set a
minute ball of fluff dashing across a leaf,Some species also glue extensive fields
of detritus to the leaf surfice in which eggs are laid and larvac secrete thel~l~e1ves
b&re the moulting to adults. The latter is an especially interesting behaviour
because in the Tarsonemidae quiescent f k d e larvae are usually carried on the
anal suckers of mak carsonemid mites.,(Figure5.6).
Mom species of Tanonrmus are thought to be fhgivores, including species
in the waikigroup that have sometimes been suspected of phytophagy (Suski
1967, 1972, Lindquist 1986, Nucif$ra & V d t e 1986). They ate commonly
fbund in protected amas on leaves and h i t (e.g. in leaf domada and under the
calyx) and are usually associated with growths of b g i . However, some species
of Tarsotlcmusand members of the genera & m t ~ m w and Dntali.0~- arc prod-
amrs of eriophyoid mites or the eggs of Teuanychoidea. Many other genera of
Tarsoncmidae can be &und on leaves, especially old rainhest leaves that are
encrusted with growths of lichens and liverworts. HoweverJ these mires, c.g.
species of Daidalotanontmus and Crratok~ronemur,are usually more abundant
on stuns and trunks where growths of epiphytes are more ~ n s i v e .
Moss mites
Oribaad mites ofien arc called moss mites (mo-16m in German) because they
dominate the acarohuna living in the epiphytes that cover stones and the bark of
the trunks and stems of trees. Species in the h i l i e s Achiptcriidae,
Ameronothridae, Camisiidae, Carabodidae, Ceratozetidae, Crotoniidae,
Damaeidae, Eremaeidae, Gd~mnatidacjHammeriellidae, Liacaridae, Liodidae,
Megeremaeidae, Micreremidae, Mochlozetidae, Mycobatidae, Nanhermanniidae,
Oppiidae, Oribatulidae, Oripodidae, Pedrocortcscllidac, Peloppiidae,
Phenopelopidae, Phthiracaridae, Tectocepheidae and Xenillidac all are common- .
ly found associated with bark and epicorricolousmoss and lichens on aet trunks
and branches (Walter & Behaa-Pelletier 1999). Epiphytes often grow in patches
and mites Living in these dumps have highly aggregated distributions. Some
specificicy to d i f k n t types of epiphytes is also known. For example, species of
Dohna arc fbund in crustose lichens, those of EiKmMnu and Tticrbodatcr
are s h c l d by bliose lichens (Anbc 1984, 1985). Mort general patterns of
hosc-spccificity may be present as well. In a series of studies on diffErrnttree
species in North America, Europe and Ati.ica, Nicolai (1986, 1989, 1993)
demonstrated that both ace species and bark type a&ct4d the development of
epiphytes and the resulting oribatid diversity. Of 19 species collected h m the
bark of 5 species of conifirousand 5 species of deciduous aees in North America
only 5 mites were common to both. Among deciduous species, those with
 MITES:ECOLOGY,EVOLUTIONA N D BEHAVIOUR
structured bark had the highest numbers of species and individuals, whereas the
reverse was true for conifirous uee species (Nicohi 1993).
Epiwrticolous oribatids graze lichens, algae and Fungi, and also may have
more complex ecological roles. For example, species of Humembatidae are
known to disperse lichen soridia (Stubbs 1995), and other oribatid mites may
spread fungal pathogens. Nanelli and TuKhetci (1993) demonserated that
SchcCoriba~skrcipcs from bark habitats on chestnut can be cultured on virulent
strains of the funrms chat cause. chesmut canker. that virulence is not reduced
in passage throu& the mite guts and that rhis s&es a h can transmit thtdis-
192 ease through carrying fungal spores on the body. Species of the c e r a m a d gen-
e& H u m b and ~ Diaptctobtztm are particularly common on twigs, - branches
and buds (Murphy & ~ a l l a1971, Momen 1987), and sometimes alarm
orchardists. However, these mites scavenge on dead plant and animal material
and eat living fungi and algae: they pose no threat to the trees.
In Japan, a stem-inhabiang oribatid, Diaptrrobates b u d has an unex-
pected relationship with the hemlock woolly adelgid (Aa%&cz -a),a darmc-
tive pest of hemiock mes in N o d America. The kmale adelgid feedson young
shoots and before dying lays about 200 eggs in a sac wvercd with waxy fila-
ments. The mite feeb primarily on the hyphae and spores of h gi; however, it
has also developed a taste fix the woolly filaments covering the eggs and while
grazing on them dislodges the egg sacs, which then M1 to the ground.
Displaocmenc of egg sacs is emrcmely high in sires with large populations of
mites and survival of displaced eggs is near zero, so this oribatid mite acts as an
inadverrent predator (McClure 1995).
Fungal sporocarps
Large, fleshy to woody sporocarps are produced by many fungi growing on
scanding dead wood and others sprout from the hcarrwood of idkctad living
uees. These include traditional mushroom-like structures Jlat persist only for
short periods of time and more elaborate, longer-lived conks, shelf fungi and
bracket fungi. All of these sporocarps soon become inhabited by mites, primari-
ly through phoretic transport by insects, especialy the beetles and flies that
breed in the h g i . All except the woodiest sporocarps are ephemeral resources,
so colonisation, devdopment and unigration must occur within a restricted
span of time. Thii is especially true during the warmer months in temperate to
subtropical dimates and at any time in the tropics. Therehe, the mite fauna of
sporocarps in these dimates tends to be dominated by species with short gener-
ation times, such as is bund in many Asdgmata and Mesosrigmata.
In temperate forests, the mesostigmatan assemblages on bracket fungi are
composed of species in about a dozen genera (Pielou & V m 1968,
Matthcwmann & Pielou 1971, Lindquist 1975b, OConnor 1984, Lindquist
1995, O'Connell & Bolgcr 1997). In subtropical to tropical Ausnalia. the
mesostigmatanfiuna of h g a l sporocarps is far more diverse and a single sporo-
carp may have more than a dozen species (Walter & Proctor 1998b. Walter etd
1998). These mites primarily belong to the fiunilies A r n d i d a e , Ascidae,
Cenomegistidae, Digamasellidae, Laelapidae, Macrochelidae, Sejidae and
Uropodidae (Lindquist 1975b OConnor 1984. Walter & Proctor 1998b). Most
mesostigmatans found in bracket fungi are mycetophiles that feed as predators
on the insecrs, mites and nematodes that inhabit decaying .
sporocarps but
- .
Amerosciidac ( ~ m e r o ~ r i u
and
f ) some Ascidae arc fungivores.
Mycophagous ascids appear to have arisen several times from predatory
mycctophiiic ancestors (Lindquist 1975b 1995, OComor 1984). For example,
species of Hopbseius are found only on living bracket fungi, where they fecd on
fungal cissue (Lindquist 1963, 1995, Walter 1999). Most species Live on the sur-
face of the bracket fungi where they can be observed probing the spore tubes
with their mouthparts; however, a Mexican species, H. tcnuis, has an artraordi-
narily elongate body that allows it to live in the spore tubes on the underside of
the hrngal shelf (Lindquist 1965). An unrelared ascid mite from brackec fungi in
western Canada and the United States, MycoCaelaps -nar, has convcrgcntly
evolved a similar elongate body and tube-inhabiting I*& style (Lindquist 1995). 1
One of the most common groups of astigrnatans in fleshy fungi are histios-
tomacid astigrnarans. These mites crawl through rotting sludge, f i l t e r - f m on
bacteria, yeasts and very fine particulate organic matter Walter & Kaplan
1990). In b o d to cool temperate forests, the acarofhna in long-lived bracket
fungi is often dominated by oribatid mites ( Pielou & Verma 1968,
Matthewman & Pidou 1971, O ' C o m d & Bolger 1997). Annual and perenni-
al bracket hgi have a much more diverse huna of oribatid mites than that of
the mom ephemeral agaric and bolete fungi. Oribatids in fungd sporocarps
show no evidence for fbeding specificity on a particular hp or avoidance of
the toxic metabolites in certain (O'Comell & Bolger 1997) and these
mites may originate from the fiuna associated with dead wood.
Under bark
Dead wood forms a significant component of above-ground biomass and
decomposition may proceed for some time before the stem or trunk crashes to
rh'e forest floor. Standing dead wood and similar cavities in high living uees are
home to a variety of oribatid mites and other deuitivores that invade from the
bark or in association with wood- boring insects. Beetle galleries within living
wood are also Likely to harbour a distinctive mite fiuna; however, fkw studies of
this fiuna exist except for those associated with moribund conifers in the
Nodern Hemisphere.
Pine, spruce, fir and hemlock all are attacked by a number of scolytid, ccr-
ambycid and buprescid beetles that cause signi6cant economic damage. The gal-
leries constructed under bark and the burrows that enter the sapwood of the
trees am home to numerous Asdgmata, Mesostigmata and Prostigmata (Kim
1971, Moser & Roton 1971). Tarsonemid mites are often prominent among the
latter and include parasites of beetles' eggs (Lindquist 1986) and fhgivores that
often have intricate relationships with the fungi, beetles and rrees (Bridges &
Moser 1986, Moser 1985, Moser et uf 1989). Mesostigmata, including many of
the genera found in decaying fhngi, arc especiaUy prominent as predators of
nematodes and mites in galleries, and as phoretics on beetles (Lindqutt 1965.
Lindquist & Hunter 1965, McGraw & Farrier 1969, Kinn 1971. Moser &
Roton 1971. Lindquist 1972, 1975, Kinn 1987, Lindquist & Wu 1991).
MITES AND BIOLOGICAL CONTROL
The fim mite reported in the literature as a biological control agent ofa p a t was
not a phytoseiid mite - without a doubt one of the most usell of all tgnilies
of bioconml w t s - nor did it belong to any of the other families of
mites usually reporred as predators on economically important p h t s . Insread, a
 seemingly inoffensive astipatan, Hemisarroptcs maluc (Hemisarcoptidae), was
found faeding on the oyster scale & ~ ~ b eh s i on apple in 1868 (Gerson &
Smilqt 1990). Rather than being microbivores or parasites of insests or verre-
brans, as are most Astigmata, all species of Hmrirampta are predators of
armowed scales (Homoptua: Diaspididae). Mite eggs are laid u n d a scales and
larvae, non-dispersing nymphs and adults M on scab, especially ovipositing
f&de scales. Dcutonymphs are phoretic under the e l p of coccinellid beetles
(Chiloconcc spp.) (Gerson & Izraylcvich 1997).
Infochemicals
More recent advances in understanding mites as biological control agents have
b a n just as surprising as the original discovery of a predatory astipatan,
although in a quite di&rent manner, Any one who has watched a phytoseiid
foraging on a leaf might think that any encounter between predator and prey
was a ma- of luck, made probable only by the energy and persistence of the
predator. Phytoseiid mites, as in all Mesostipta, are bliid and lack the dis-
tinctive chemosensory solenidia characteristic of acarifbrm mites. Thedbre,
phytoseiid mites welt thought to sense prey only from short distances and pri-
marily by touch and contact chunoreception. However, it has now been con-
vincingly demonstram that not only do phycoseiid mites such as Pbytoduluz
pmimilis sense their prey lium long distances but they also respond to plant
volatiles that can call in the predators from f i r away (Didcc & Sabelis 1988,
Didrc e t d 1990. Vet and D i c k 1992, Bruin etaL 1995. Takabayashi & Dicke
1996. Didre et aL 1998).
The realisation that plants arc actively involved in their own defence should
not have been so unexpected; it is a direct prediction of aitrophic-level theory
(Price et aL 1980). Predatory mites inhabit a complex chemical landscape com-
posed of cues fiom plants, pests, competitors and conspccifics,and they must be
able to distinguish among these signals properly. While responding, mitcs must
negotiate a compla physical landscape that includes structures l i i leaf hairs,
domaaa and nectaries that are also, in part, priniuced by the plant for its own
defincc. The effcerivencss of phycoseiid mites as biocontrol agents is a function
not only of long-distance amaction to prey kairomoncs and arrestment within
patches of prey but also of the ability to recognise the information contained in
volatiles released by plants in response to damage by herbivores, to utilise plant
produced structures such as domatia and to navigate between other plant com-
ponents such as glandular hairs Walter 1996).
Induced resistance
Spider mites (Tetranychidae) arc major pests of grapes in most of the world's
vineyards but outbreaks arc often pmented or controlled by phytoseiid mites
(Hde & Sabelis 1985, Duso 1992, 1993). In Califbmia, however, Richard
Karban and hi coworkers at the University of California, Davis, have found an
unexpcctad interaction between two species of spider mites. Zinfandel p i p e s
that arc attacked by Willamettespider mites (Eomnmychus wiUammn) early in
the season are resistant to attack by Pacific spider mites (Tcmnycbuspm+)
Iater in the season-
- - --- --
W~Uamettemites fml primarily on grape, overwinter under bark and fbrm
small colonies with lide webbing on the upper surfgce of young leaves in early
spring. Damage to plants can be serious but often populations fad to reach
damaging levels and in the Gntral Valley of Caiornia W h e t t e mite is not
considered a serious pest. In conuast, Pacific spider mites am& a broad range
of plants, including many weeds, form large colonies and produce dense web-
bing that protects them both fiom chemical miticides and fiom all but spe-
cialised predators. Pacific mites attack grapes in the Central Vdey lam in the
season and thrive during hot, dry conditions and on mature leaves. Damage to
grapes causes the leaves to appear burned, leaf drop is extensive and yidd (sugar
l e d and fruit volume) is drasticdy reduced (Katban ct 1997).
Treating vineyards with broad-specaum miticides has been g e n d y inef- 1
feccive and has caused resurgence of Pacific and Wdamette mite populaaons.
Pacitic mite problems have bccome chronic and acute The use of chemicals less
disruptive to predator populations provides some help; however, Karban and his
coworkers fbund that the best method for controlling Pacific mite populations
was to avoid miticide applications and release Wlllameree mite in vineyardsearly
in the season. When chemicals are not used, Wlllameree mites caused lide dam-
age to grapes but these vines showed increased resistance to Paciftc mite result-
ing in Little or no Pacific mite damage. Although elevated predator populations
may explain some of this &, resistance to spider mite feeding i n d u d by
earIy season herbivory appears to be more important (Karban etd 1997).
Transgenic mites
Mites may be the fiat arthropod biocontml agents engineered using rcmmbi-
nant DNA techniques to be released into the field. The reasons fbr Jli preemi-
nence in a very &ntentious area of modern IPM are wo. First, an &nsive
body of work exists that shows that wild-type suains of many species of phyto-
seiid mites have been released over and over again without causing environmen-
tal harm (Hoy 1992). Second, Marjorie Hoy at the University of Florida and her
team have produced transgenic suains of Gakmhmw (= MetuseiucI*r) m&-
i d i s that are ready for release (Li & Hoy 1996. Presnail n aL 1998). Although
there is some concern that transgenic prcdaton will be used primarily fbr short-
term solutions, such as producing pesticide-resistant predators to augment
chemical control programs (Hoy 1992). the benefits to the environment of
reduced use of pesticides and deurased race of evolution of resistance to chemi-
cals in pests still will be substantial.
Biocontrol of weeds
Biological control of mite pesc by other mites is a common tool in many IF'M
systems and the use of mites against weeds appears to be a rapidly developing
field. However, the first demonstration of the potential of mitcs for biocontrol
of weeds was entirely by acciden~Prickly pear and other cacti are noxious weeds
in many parts of Australia,.ap#ially Queensland, where in the early part of the
twentieth century 25 million hectares were infesud. In 1924, however, the cac-
tus spider mite Trrmnychus durrtonrnr was discovered to be established and
spreading at a rate of 80 km per year. The spider mite soon besame a significant
control agent of the prickly pear Oprtntia inmis. Heavily i&ed plants pro-
d u d fewer fruit and prickly pear densities dropped 75% in parts of
Queensland. Although the desert spider mite looked to be the first example of a
good mite bioconuol agent of a weed, mite populations declined dramatically
 MITES O N PLANTS

when cactus moth (CutobLrcck spp.) populations devastated prickly pear
(Hill & Stone 1985). More recently, and deliberately, Tcranychrrr finteprius is
beingtested against gorse ( U . n r r o ' P ~in) New Z&land an2 Tasmania.
Rescad into spider mites as biological conuol agents of weeds has been
limited by the commonness of polyphagous crop pests and by the difEculty of
distinguishing species in che most promising p u s : T-chur (Andres 1983,
Cromroy 1983). However, because aiophyoid mites tend to be highly hosr spe-
cific those species that a d shoots and flowers, and so reduce seed set,or that
kill their hostr, are potentially excellent biological control agents. A good exam-
1
6 ple is the campaign against rush skeleton weed, Cho&& juncea (Asteracceae),
in temperate to semi-arid open scrublands in the western United States and
south eastern A d i a (RosentM 1 9 m .
Skeleton weed is a major weed in dryland wheat Farming in westem N o d
America and many pam of Australia. The wed, is an apomicric perennial that
overwinters as a rosette. In the spring the rosette bolts to produce a skeletal flow-
ering stalk which can yield over 20 000 winddispersed seeds. Even root frag-
ments can produce new plants. The rosafe reforms after autumn rains (parsons
& Cuthbertson 1992).
The skeleton weed gall mite, Aceria c h - is highly host specific The
mire attacks only skeleton weed and mites fkom diffuent areas of Europe p&
(or are Limited to) different strains of the ~ l a n (Carkhe
t & Wapshere 1974.
Cullen & Moore 1983). The mites overwinter in the rosette and ascend the stem
to the flower buds during the bolt. Summer generation dmes are around 10 days
and h a l e s form galls in vegctaave and flower buds that can reach 5 an in
diameter and harbour over 500 mites (Rosenthal 1996). At high levels of i n k -
tarion, seed production and plant growth are suppressed, apical development is
stunted and plant longeviry reduced. In Australia and the United States, skele-
ton weed gall mites have been released as part of a complex of n a n d enemies
that indudes a gall midge and a rust (Sobhian & Andres 1978. Cullen ct d
1982), and there seems to be general agreement that the mite is a useful part of
the complex. Other species of Ac& for example the lantana gall mite Ac&
lantanrrc, and a variety of other eriophyoid mites are being considered for use
against a variety of weeds (Cromroy 1983, Amrine 1996, Rosenthal 1996).
Many spider mites produce extensive webs and appear to have d e d a
subsocial level of colony organisation. Gall mites and wcb-producing spider
mites arr well protect4 h m environmental extremes but predatory mites are at
the mercy of wind, rain and larger predators on the phylloplane.
Predatory mites d y d out protected areas on leaves and many
species of woody plants have taken advantage of this behaviour by producing
idis of hairs and more elaborate pits, pouches, pockets and domes in their vein
axils. These mite-sized 'little houses' are called leaf domaria and extensive evi-
dence now arisrs to show d m the m i d e a f domatia assodation is widespread
and generally m u d y beneficid. Plants benefit because many plant-parasitic
mites are capable of ovcr-exploidng their hosts, strongly reducing reproductive
output and even killing large aces. However, a variecy of voracious predators,
especially phytoseiid mites, are capable of suppressing populations of plant
parasites. The mite-leaf domatia mutualism and other r e e d y discovered (or
rediscovered in the case of leafdomaria) bchavioural interactions between mites
and planrs hold promise for increasing the &ctiveness of n a d enemies in
agricultural systems.
Agricultural fields, however, have atypical acarohunas of low diversity.
Forests throughout the world are covered and completely infiltrated by a Fine
dusting of acarins. In undisturbed forests, fungivoes and scavengers dominate
this &ma, oficn at incredible densities. Given the antiquity of rhis association,
chue has been h e enough for interactions as intcrrsting as those berwecn
plants and herbivores and prcdatofi to develop. The discovery of the diversity
and abundance of mites in rainforest canopies is quite rrccnt, however, and our
state of knowledge about these animals and their associations can only be
described as near complete ignorance.

SUMMARY
During their long evolutionary association, mites and terrestrial plants have
developed a variety of interactions. Some seeds with sadcy, mucilaginous coats
are reported to trap sod mites but in general these interactions rang-from mum-
ally beneficial to severely detrimental to the plant Mite parasitism of vascular
p&a has evolved at least a dozen times, indluding a number of independent
colontations of plant reproductive organs by pollen- and nectar-fieedin%
mesostigmatans and by gall mites. Since these mites d i d Ya f k plant fitam,
they must be important selective agenrs. The Eriophyoidea, which indudes most
gall-forming mites, is the most succes&d radiation of acarine plant parasites.
Many f h s and most conifus and woody angiosperms arc hosts to eriophyoids.
Although the infktions often appear to be relatively benign, eriophyoids are
capable of scvcrely damaging or killing plants through heir own f d i n g and by
P-Msmission of d iplant viruses. In agricultural systems, however, it is usu-
ally the damage caused by spider miter that results in the most economic loss.
 T
o most non-biologists, a 'mite' is an almost invisible creature chat lives
1: A N I M A L S in the carpet and gives you asthma or that burrows in your skin to pro-
duce socially unacceptable scabies. Cat owners may curse the ear mites
that infest cheir pets and those who know that tick; are mites may men-
tion Lyme Dixase. Such medically important associations between mites and
mammals are discussed in most parasitology texts; therefore,-in this chapter we
cover ticks and ocher human- and livestock-associated mites superficially,concen-
trating instead on lesser known relationships becween mites and the animals they
use for room and board. These associations are not always negative; in h a , many
seemingly parasitic mites have no impact on their hosts or may even be beneficial
.
(see oaee 222).
I "

One of the recurring themes of this book is that mites live in the most aston-
ishing places. This is particularly apparent among animal-associated acarines. A
complete list of associations benveen mites and other animals would occupy the
entire chapter but to whet the reader's appetite we have providedTable 9.1, where
we list the associations that acarologists use to shock jaded students or to start con-
s dull parties. Afcer perusing this list many will be impelled to exclaim,
v e ~ d o n at
'What's a mite doing there?' or 'How did a mite gctthere?'. The first question is a
proximate one -what is the ecology of the symbiotic mite? -and the second an
ultimate one - what evolutionary history and selective pressures have resulted in
this association?In the first section of this chapter we discuss the ecological termi-
nology dealing with symbiosis and then outline some major hypotheses about how
different symbioses may evolve. The next two secrions discuss the life histories and
behaviour of mites associated with invertebrates and vemebrates respectively and
the fourth section surveys the diverse effects that parasitic mites have on cheir
hosts. Finally, the last section addresses the controversial topic of coevolution
becween hosts and syrnbionts from an acarine point of view.

TYPES OF ECOLOGICAL INTERACTIONS

One way to categorise the diversicy of interactions between pairs of individuals
is by the effect each has on the other's fitness. Box 9.1 depicts the categorisation
we will follow. Neutralism is a situation in which two interactors have no effects
on each other, positive or negative. Competition negatively affects both individ-
uals, while proto-cooperation and mutualism increase the fitness of both incer-
actors. Amensalisrn, although seldom discussed, is a common phenomenon in
which one individual is disadvantaged by another that is unatfected by the inter-
action (e.g. a mite is stepped on by an elephant). Commensalism occurs when
one individual benefits by associating with another, the host, and the host nei-
ther gains nor loses.
The final three categories, parasitism, patasitoidism and predation, can-
not be distinguished by differences in the effects that one individual has on che
other. In each case, one individual gains from the interaction (the parasite, par-
asitoid or predator) and the other loses (the host or prey). The difference
benveen the interactions is one of degree. A parasite does not kill its host in the
process of achieving its own fitness. Parasitoids and predators invariably kill to
achieve their ends but a parasitoid kills only one host in its lifetime (usually
slowly) and a predator kills more than one prey. However, these categories are
not always held to by the organisms they describe. A water mite larva may act as
 a parasite in one situation but in another, for example on a weakcr or smaller
host, as a parasitoid ~ikewise;%orn'lochim mites have no effect on their bury-
& beetle hosts in some circumstances (= &mmensaliim) but increase their fit-
nS1h s&=(-muruatism)-(seeTagc 222). In rhii chapter we will discuss
commensalism, mutualism, parasitism and parasitoidism between mites and
other animas.
Another way to categorise interacrions is by the location of the two individ-
uals. Symbiosis occurs when one individual lives in or on another. It may be a
highly integrated relationship, such as that between tree roots and mycorrhiza
fungi, or loose, as in downfish living among the tentacles of sea anemones.
Although sometimes used as if synonymous with m u d i m , symbiosis has no
necessary c o ~ o t a t i o nof being beneficial to both parties. The prefix 'ecto-' is
used fbr a symbiont that lives on the outside of its host (e.g. ectocommensal) and
'endo-' fix one chat lives inside. Phoresy is a pamcular type of symbiosis that is
defined by the function of the interaction - to allow a smaller individual (the
phoretic) to move fiom one place to another on a larger (the host or curia).
Despite the apparent simplicity of thii relationship there is controversy about
what constitutes phoresy (see page 210). A nidicole is an animal that lives in the
nest or den of another (e.g. dust mites in human habitations) and an inquiline
is a particular type of nidicole rhat dwells in the nests of social ins-.
EVOLUTIONARY PATHWAYS BETWEEN
INTERACTIONS
The nature of ecological relationships between taxa is fluid over time. For exam-
ple, within the liespan of our own species the parasitic relationship between
humans and the honey bee Apis m c I l r i has~ become primarily mutualistic. We
benefit fiom the bees' produaion of wax, royal jelly and honey and from their
- services as pollinators; the bees benefit fiom our protection, custom-built hous-
ing
- and worldwide distribution.
Longer term evolutionary change in symbiotic lineages may result in more
BoxQ.1 T ~ ~ O F ~ ~ ~ ~ ~ * ~ ~ ~ F ~ ~ B E N I E ~ J ~ I N M Y ~ W I U J . U T E G O R ~ S E D Many
~ W t ( E N T H E Y A R E ~ N G C O M P A R m T D W B V T l i E Y A RNOT
E
EfFece on fltness of A and B
when not i*raeting when intersctlng
specialised behaviours in derived taxa but with early types of interactions still
exhibited by primitive taxa. For example, some derived species in the
Proglyphidae (Astigmata) arc parasitic on the skin of birds, while others retain
the ancestral relationship of being dctritivorous in b i d ncscs (OConnor 1982).
In many symbiotic taxa, however, free-living relatives are either extinct or
unknown (e.& fbr lice, fleas, ccstodes). In contrast, non-parasitic relatives of par-
asitic mites are common (eg.Tteat 1975, Radovsky 1985, Houdc & OConnor
1991). Closely related taxa that exhibit a variery of ecological relationships allow
the testing of hypotheses about the direction of evolution (e.g. )horsy leads to
parasitism') and about fbrccs behind such changes.
Water mites, in which related parasitic and non-parasitic species ofien co-
occur, arc a particularlygood group for testing such hypotheses. Some other taxa
also show evidence of repeated gains or losses of parasitism (e.g. leeches. Siddall
& Burreson 1995; copepods, Poulin 1995), but mites provide the most numer-
ous and dearest examples of switches in liestyle. It is therefore strange that
acdcologists have produced no phylogcnedcally based compamtive tests of the
fbrces sdecring fbr and maintaining parasitism. Evolutionary narratives are com-
mon (e.g. H o d & OConnor 1991) but dadogams demonstrating that pur-
p t c d causative fgaors did indead precede hypothesised m l t s are absent. So
the fbllowing scenarios are what some scoffers might refer to as adaptationist
story-dbg (Godd & Lcwontin 1978) but they arc actually hypotheses waiting
to be tested. It is also important to note that these categories are not mutually
d u s i v e but-simply -nt ways of subdividing the literature into themes.
Cohabitation predisposes mites to parasitism
Waage (1979) suggested rwo types of evolutionary routes to parasitism. In Type
A, adaptations fbr association betwecn the parasite and host preceded adapta-
tions for keding. In Type F rouus, adaptations rhat would eventually allow feed-
ing on the host p d e d adaptations for association. Parasites that evolved
through the A pathway typically have free-living nidicolous relatives and dearly
have secondarily evolved mouthparts adapted to M i n g on host products (e.g.
blood). Followers of the Type F pathway had the right mouthparts in the first
place but only secondariiy developed an association with the host.
BTTH EERE
authors ~ ~ S Olineages
describe N of parasitic mites evolving from nidicolous
ancestors (Type A route). Moss (1979) presumes that the ancestral
harpyrhynchid evolved fium cheyletid-lii nestdwelling predators. Kim (1985)
suggests that the ancestors of muostigmacans parasitic on mammals and of
w i d ticks were originally nidicolcs that fed on wastes and remnants of the
host's me&. Fain and Hyland (1985) suggest that parasitic psoroptoids (in
mammals) and andgoids (in birds) probably arose from nidicolous
Pymglyphidae.
Unionicolid water mites may have bllowed a diffkrent Type A route. W at u
mites, like all members of the Parasitengona, have avo calyptostatic instars
(proconymph and mtonymph) that act as immobile 'pupal' stages separating the
active brva, deutonymph and adult. In the genus Unwnir& che calyptosratic
instars are spent embedded in the well-aerated tissues of other animals, primari-
ly sponges and mussels. For species associated with sponges, the relationship
pno fiuther than housing during these rransfbnnation stagu. Some mussel-
&red species (termed 'temporary mussel mites' by Hevers 1980) & have
this relatively benign interaction, and deutonympk and adults are free-living
 MrTES: ECOLOGY,
EVOLUTION
A N D BEHAVIOUR
predators in the water column. But other Unionicokz species are parasitic on
mussel tissues in their p o s t - I d stages ('permanent mussel mites' s t n n r Hevers
'
1980). Perhaps further study on the ecology of these mites will dunonstrate an
. additional, transitional type of Uniaicokz that dwells in mussels but f;esds on
zooplankton drawn in by the host.
I Dietary adaptations precede parasitism
I
204
What of W q ' s (1979) Type F routes? Radovsky (1985) k l s that mesoscig-
matic mites a z morphologically preadapred tor parasitism and that the switch
from a free-living to a parasitic l i t y l e is often accompanied by only slight phy-
ical changes. The typical chelicerac in &-living Mesostigmata have muscula-
ture that can be used for penetration, are very dose to the shape of a piercing
stylet and require litde modification to perform like the mouthparts of blood-
sucking insects. However, d i k e dassid Type F examples, such as the evolution
of blood-sucking by nectar-sucking mosquitoes, these mesostigmatans Likely
went through a period of dose association with their eventual hosts.
The Parasitengona parasitise both vertebrates and invertebrates and likely
evolved from mites in the Anystoidea that had k - l i v i n g predatory larvae
(Wiggins ctaL 1980). The transition from a predatory to a parasitic relationship
could have becn made by the mite larva feeding on large prey that remained
motile and was not necessarily killed by the feeding activicy. W e n s et aL
(1980) suggest that the advantages of transport conferred upon such larvae
would select fbr parasitism.
Phoresy precedes parasitism
Phoresy appears to have hvoured evolution towards parasitism in several lineag-
es of mites (Athias-Biiche 1991, 1995). Treat (1975) considers that many
instances of parasitism in mesostigmatans associated with Lepidoptera arose
from phoretic associations. Phoresy in these moth mites may have originated as
accidental sturnblings upon by the mites, which benefited from the transferral.
Some mites combine phoresy with occasional parasitism. Treat quips (p. 89) 'a
mite, normally predatory, attaches itselfto an kas a phoretic ... During irs
ride it taps its host for a light snack. Is it on its way to a career of crime? Perhaps
so. Even among moth mites it is not always easy to tell a hitchhiker from a
hijacker.'
Treat W ht the transition fiom phoresy to parasitism is particdady appar-
ent in Blatcimks (Ascidac). The hypothetical a n d cype can be represented by
BI;rttisocirah r ( m h i c i n r r and B. Recgani, which have been collected h m nesn of pack
rats, various plants and animal, and from the tympanic recesses of moths Closer
to parasit@ is BLzttirociuz rmrrJi which eats the eggs of several species of moths.
Funale mites are phoretic on the adult moths. Treat blind that in most cases, there
was no evidence that B. kusaliikd uvon its hm, however, he sometimes obscrvcd
scars on the moths and mites app-tIy in the act of k g . ~ i & & there is
BI;tffliron'uspa*zgiO- in which &nphs-and adults of both se& occur on moths,
'.
fbed on haemolvmvh and can mroduce without anv other fbod
When present, the asti&- deutonymph'is typically a non-feeding
phoretic stage but a fiw have become parasitic (OConnor 1982). Athii-Binche
(1991) suggests that endotollicular hypopi (e.g. in the Hypoderoidea), which
appear to gain weight while in the follicle, came ftom purely phoretic hypopi,
Houck and OConnor (1991) and Houck (1994) describe how deutonymphs
of H ' o p p r a e o o m ~ n(Hemisarcoptidae)
i appear to be in the midst of a tran-
sition from phorcsy to parasitism. In all members of this genus, free-living stages
are predators of diaspidid scale insects and deutonymphs are transported bybee-
tles in the genus ChiCororus (Coccinellidae). Deusnymphs-of H. cuorcmrlni Swell
up while on their host C axtiand cannot d-dop to tritonymphs ifthey q m o t
allowed this association. Deutonymphs stay on the hosts for 5-21 days which
'cannot be completely explained by the need to disperse because it also occurs
when resources arc p l e n W . Haemolymph from reflexive bleeding of the host
frequently bathes the subdyual zone where the deutonymphs reside but the caus-
tic fluid does not harm them. Radio labelling showed that substances move fi-om
beetle to deutonymphs, apparently duough the attachment sucker. The authors
suggest that the interaction has changed &om the serendipitous use of reflexed
haemolymph controlled by the host to the deutonymphs exrracting fluids as
required. Somewhat teleologically thiy state that 'the ultimate evolutionary sig-
nificance of the dcutonympM morph is to serve as a transition from a free-living
existence in temporary environments to a more stable parasitic existence' Athias-
Binche (1995) considers that the honey-bee parasite Vmn,ajacobzonialso evolved
parasitic tendencies via a phoreric roue, with paraphagy (flxding on host cxu-
dates or secretions) as an inurrnediate step.
Loss of parasitism
Radovsky et aL (1997) report that an undcscribcd species from the
Macronyssidac, a M y otherwise composed of parasites, is a voracious preda-
tor of other mites that live in the guano that coats bat caves. Based on its mor-
phology, the mite is clearly derived from parasitic ancestors and the authors state
that it rcprcscnts 'a rare and hitherto undocumented evolutionary shifi from
~arasitismto reda at ion ...' It is not the onlv case however. as A. Wohlanann
notes (pus. comm.) that larvae ofJohnrtoniana mpax Uohnstonianidae) and a
few species of Abroloph (Erythaeidae) are predatory. Both are from the
Parasitengona, a group characterised by parasitism in the l a d stage. Another
example of a dietary shift is that of larval Balauztium (Erythraeidae) that have
switched from the normal parasitic behaviour of eryrhraeid larvae to feeding on
plant fluids and pollen (Newcll 1963).
Although there are fkv camples of lineages in which a particular lil-history
stage has switched fiom parasitism to predation or herbivoy, there are many
instances in the Hydracarina in which kedhg in the larval stage has been com-
pletely suppressed. Smith (1998) lists 29 species of water mites from 8 &dies in
which the larva is not parasitic Larvae either dose, swim about brieAy and then '
eransfbrm m the cilyptostatic promnymph without feading, or aansfbrm to the
protonymph without dosing at all. Smith feels that loss of l a d parasitism has
evolved at least 21 times. Non-parasitic species can often be matched with closely
related species that produce parasitic larvae,suggestingthat while loss of parasitism
is an ongoing process, it is unlikely to lead to discina li&ages of non-parasitic
species. Such spades pairs may be so morphologicallysimilar as to be confUsod tor
a single species (eg. Davids 1997a). In the t a m s t d Parasiangona, o d y one
example of suppression of larval &ding is known, in a species of AICothrombium
(Trombidiidae) (Smith 1998). It is not dear whether chis propensicy to dispense
with parasitism is a true dfirence beeween temmial and aquatic parasiangones
or w h d e r it d e a s a paudcy ofsrudia on land-dwdling species.
 Why have water mites repeatedly given up parasitism? O r more generally,
what would lead to the suppression of a feeding stage, especially one that also
serves as a transport stage when on a flying host?
Suppression of a fcodiag h e has evolved repeatedly in marine inverte-
brates (Strathmann 1978). Species producing smaller eggs tend to have larvae
rhat &ed for a rclativsly long time while drifiing in the plankton. Species that
produce large, yolk-rich eggs tend m have non-f$eding, non-planktonic h e
that rely on yolk reserves for development. Lampreys (Agnatha) are another
example of a taxon in which a parasitic stage is sometimes skipped (Youson &
Beynish 1991). Smith (1998) points out chat certain characteristics of lampreys
-
and marine invertebrates that have given up juvenile foeding relatidy larger
eggs and smaller size at adulthood - are shared by water mites with non-feed-
ing lame. So as well as giving up transporr, non-parasitic water mites tend to
produce h e r , larger larvae per dutch (Cook et czL 1989, Davids 1997b).
What ben&t could possibly outweigh loss of dispersal ability and r e d u d
fecu~ldity?The riskiest stage in the life cydc of a water mite is likely m be the par-
asitic one, as the probabiiry of finding a host and then succDsfuly detaching over
water appears to be quite low. Collins (1975) estimates that most mortality of
Wan&& && occurs in dre transition hom a s e a d i n g to a parasitic luMI
only 10% of larvae s u c c e s s ~ yencounter a brine fly, avoid its d&nces and leap
onto the host. A larva may encounter only one potential host in its &pan.
Meyer (1985) calculated the host-finding success of Hy&dn,ma d;rpititnr larvae
(Hydrodromidac) in a Zakc in Germany. Only 2060 of 181 500 mites attached to
ahos~ an astonishing mortality of 98.9%. So within a given body of warn, pro-
duction of bnnc with a %on-parasitic' strategy would result in greater fitness for
a h a l e water mite than would production of parasitic lvvae. Collins (1975)
suggests rhat Wan&& tbrrntalis has not abandoned parasitism, even though it is
so risky, because the hot-spring pools they inhabit are so ephemeral that it needs
the flies more for dispersal than fbr nutrition.
How much energy does a larva gain through parasitism? For water mites, a
larva may increase its volume from 3- to 600-fbld, depending on the species
(Smith 1988, Davids 1991). For some species of Eykzu (Eylaidacj, the larval
nutrition provides up to 45% of the adult body mass. In terrestrial parasiten-
gones, the range of increase during parasitism is 10- to 576-fold in fresh weight
(A. Wohltmann, pen. comm.). Thus m an Eyhu Lnn, foregoing parasitic feed-
ing would have a greater &kt on fitness than it would for many Unionicolb or
Limnesk larvae, whose volume increases less than 5-fold.
The above leads to the prediction that loss of parasitism should be more like-
ly in water mite species that (a) live in stable habitats and (b) have larvae that
engorge little during their parasitic phase. However, Smith (1998) found no evi-
dence that water mites that have forgone parasitism inhabit unusually stable
habitats; in fict, some eyen inhabit temporary pools. There is indirect evidence
for (b). None of the water mites in Smith's list arc fiom the f$milies
Hydrachnidae or Eylaidae, the taxa in which larvae show the greatest engorge-
ment. Most are concentrated in the Hygrobatidae, Limnesiidae, Pionidae and
certain subgenera of Arrenuridae. These taxa arc primarily parasites of small flies,
on which the larvae spend only a few days and engorge little.
The lack of non-parasitic lineages in water mites and the commonness of
related pairs of parasitic and non-parasitic species suggests that while non-para-
sitism is beneficial in the short term, it is a dead end in the long rum Lack of
dispersal may doom non-parasitic Lineages to extinction through loss of habitat
or deleterious inbreeding. To test the latter idea, Bohonak (1998) collected over
1100 Amnunu from five parasitic and three non-parasitic species from southern
Ontario and New York. He divided the parasites into three categories of poten-
tial dispersal ability: mites on odonates were ranked as having greatest dispersal
potential, those on mosquitoes second and those on midges third. Non-parasitic
ones were last. He predicted that heumqgosity would be higher in more wide-
ly dispersing species. In general, these species did tend to possess higher average
heterozygosities than poorly dispersing species; however, the rank correlation
with dispersal ability was not significant. Bohonak also found little evidence of
population differentiationamong non-parasitic species, even across hundreds of
kilometres. He suggested that time since glacier reueat had been insufficient to
allow genetic differentiation of the populations.
Is there evidence of life-history flexibilitywid& a single spccies?Two species
of water mites have been reported ,?produce &rent sizes of eggs. Crowell
(1960) fbund that one 'fbrm' of Thas mIli (Hydryphanadae) produced eggs
with an average diameter of 0.142 mm and another form pioduced fnvcr, 1 ~ -
er eggs with diameters of 0.24 mm (volumes 1.5 and 7.2 x10-3 mm3 respecuve-
ly). B6-r (1962) observed that fernales of Piom n o h (Pionidae) lay two
difkrcnt sizes of eggs. Well-fkd females held in warm water laid eggs about 0.27
mm in diameter. He held the same females for G weeks without food at 5 4 ° C
and when they were brought up to room temperature they laid small, yolk-poor
eggs of about 0.19 mm in diameter. From the big eggs hatched big larvae that
uansfbrmed into protonymphs without having to undergo a parasitic stage. The
small eggs produced small larvae that died after 10 days without a host. Btittger
suggested that afier winter, &males produce small, parasitic l a m e and that dur-
ing the summer they product Iargc, non-parasitic ones. It may be that such a
phenotypically plastic 'mother' species gives rise, perhaps repeatedly, to non-par-
asitic daughter 'species' that repeatedly go extinct.
Loss of phoresy
OConnor (1982) mentions that the astipacans G&cyphagus domesticus and G.
destructor are stored-product pests with 'inert' deutonymphs that are dispersed
by wind rather than on a host. Likewise, Acanrs species that live in nests nor-
mally have deutonymphs phoretic on fleas but this stage has been lost in stored-
product species. Some astigmamn associates of beetles that remain on heir hosts
for their entire life no longer express the deutonymph (Eidcwort 1983). The 30
findies in the p u p Psoroptida, permanent symbiontsof vertebrates, also have
lost the deutonymphai stage (Houck & OComor 1991).
OConnor (1982) considers that the repeated loss of the phoretic deu-
tonymph in the Astigmata is correlated with permanently parasitic lifestyles and
with the transition h m living in ephemeral rcsourccs to life in stable, wide-
spread habitats, such as litter and soil. In such situations, rransport via phoresy
would be less us&d or even disadvantageous. A supporting example is that of
the pitcher-plant dwelling astigmatan Sarrclcenwpru (Hisaostomatidae). The
Sammirl pitcher plants typically occur in colonies in peat bogs. Deutonymphs
of Sam~rniopurmove h m aged pitchers to new ones by waking (OConnor
1994). Although deutonyrnphs retain the physical modifications fbr phoresy
and may occasionally use these tbr long distance dispersal, most migrate to other
pitchers of the same plant or nearby plants. OConnor (1994) suggests that an
 MITES: ECOLOGY.EVOLUTION
A N D BEHAVIOUR
Parasitengona comprises 7000 named species placed in more than 50 h i l i e s .
Its members are termed protelean parasites, meaning that the l a m e are parasitic
but the p o s t - l a d stages are free-living predators. Larvae of two of the tenstri-
al f k i i e s . Leeuwenhoekiidae and Trombiculidae, and of one t g n i y of water
mites, Thermacatidae, are parasites on vertebrates as larvae but those of the
remaining groups parasitise arthropods. AU major orders of insem and arach-
nids have been described as hosts (Welbourn 1983), including other parasiten-
gones (Wendt et d. 1994) @gute 9.1). In a k w Families of water mites, the
p o s t - l a d stages are parasitic on freshwater mussels, snails, crayfish and l a d
mayflies. A few species in the mainly marine group Halacamidea are thought
to be parasitic on crafish, sea urchins, nemerteans and hydroids. The fiery-
gosomaridae parasitise scorpions, codnoaches and reduviid bugs, as well as r e p
tiles. Some Ercynetidae are parasitic on terrestrial slugs (Baker 1970).
When the Astigmata arose within the Oribatida (see page 91). one of the
changes in l i history was a specially modified deutonymphal stage, the hypo-
pus, adapted tbr phoretic dispersal on in- (OConnor 1982). Although
numerous lineages of Astigmata have become permanently associated with
mammal and b i d hosts, there are many fsmilia that still show the ancestral
association with arthropods. Beetles, bees and wasps are fi~ouredLhosfs,and
carry deutonymphs of Acaridae, Glycyph+daie -Carpoglyphidae, Chaeto-
dactylidae, GaudicUida2, Platyglyphidac. Canesmniidae and W~ntersdunid-
riidae. Other phomic hosts indude dipterans and lepidopterans.
Many asdgmamns assodated with bees and wasp bein-the-nests of their
hPZi@ean-be+, act-as-coGmLm~ds,m~tualists>~zi%ires
(c.g~WiIitersdunidtiidae).The-Ewingiidiie live in the gills and vasa deferentia of
pagurid land crabs but their feeding ecology is unknown (OConnor 1994).
Some species in the Histiostomatidae are found in the egg cocoons of freshwa-
ter leeches and terrestrial earthworms; likewise, a histiostomatid and an acarid
species have been found wandering on the epidermis of a freshwater leech
(Proctor ct aL 1997). For these annelid-associated astipatans, it is unclear
whether the relationships are predatory or parasitic, or whether the mites feed
on associated microbes. Most of the invertebrate-associated astiginatam appear
to have purely phorctic relationships with their hosts but there are exceptions.
Deutonymphs of Hnnrjarcopw c o o m n i (Hemisarcoptidae) are reported to be
parasitic on their host coccinellid beetles (Houck & OConnor 1991). The epi-
dcrmoptid M%CS ntrvdonaldi is hyperparasitic on hippoboscid flies, them-
selves parasites of birds (Kana1978).
Phoresy and dispersal
Acarologists have been long fascinated by phoretic associations between mites
and other invertebrates and there are numerous reviews of chis phenomenon in
mites in general (e.g. Binns 1982, Athias-Binche 1991, 1995) and for pamcular
tam (e.g. Hunter & Rosario 1988, Houck & OConnor 1991, OConnor 1994).
The term 'phomsy' has a history of controversy. Many definitions have been pro-
p o d and none has yet been accepted by all acarologk. In 1971. Euish and
AmcU restricted phoresy to d r to attachment of one animal to another only
when attachment was temporary and actively sought with neither W n g nor
ontogenetical changes taking place during attachment. Athias-Binche (1991)
uses a similar definition but states that while on the host, the phorecic is '+a-
cent'. Houdc and OConnor (1991) dislike the stipulation of 'actively seeking
1 hosd because deutonymphd astigmatans may be stationary while waiting for a
hosc to pass their way. Their more complex definition is that phoresy occurs
when 'one organism (the phoretic) receives an ecological or evolutionary advan-
tage by migrating fiom the natal habitat while superficiallyattached to a select-
ed interspecific host h r some pomon of the individual phoretic's lifetime'. An
additional requirement of Houck and OConnor is that the phoretic cannot ben-
efit nunitionally or developmendy while on the host.
To continue the tradition of tailoring phoresy to one's own p r e b c e s , in
this book we use a verbally simpler definition: phoresy is a rype of temporary
symbiosis whose function is to allow a smaller individual (the phorecic) to move
from one place to another on a larger individual (the host or carrier). This defi-
nition allows phoretics to make more than one use of a host For example, the
pseudoscorpion Co.4yCochrmcs sco*pioicicz (Chemetidae) dispuses fiom its nor-
mal habirat of decaying aees by riding on giant harlequin beetles (AEI.otnuclongi-
manus, Grambycidae) (2% & Zeh 1992). While on the host, they f d on mites
also riding the beetle, and male pseudoscorpionsd e h d territories and mate with
females. Feeding and mating activities on the host would eliminate C srwpwidu
from the category of phoretic in the other definitions but none of rhe abow
authors would deny that the primary benefit received by the pseudoscorpions is
transport to new habirats. Similarly, water mites rhat are a;msporccd between
water bodies as parasites benefit from the aansport, as they have no other means
of moving overland between aquatic habitats. Even deutonymphs of Pamilochinu
c a d i (Parasitidae), Eunous examples of phorecics, sometimes feed on nunatodes
or oral secretions of their beetle hosts (Brown & W h n 1994).
An example of somethiig that is sometimes called phorcsy (e.g. in Arh'tas-
Binche 1991) but does not meet our criteria is the proparasitic attendance
shown by water mites, in which larvae atrach non-parasitically to a juvenile
insect and wait until the adult insect emerges. It is not phoresy because there is
' no loss of fitness to the mite larva if the juvenile insect does not move during
this period Water mites that parasitise adult black flies (Diptera: smuliidae)
associate with the sedentary pupae beforehand. Likewise, larvae of terresmal
'
parasitengones in the h i l i e s Johnsronianidae and Micmchrombidudae attend
i m m o b i pupae of their dipteran hosts tbr up to 23 days (Wohltmann 1996,
Wohltmann & Wendt 1996). ClearIy, no uansport benefit of association is
accrued in these cases. In this section we will concenrrate on mite caxa that gain
no apparent benefit fiom phoresy other than transport, and will discuss phoret-
ic parasites and mucualists in subsequent secrions.
What is the value of phoesy? The shott-term benefits probably indude
escape from physically deteriorating habitats, emigration from ovucsowded
natal sites or transport to new sources of food. Phorecic species are especially
common in ephemeral and patchy habitats such as rotting wood or fruit, dung,
hngi, carrion, and tempomy water bodies (OConnor 1984a, Hunter 8r
Rosario 1988). In contrast, mites in continuous and relatively constant habitats.
such as leaf litter and tbliage, rarely show adaptations b r phorgr. It b interest-
ing to note that species of Simpses (Pymephoroidea) that feed on grass-associ-
ated fungus - a continuous resource - have no phoreac phase, whereas those
that feed on patchily distributed fungi disperse p h o ~ t i c a l(OConnor
l~ 1984a).
Being small, wingless and having sense organs with a limited range, mites that
live in ephemeral habitats benefit from associating with larger a n i d that can
move h t h e r , Faster and can detect appropriate sites fiom a greater distance. For
 example, under its own power the astigmat.an Cafog&phtcc rodionouican walk only
5.2 mm in a minute (Binns 1982), while as a deutonymph phoretic o n a winged
insect it can cover 1000 times the distance in the same time. Long-term benefirs
of dispersal and migration by phorcsy include prevention of inbreeding and
access to new areas for colonisation (e.g. oceanic islands, Athias-Binche 1995).
Examples of phorecic relationships with invertebrates can be found in all
acariform suborders and in the Mesostigmata. Typically, only one life-history
stage is phoretic in a given species. In the Astigmata the phoretic stage is the deu-
tonymph, while in the Prostigmata it may be the fertilised adult female (e.g.
212 Pygmephoridae), the larva (e.g. Parasitengona) and, in one case, the tritonymph
(Erynetcs sp., Ereynetidae) (Zhang & Sanderson 1993). In Mesostigmata, deu-
tonymphs arc phoretic in Sejina, Microgyniina, Uropodina, Parasitina and early
derivative Dermanyssina (e.g. Digamasellidae). In the Trigynaspida and derived
,. , females) are the ~horetics. Mitchell (1970)
Dcrmanyssina, adults (typically
points out that when dispersal occurs prior to mating, in order to be fairly cer-
tain (87.5%) that at I w t one individual of both sexes are present, at least four
mites must meet after phoretic migration (assuming equal sex ratios and proba-
bilities of dispersal). Hunter and Rosario (1988) note that for Pararim spp.
(Parasitidae) on bumble bees, mites that disperse prior to mating tend to do so
as groups rather than as individuals. Zhang (1992) suggests that Allothrombizm~
prrlvirzun (Trombidiidae) larvae parasitise already parasitised aphids (superpara-
sitism) in order to increase the chance of finding a mate in the new habitat. This
may be a general explanation for the clumped distribution of larvae o n hosts typ-
ically observed for parasitengone mites (e.g. Smith 1988).
T h e phoretic stage may be specifically modified for transport on the host
(Table 9.2). The best known of these is the astigmatan deutonymph, often
9.2
TABLE M m TAXA THAT HAVE STAGES tiOD(FIED FOR PHORW (EXCLUOING P A R A 4 K IAXA)
Taxon Stage modified Modifications
Uropodidae dcutanymph anal ped~celin some spp.
Ascidae i? phoretomorph body Raper and broader, integument
(Antennosews jonus)
and setae smoother than non-phoretornorphs
Asti'gmag dwmnyrnphs reduced kegs and mouthpara, dorsovenual ft-ing.
increased xlemtization, attachment structures
(sucken, claspers)
termed the hypopus (plural hypopi). Hypopus was originally a genus name
applied to strange, flattened rnites with reduced legs that were found artached to
insects. later it was realised that these mites represented a stage conlrnon to
many asrigmatans. T h e phoretic deutonymphs of astigmatans have a variery of
modifications, in part dependent on the host taxon. Entomophilous forms
attach to arthropods using a caudovenrral sucker. Pilicolous forms have reduced
suckers but use a different ser of modified setae co auach ro insect setae or to
mammal hair. In cndofollicular rypes, living in the skin of birds and mammals,
artachment oreans are highly
" " , reduced or absent (Houck & OConnor 199 1). I
, Hypopi lack functional mouthparts and resemble neither the preceding 213
protonymphal stage nor the subsequent tritonymphs and adults; they are thus
termed a heterornorphic stage. Larvae of Parasirengona are both parasitic and
phoretic, and are also extremely heteromorphic relative to the subsequent stages.
The most highly modified of mesostigmatan phoretics are the heteromorphic
deutonymphs of families in the Uropodina. As the name implies (uro = tail, pod
= foot), most uropodines attach to their arthropod hosts by a stalk secreted from
the anus, although others use caudal suckers, claws or chelicerae.
Expression of the heteromorphic stage may be facultative. In the Astigmata,
the phoretic dcutonymph is often skipped, with protonymphs transforming
directly to the rritonymph. A few species of water mites may have facultatively
non-phoretic (and hence non-parasitic) larvae (see page 205). Many species in
the Pygmcphoridae and Scutacaridae (Prosugmata) have two types of females,
one that is not phoretic and another that is the phoretomorph (Moser & Cross
1975, Eberman 1991 a, b). The srolyti species group of Pyemotes (Pyemotidae)
has phoretomorphic males and females (Krana 1978). In these taxa, phoreto-
morphs are distinguished by enlarged tarsal claws on the first pair of legs, used
to cling to the host, as well as other characteristics (Table 9.2). Binns (1982)
notes that phoretic morphs of many different taxa share similar morphologies:
dorsoventral flatrcning, oval or circular bodies and flanges covering all or some
appendages. This convergent morphology may serve to reduce loss of moisture
when on the host and to present a smooth dorsal surface making it difficult for
the host to remove rnites by grooming.
The striking differences between phoretic .md non-phoretic females has
often resulted in a single species being described as two separate spccies. The
most confusing situation, termed by Lindquist (pets. comm.) 'a taxonomic and
nomenclatural can of worms', is the Pediruhter-Siteroptes dyad. Members of the
genus Pedicularter (typically placed in the Pygmcphoridac) appear to be phoret-
ic morphs of Siteroptes species. As the genus Siteroptes is often placed in its own
family, Siteroptidae, the confusion is at both the generic and familial level. Cross
& Kaliszewski (1988) sidestepped the problem by simply describing Pcrlarhtcr
firhnnanni as a member of the Pygmephoroidea, a superfamily that includes
both contentious families. Similarly, there is one known example of phoreto-
morphy in the Mesostigmata, the ascid Antennoseizu janus (Lindquist & Walter
1989), in which the phoretomorph and homeomotph were originally thought
to represent different species.
Photcric phases may lie in wait for passing hosts or they may actively seek
them out (Binns 1982). Deutonymphs of Histrostoma Iaboratoriunz
(Histiostornatidae) adopt a characteristic 'questing' posture in which they stand
on their third and fourth pair of legs with their bodies propped against their pos-
terior margins, gently waving rheir first and second pair of Iegs. Should a host
 MITES: ECOLOGY.EVOLUTIONAND BEHAVIOUR A N I M A LAS
S HABITATS

exchange for the attractive secretions. What the housing of these foreign species that have extensive contact with the water as adults (Coleoptera) or as both lar-
indicated was not stupidity on the ants' part, argued Wheeler, but simply a result vae and adults (Hemiptera), and do not show prolonged pre-parasitic atten-
of the habit of trophallaxis. He provided a litany of social evils in human life that dance. Few families and fewer orders of aquatic insects escape water mite
had parallels in ant societies (p. 197): 'We not only tolerate but even foster in parasitism. The exceptions are the Ephemeroptera (mayflies) and Megaloptera
out midst whole parasitic trades, institutions, castes and nations, hordes of (dobsonflies, alderflies). These exceptions are readily explained by their excep-
bureaucrats, grafiing politicians, middle men, profiteers and usurers, a vast and tional life histories. Mayflies are the only order of insects to display a winged
varied assortment of criminals, hoboes, defectives, prostitutes, white-slavers and moult, from the subimago with its heavy opaque wings, to the imago, with its
many other purveyors of antisocial proclivities...'. lighter, more functional wings. These secondary moults would likely dislodge
It is possible that the myrmecophilous oribarid Aribntesjuvmis (Aribatidae) any mite larvae that had attached to the subimago. Megalopterans and species of
6 is one such intoxicating inquiline. Itu and T&u (1974) feel that these rotund Neuroptera that inhabit water (spongilla flies, Sisyridae) are holomecabolous 217
mites are completely dependent on Mymerim ants for transport, food provision insehsthat undergo their pupal stage in cocoons or chambers on solid ground.
and care of their eggs. T h e mites do not walk on their own and are carried from The adults do not return to water except to oviposit and there is little opportu-
nest to nest by the ants along with the ants' own brood. The ants regularly lick niry for a mite larva to contact a host.
the mites, each mire being groomed up to eight times per hour. Presumably, the
mites produce a tasty exudate that Mymecinu enjoys. Mite eggs are removed
From the oribatids' ovipositors by the ants, licked and placed together with the
ants' eggs. Itu and TBkaku did not observe trophallaxis between Aribates and
Mymerim and assumed that mites feed on fungus growing in the nests. Mites
maintained without ants died within six days but those with ants lived more
than four times longer. The author's statement that the mites are unable to walk
on their own is somewhat puzzling given that they found both males and
females in ant nests. W ~ t hone known exception (see page 67), oribatids trans-
fer sperm by depositing spermatophores on a substrate; it is difficult to under-
stand how immobile males and females would be able to mate.

Parasitism and parasitoidism

As we have stressed above, the difference between being phoretic or commensal
and being parasitic is nor necessarily large. Phoredc mites may not interfere with
a host's locomotion when in small numbers but may seriously impede the host
when abundant. Commensals may be innocuous when food supplies are in
excess but become debilitating kieptoparasites in lean times. Parasites may cause
no more than a momentary itch or they may greatly weaken the host. However,
because parasitoids invariably kill their hosts, they can be nothing but ememe-
ly bad. In this section we describe the ecology and behaviour of selected groups
of mites that have clearly negative effects on their invertebrate hosts.
(a) Parasitengona Figure 9.2
A chigger or s w b itch mice (Tmmbialidae).a vcrtcbare-biting pamsirengone larva
The Parasitengona is the largest group of mites that have parasitic relationships
with invertebrates. Although we may be more familiar with the chiggers and
scrub itch mites that bite vertebrates (Figure 9.2), the vast majority of parasiten- Insects arc not the only hosts of parasitic water mites. Postlarval stages of
gones have larvae that attack arthropods. Welbourn (1983) details the host-par- some taxa parasitise mussels and snails. The Astacocrotonidae have been
asite relationships of terrestrial members of this cohorr, and Smith and Oliver described as parasitic o n the gills of a freshwater crayfish. There are also isolated
(1986),and Smith and Cook (1991) those of the aquatic ones (Hydracarina). reports of postlarval water mites parasitising fish, either in their digestive cram
Other than host associations, lirtle is known of the parasitic behaviour of the for- (Cupp and Willis 1982, Yankovskya & Fernando 1982) or on their gills (Tedla
mer (but see Wendt rt al. 1994, Wohlunann 1976, Wohlanann & Wendt 1996). and Fernando 1970). Rather than these instances representing parasitism, it
In conrrast, there is a great deal known about the behaviour and ecology of water seems more likely that the mites were swallowed by the fish and remained undi-
mite larvae, at least those in Europe and N o d America gested in the first case or tried to crawl out through the gills in the second.
Water mite larvae primarily parasitise the adults of freshwater insects. They Smith and Cook (1991) use a rwo-tiered system to classify water mite larvae
reach the adults by attending the pupae or final insrar larvae of their hosts and based on where they search for their hosts. 'Terrestrial' larvae search for their
rapidly transferring to the adult when it emerges. Some taxa parasitise insects hosts on the upper side of the surface film, while 'aquatic' larvae search for hosts
MITES: ECOLOGY,EVOLUTION
A N D BEHAVIOUR
within the water column or on the benthic substrate. The turcraia search mode
appears to be ancestral,judging by the more primitive morphology of larvae and
addm of such tma (Hydrovolzioidea, H b h a n t o i d e a , Evlaioidea). The aauat-
ic search mode e v o i d at least t h k -&es, in the. Stygothrombidihe,
H y d c d d a e and in the basal lineage leading to the Lebcrtioidea, Arrcnuroidea
and Hpbatoidea. As discussed above (see page 205). parasitic behaviour in
water mite lanrac has been lost in at least 20 &rent lineages.
The process of atrachment, from searching for the host to the initiation of
parasitic fkding, has aaraaad the attention of many works. Mitchell (1960)
.observed the host-Seacching behaviour of AmursrsfissieornQ which parasitises
dragonflies. He cowidcrcd the movements of the larvae to be random and con-
duded that thue was no distance ptrtepdon involved in finding a host. Davies
(1959) had a dif&mtopinion and Mt it was possible that some chemical fic-
tor, released as the pupal skin splits, stimulates larval S p d o n (Sperchontidae)
to congqpte near emerging adult blacktlics. Gledhill et d (1982) studied
S p d o n s&&r brvac in Engbnd and saw that the mites would enter the pupal
cases of blackflies long M re the iosecP were ready for ccdysis. This early
colonisation appears m &te Davies' concept of a chemical cue leading to the
congregation of mites at dmes of mass emergence. Smith and M c l w (1984a),
in their study of ilrrrnunrs parasitism on A r h mosquitoes, o b d that mite
larvae appcared to bc a d to mosquito pupae over short distances. The
attraction was not a response to vibrations because mite larvae were also atuaa-
ad to anaathecised pupae. They Mt a water-borne chemical cue was most Like-
ly, although other cues could not be disregarded.
Prior to attachment for &ding, watu mite larvae can be easily removed
tiom the preadult host without any apparent harm. Upon beginning parasitism,
the larva i n d u c e s its chelicaae and produces a srylostome (discussed below).
In this case the mouthparts bemme firmly embedded in the body of the host
and prevent the easy removal of the parasites. The window of opportunity for
tramdk may be very brief and some h e may be left behind on the host's exu-
viae (Proctor, pus. obs.). Perhaps this danger has selcaed for an interesdng
mode of pre-paasitic attachment shown by Unionicokz (Unionicolidae),
Hygrobac~rand Atmtnirirs (Hygrobatidae). Lvvae of these genera bite through
the pupal skin of their dipteran hosts to embed their chelicuac in the integu-
ment of the adult developing within (Ullrich 1976). When the adult doses, the
mite larvae are dragged through the pupal acuviae rather than having to active-
ly transkr. These larvae arc very long and narrow compared to mite larvae that
transfir in a more conventional manner, most likely to allow them to be pulled
more easily through the old pupal skin.
Many authors have described tube-like structures that penetrate into the
body of the host at the site of chcliceral penetration. These structures, which
may be flask-shaped or ramified, are termed styiostomes. Stylostomes are also
produced by the larvae of some terrestrial parasitcngones, although these are of
a s w d y diCtirent f'om (Abro 1988). Smith (1988) says it is not dear how
many. species of watu mites use stylostomes and that barbigera
(Hydryphantidac) apparently does not. W~thina species of mite, stylostomes
tend to have the same structure rrgardleg of host species but structure can vary
between congeners (Lanciani& Smith 1989). Abro (1984.1991) has examined
the process of stylosome hrmation microscopically. After transferring to its
adult damselfy host, an Amnunrs larva (Arrenuridae) biter througb the host
inte&umentand injects a bleb of fluid. Into the interior of this droplet another
fluid is injected that condenses along its outer surface to fbm a tube. &ro f&
that the role of the vesicle is to provide a b d e r for this developing stylostome
against immune reactions fiom host tissues. As more of this fluid is injected,
the tube elongates u n d it reaches an open haemolymph space in the host's
body. The original bleb darkens (presumably because of the host's immune
response) and solidifies and cements the W s CheLicerae to the host's integu-
ment. In water mites the stylostome ends blindly but in the terrestrial chiggers
it appears to be an open-ended tube. It is easy to understand how chiggers
might suck up the liqudied cissues of their hosts through such a drinking straw
but it is less apparent how water mites get nutrients &rough their closed sty-
lostomcs. Abro (1984) feels that Anrnuncr larvae tked by pumping out diges-
tive enzymes into the stylosmme. The stylostome's wall is permeable to this
fluid, which is forced out to liquefy host tissues. Subsequent sucking by the lar-
val pharynx draws the surrounding fluids back into the stylostome and to the
mite's mouth. The long stylostome tube may d o w a greater area of the host's
body to be probed than would be available to mites feeding on tissues only at
the site of penetration. Abro (1984) suggests that the blind-ended tube of water
mites is adaptive in preventing fkgments of cuticle from being sucked into the
narrow oesophagus of the larval mite; chiggers can get by with open-ended
tubes because they fkd on nonshitinised hosts. In Anmurur spp. a stylostome
begins to form within 10 minutes of attachment to a host and reaches its find
shape aficr one day; however, in larvae of Hydracbna spp., which remain on
their hosts for a much longer time, the srylostome grows considerably ovcr a
period of months (Smith 1988).
Detachment and re-enay mechanisms are not well understood It is dear
that water mite larvae on aerial hosts have a more uncertain fate than those par-
asitic on aquatic hosts like beetles or bugs. Ellis-Adam & Davids (1970) found
that brvae of Piom &icokz dropped from their chironomid host apparently at
random, "&ardlmof the midge's proximity to water. Ullrich (1978) also states
that Spmhon parasites of simuliids leave their host randomly, whether over open
water or not.
It has ofien been stated that mite larvae should p& the host sex that is
more likely to be in dose proximity to water. Smith and Mdvcr (1984b) state
that Armrum larvae detach kom their mosquito hosts when the mosquitoes
return to water to oviposit. H o w m they found no consistent pr&rencc of the
mites for kmale mosquitoes. Davies (1959) and Booth (1978) hund signifi-
cantly more mite larvae on female dipterans but Booth attributed this greater
load to the brger size of the female flies. Gledhill et aL (1982), on the other
hand, fbund little evidence of preference h r &male blackflies over males as hosts
for Spmhon brvac. Mitchell (1967) and Robinson (1983) both found that male
donates were more commonly parasitised than were &males. Mitchell suggest-
ed chat the larvae may be choosing m k because this sex tcnds to runain near
territories around water.
- -
Oviposition behaviour - irrespective of host sex -may a&a detachment
rate. ROUT (1997) found that Anrnurus tot larvae were more likely to
detach fiom mating pairs of the d d y CbcMMn brUUtyL2lum than from
pairs of C.p~ccILrHe amibutcd this to C h u m h u m ovipositing under water,
thereby wetting the integument of the pair, while C pucb oviposits in floating
aquatic vegetation.
MITES:ECOLOGY, EVOLUTIONA N D B E H A V I O U R
(b) Dicrocheles (Laelp&)
Asher Treat's 1975 book Mites of Moths and Butfq% is a lyrical and entertain-
ing exploration of the mites associated with lepidoptuans. Although Treat
describes many fascinating acarincs, the most astonishing are the mothcar
mites. Many moths have p a i d tympanic chambers on their abdomens or tho-
races. -Each chamber is divided into an interior and exterior 'room' by a thin
tympanic membrane that acts as an eardrum. The main function of a moth's ears
is to listen for the ultrasonic cries of hunting bats. About a dozen species of mites
have been d e n from the outer ears of noctuid mochs but only t h e of the
genus Dirrorhrks are known .to invade the inner chamber.
Species of Dictochtks are cympanicolous and are faund on n o d & on all
continents (except, of course, Antarctica). Occupancy of moth ears by the best
known species, D. p h h h t c r , is unilateral. The occupied ear may be right or
left but, regardless of which, the other car is almost invariably lefi undisturbed.
I k t i o n appears to occur when moths ked at flowers, as it does far mcsostig-
matan mites phoretic on hummingbirds (see page 178). When a k d e D. pha-
larno&ctrs'is p l a d on a restrained moth, she first explores both 'shoulders' of
the moth'repcatedly and eventually rushes for one ear. She revisits the junction
between thorax and abdomen several times but always returns to the same mr.
Treat &Is that this repolted travel reflects the laying of a pheromone trail by the
first mite because D. phakzrnodccctcs subsequently i n d u c e d to the same moth
almost always take the same route. He bund no evidence that mites exploring
'virgin' moths had a preference k r the left or right side.
Soon after arriving at the chosen car, the female xdoves both the tympanic
and counteqmpanic membranes and engorges on host haunolymph. She lays
eggs in the rympanic air sac and on the conjuncdval membrane, up to 80 eggs in
her lifetime. Treat noted that 'public sanitation* appeared weU regdad in
DierochcCes colonies. Mites excrete only at the outer margin of the tympanic recess
or at the rear of the counterrympanic cavity. W h e n the young reach adulthood
they mate. At this point the ear may be too crowded to accommodate more off-
spring. Treat observed that the departure of young mated f d e s appeared to be
encouraged by jostliig movements of more established individuals. Debarkation
tends to occur at nighdill, when the moth actively searches for flowus. Mites
move from the cars to the v e n d side of the head. If a flower is OW to the
moth, several mites may quickly transfer on to it via the moth's proboscis.
Ald~oughD. phalaolodecctcs often n e d in flowus b r several hours, Trtat did
not see them fatd on nectar or pollen. These young fern& readily mount other
moths that come to fked, in quest of uncrowded cars to colonisenise
It would be an unwise mite that would damage the auditory abiity of its
host. What e&ct does being d&ned in one ear have on the escape response of
moths parasitid by Dimchela phalamohcm? Treat occasionally collected
moths with 'ghost colonies' in which evidence of previous occupancy of an cu
was obvious but no mites remained, m g that the moths had no problem
surviving bat attacks both during and afier infestation. Treat also observed
infested moths showing the characteristic jinking and diving indicative of bat
avoidance. It is possible that bilateral colonies do occur but are not observed in
moths collected at light traps because such completely d&ned hosts tend to be
caught and eaten by bats.
In the summer of 1975, when h is book had already gone to press, Treat was
rather shocked to find moths at his collecting light that had both cars heavily
colonised by what looked like Dhcheks phalamodectes (Treat 1977). Since he
had seen only ten bilateral infestations in 23 years of mllecting, Treat Llt that
something was amiss. Upon closer inspection, they proved to be DimchcCes
scc&, a species previously reported to produce bilateral infestations in New
Zealand moths. Of 26 atpertnental infaunations of various moth horn, Treat
found tha~20 were bilateral. But although D. sccctutu eypidy invaded both
ears, in most instances the tympanic membranes and acoustic sensilla were not
destroyed and moths retained acoustic sensitivior. Another &rencc between
~irroChe~es phlrlaenoh- and D. sce&trs was h a t the latter took a sub&r
(beneath the wing)route to the moth's cat rather than a do& midline approach.
1
22 1
This could be one of the reasons why D. sccdasKs produces bilateral colonies:
pheromone paths laid by pioneering mites may not be noted by mites that
approach
..
the moth fiom the other side.
Another p u p of e a r d d i n g mites also avoids the danger of deafening the
host by not puncturing their ear drunls. 'Otopheidomenidae' means 'ear-sparing'
and refers to the fact d ~ athe
t mites of this M y do not damage tympanic area^.
Eggs are usually laid in both eats. Many otopheidomenidslive on sphingid moths,
which do not have cars, while others parasitkc hernipcerans (Krana 1978).
(c) Acarine paraitoiri;
A parasitoid slowly but inevitabIy kills its victim, only one of which is required
for the parasitoid to complete its development This places its strategy between
parasitism and predation. The best known parasitoids arc the tiny wasps ofien
used for biocontrol of insects pests. Parasitoidism is also common in the Diptera
(e.g. Tachinidae). Among parasitoid insects, the larval stage feeds on the
hosc/prey and the adult &males are free-living and search for victims for their
ofipring. The situation is somewhat different in mites, as adult females both
search and 'paras~dise'. Parasitoidism is common in the prostigmatan cohort
Tarsonemina but has not ytt been recorded among other groups of mites
(Kaliszewski et rrL 1995).
Members of the Pyemoadae and Acarophenacidae are parasitoids of a wide
range of insect h a and a d eggs, larvae, pupae and soft-bodied adults. Female
mites search out and atsach to a victim by their mouthpans. Pyemotids are
known to inject a toxin that imrnobilises the insect. Species of pvnnOm, hay- or
straw-itch mites, ofkn bite non-carget organisms including livestock and
humans. The injected toxin causes intensely itchy and painful blisters. During
facding on insea hosts, the body of the female parasitoid swells up to contain
many w.Swelling of the posterior body is termed physopuy and is also seen
in hngus-feeding members of the Tarsonemina (e.g. Pygmephoridae).
Kaliszewski ct aL c1995) suggest that physogasuy in fungivorous ancestors was
a preliminary step towards parasitoidism, rather than parasitoids evolving from
predatory ancestors. Eggs typically remain in the female's body until they reach
an advanced stage of development, either hatching out as adults upon oviposi-
don or even within the body of the mother (seepage 45). So the parencal fmale
acts as a conduit for all numtion needed for complete development of her off-
spring. Wrensch and Bruce (1991) found that Pymotcs mmtLf n'males produce
on average 254 obpring, of which 92% are females, resulting in a population
doubling time of only 1.1 days. The rapid rate of population in- achieved
by such auncated l i e histories has encouraged some to consider use of pye-
motids as biocontrol agents of stored-~roductpests. However. Eidcwort (1983)
notes that the limited powers of dispersal of these mites, plus the nasty side
MITES: ECOLOGY,
EVOLUTION
AND BEHAVIOUR
e h t s on humans, would seem to make them poor choices for biocontrol of
insects near human habitations.
Some parasitoid mites miy have solved the problem of moving to new sites.
Adult f;cmale Adancykdism (Acamphcnacidae)ace parasitoids on eggs of thrips.
Unengorgcd firnae Adarrylidium have been fbund attached to adult thrips,
which implies a phoretic relationship that allows the mites a higher probability
of finding fbod (Eidcwort 1983). This may be similar to the pattern in water
mites of larvae parasitking adult insens whose cggs, larvae or pupae arc con-
sumed by p o s M stages (Proctor & Prit~hatd,1989).
Sometimes the results of mite behaviour on host fitness are identical to par-
asitoidism, even though a host is not eaten. In the hgivorous TtOChMnth3difcm
mmbuCarrrmCPygmephoridae), adult fbales are phoretic on female alkali bees,
Nomirr mehndm' (Halictidae) (Lindquist 1985; Kalistmski ct aL. 1995). As the
fkmale bet provisions each brood cell with pollen sufficient to f;ead a single off-
spring, a female I: tihkztum d i d . The bee oviposits and seals the d.
The mite then empties her spore-bearing pockets (sporothecac) onto the pollen.
The spores germinate and develop into a fungal mycelium p w i q on the pollen
store. Lindquist (1985) hypothesii that the W e T trr'buhurn kills thc bee
egg or larva almost immediately, as living bee bnrae have not been fbund in cells
that contain mites. The developing bet would have becn a competitor with the
mite's fungus h r the brood provisions. The mite keds on the mycelium, under-
goes physogasuy and reproduces. Afier mating, her adult daughters escape fiom
the brood cell and seek f;emae bees to carry them. Kaliszewski n aL (1995) fkd
that because i? hbuCarum reproduces only in cells that contain a dead larva, efie
e k is the same as that of a parasitoid.
Likewise, females of Iponmrur species (Tacsonemidae) act like parasitoids
when kcding on the eggs of bark beetles fiom the scolytid subfkdy Ipinat.
Lindquist (1969) provides a detailed description of the taxonomy and biology of
this group. Iponemur kmales use adult bark beetles as phontic hosts and dis-
mount to feed when eggs are laid in galleries in pine trees. The mites invariably
kill the eggs and each mite typically does not require more than one egg to com-
plete its development. Feeding f;tmales become physogastric and lay fiom 40-80
eggs. The eggs develop directly into adults without feeding. Males mate with
newly d o s e d ~males,which then seek out young beetles on which to hitch a
ride to the next aee. Lindquist noted a positive correlation between the size of
the unengorged female and that of the host. He felt thii correlation was deter-
mined not by the phoretic interaction but by the parasitoidic one, as larger bec-
tlcs lay larger eggs suitable for fkding larger mites.
Mutualism
There have been fkv unequivocal demonstrationsof mucualism among mites and
hosts (Eidcwort 1990). The most obvious benefit that a mite could pxwide is
reduction of harmfbl parasites or competitors. Eichmn (1994) notes that queen
bumble bees bearing P a & h (Mesostigmam Parasiadae) have low levels of
parasiac nematodes. Hunter and bsario (1988) suggest that some phoretic
species of mesosdgnacatls benefit their beetle hosts by p&rcntially fkcding on
h a r d nematodes (eg. D&lac&ps modrjetw on the southern pine beetle and
CrrcoIn'puzcoehnonuon the bark beetle Ipr con+) or on competing species (eg.
Poecilocbifirr mmphm' pierces fiy eggs deposited on mouse carcasses prepared by
its burying beetle host). Eickwort (1990) suggests that f l n g u s - f d n g
I ANIMALS
AS HABITATS
astigmacan~,tydeids and pypephoroids, and neaophagous mesostigmatans and
a d d s may serve a sanitary role, as would hidostomatids that remove bacteria
h m host bodies and provisions. For example, Paqgm+ottu cozktriutnw
(J?ygmephoridae) fkeds on the mecomium of the larvae of its phorctic host, the
bee Agqosttmon narum, possibly reducing disease in the larvae (Athias-Binche
1991). Likewise, Houck and OConnor (1991) mention that Anoerur
(Histiostomatidae)occurs with soil-dwelIing bees where it filter fix& on microor-
ganisms by skimming the surfgces of provisions and larvae Scimr&&ps
(Laelapidae), bund on burtowing &aches ( M m p a d h z , Cmmzpbew and
Ncogeos~dpbn;),may oonmbutes to the hygiene of the cockma& burrows by
fkding on potendally damaghg asdgmatans (Halliday 1993).
The relationships between carrion-f;ceding burying beetles (Silphidae) and
their ubiquitous mites, species of Poecilochims (Parasiticlae), have bcen studied
by many authors (e.g. Schhwan & Miiller 1992, Brown &Wilson 1994, Schwarz
1996). Burying beetles of the &enus Nmphorus (aka.Ncmphonrr) arc a r m -
ed to the odour of rotting vertebrate flesh. If the carcass is small enough, a
male/f;emaepair will bury it and fbrm it into a fleshy '~est'fbr their lafvae. The
parents remain with their ofIipring until the larvae arc in an advancad stage of
development and then leave to search fbr other carcasses. Deutonymphal
PoeEilocbitlLs are phomic on the beetles and dismount to fi.md on fly larvae and
nematodes that compete with the beetle larvae fbr the carcass, complete their
development, mate and reproduce in the nest chamber, The next generation of
mites may depart with the parents or with the newly emerged young beetles.
Thcy are also able to $witch from their original host to a new one, should two
beetles meet and interact (Brown & W h o n 1994). Wilson and Knollenberg
(1987) performed 18 experiments on several species of I \ r ' u ~ o p h oand
~ their
Poecilochirus. In most experiments, the mites had neither positive nor negative
efficcs on host fitness but in fbur experiments the mites had positive e&cts.
Negative effacts were observed in a fiw replicate. in which mites existed at den-
sities rarely observed in nature. Previous studies of the interactions between
mites and the beetle N. tomtnaoncs suggested that doeply buried carcasses were
protected from fly oviposiaon, while shallowly buried ones received many fly
eggs. If fly larvac hatched in the absence of the mite I? mmphon' they outcorn-
peted the beetle larvae ( W i i n 1983); so mites appeared most beneficial when
carcasses were shallowly buried. However, in Wllson and Knollenberg's experi-
ments they found that N.ca!@dicnr, which puts carcasses in shallow depressions
covered by leaves, did not s&r when its mites were removed. They modified
(but did not test) Wilson's (1983) hypothesis by suggesting that flies may be
leery of walking underneath leaves to oviposit fbr fkar of spiders. One benefit fix
the beede N.o&iioUis was that mites reduced the number of nematodes carried
to filntre carcasses.
Acarinaria and the conundrum of Kettttethiella
The most puzzling aspect of mitcl'invertrbtate symbioses is that hosts ofien
. appear to encourage their own colonisadon by having structures seemingly
designed to carry mites. The presence of the& pits or pockets, termed Pcarinat-
ia, has led many to assume that the mites benefit their hosts in some way.
Carpenter bees (Mcgachilidae) ofkn have prominent acarinaria. Skaife (1952)
studied the relationship between one species of Afiican carpenter bee,
Mrsotrithia a@n,and its laelapid pocket mite, Dirwgamasus bnrrmsi.
 Most female bees have acarinaria (on abdomens), but all males and some
fern& lack them. Up to 17 young female D. brarmn'can occupy each podcct.
At the time of S W s paper, 36 species of Dimgamaw had been found, all asso-
ciated with bees. During the aununn and winter the mites remain in the acari-
nark and die if removed fiom the host, even if honey and pollen ase provided.
When the female bee nests in the spring, one or two mites disembark with each
oviposition m n t and are d e d in a chamber with the bee egg and fbod mass.
Because the bee stam by laying female eggs and ends with male eggs, the first
mites to disembark are imprisoned with a f d e lama and later mite. get males.
Mites do not do much until thc lam has fed and enters the pre-pupal stage. At
this point the mites creep over the resting larvae and become very fit, 'as thick
from above downwards as they are wide'. The D. brrunsi die at this point if
removed from the pre-pupa but, if placed in a glass cube with nothing but the
larva, rhqr flourish. Thus the mites do not M on provisions or on other species
of invertebrates eypidy present in the chambers. Skaik concluded that they
must feed on exudate fiom the bee's skin. When the bee h pupates, the mites
lay their eggs on the pupa. Skaife never observed males and so assumed the mites
were totally parthenogenetic Larvae and nymphs feed on pupal exudate. Afcer
4-5 weeks the adult bees emerge and demolish the divisions between cells. Mites
and bees freely intermix and the mites crawl into the acarinaria of female bees
(SOthose locked in with male eggs are not doomed).
Skaife observed that the mites do not appear to harm their horn in any way.
Pupae heavily inkted with D. bmunsi produced adults as vigorous as those fiom
pupae without any mites at all. Conversely, they did not seem to benefit their
hosts. Skaife removed all the mites from some nests and the bees reared in them
behaved normally. Furthermore, a small percentage of female M. c a m lack the
abdominal pouch and do not harbour mites. The presence of mites docs not
c a w acarinaria, as pupae without mitcs did not grow up lacking these srruc-
tures. It is bossible that the benefit of D. braunri for their hosts was too subde
fbr Skaife ro observe or that rfie benefits would man&r only in certain condi-
tions (e.g. if the nests were infisted with dangerous fungus or bacteria, or with
parasitoids l i Tmhommidium, see page 216).
The most astonishing study of hymenopterans with acarinaria is that of
Cowan (1984), on the solitary wasp Anciztrocm antihpe (Eumeniclae) and its
symbiotic asrigmatan Klmnctbielkz trirctosa (Wintersdunidtiidae). The natural
history of this mite encapsulates many of the things that make mites such excit-
ing subjects for study. Female wasps nest in tubular cavities in wood, where they
leave paralysed caterpillars as b o d for their offspring. Only one wasp larva
develops in each cavity. Deutonymphs of K trisctsa are phoretic on adult wasps;
when the female wasp oviposits, several deutonymphs aawl off into the cell. The
mites rest on the wasp egg and, although they do not appear to feed,they do get
fitter. It is possible that they absorb water or egg fluids through their inrcgu-
ment. Afcer moulting to tritonymphs, the mitcs share the haemolyrnph of the
paralysed caterpillar with the wasp larva.
By the time the wasp pupates, the mites are adult. They then f$ed on
hacmolyrnph of the quiescent ptc-pupal wasp. The mites endeavour to stay at
the posterior dorsal region of the host when not tieding, possibly because this is
the hardest place for the host to reach with its mouthparts. Nevertheless, G w a n
bund that female wasp Larvae wen able to decimace their mites (only 16 sur-
vived of 123 on female larvae versus 132 of 137 on male larvae). Cawan found
no evidence that mite deutonymphs distinguished between eggs destined to
become males or females.
A virgin f i d e K setom develops a single large egg chat hatches internally
into a larva, which immediately moults into a male protonymph. Females then
give b i to the protonymphs, which arc very small (probably because the lama
does not fixd). The male pmtonymphs transform to mtonymphs without an
intervening deutonymphalcning&ge. Aft& giving birth to these puny males, f d e s
may mate with large males that dcvelopcd fiom male deutonymphs that entered
the wasp's cell b&re it was sealed. However, Cowan fbund only 9% of all deu-
tonymphs entering celk became males. So, most females (1 14 of 132) had to 225
mate with small males. Arrhenotokous producrion of small maIes appears to be
a bet-hedging strategy by females in c& they are trapped withou; Hny mates.
Large males arc not aggressive to small ones, possibly because they do not repre-
sent serious rivals; however, small males zrtadc and kill each othw
Mated firm& mites deposit their eggs (up ro 125) on the wasp pupa and
mite larvae and protonymphs faed on the pupa apparently without causing it
harm. By the time the wasps emerge from their pupal cases, the mites are deu-
tonymphs and attach only to the acarinaria on the wasps' propodeurn. The max-
imum number that can squcac into an acarinarium is 400, and any extra mites
end up Wing or being scraped OK As mentioned above, female wasp h e kill
the mites in their cells prior to pupaaon but male wasp larvae do n o t So adult
female wasps emerge with few or no mius but the acarinaria of males are packed
with them
How then does K sctosa get into the egg chambers of the next generation of
wasps? Females are infested v e n d y when they copulate, at which point the
deutonymphs run off the male and into the female's genital chamber, there to
await her ovipositioa Deutonympk that do not uansfer to fimale wasps arc
doomed because males do not visit nests. Female wasps ofien mate with dBzr-
ent partners, allowing the possibility of different mite genotypes boarding a
given female. The occasional mite that avoids being killed by femae wasp larvae
a h ina-eases the potential fbr outbreeding. The aggression shown by small male
mites suggests that mixing of genotypes in a single cell is common.
Why do female wasp larvae kill mites but male larvae do not) If the mites
are being beneficial (eg.destroying parasites), why would this be good f$r males
but not funales? And why do the kmales have acarinaria if they almost never
carry mites? Cowan wondered whether the presence of mites in the female's
venereal chamber may inhibit intromission by subsequent males and this acarine
chastity belt may be advantageous to males in s d competition Cowan also
noted that the mites a male wasp transmits do not persist on his descendants but
only on his mate's; because of the haplodiploid genetic system, male
hymenopterans have no sons (haploid) and their diploid daughters usually
destroy the mites u;msmitted by their fathers.
Athias-Binche (1991) exprrsses great puzzlement over the relationship
between KinmtbicCla and A n z i s m c m Why would the host develop an acari-
narium for this not obviously beneficial mite?Arr acarinaria to protca mites and
ensure their presence or to reduce distwbance to the host caused by having h i -
tating little Ates all ovu one's body (the 'mice pocket' hypothesis, & page237)?
Cleady, a grcat deal is unknown about the evolutionarv processes resultine" in the
appa&t haptation for mite carrying in many beesW&dwasps, as well as b r
other potential m u d s r n s . Manipulative experiments such as those of Wilson
 MITES:
ECOLOGY.EVOLUTIONA N D BEHAVIOUR
and Knollenberg (1987), rather than observational studies, seem the only way to
solve t h e mysteries.
LIFE WITH VERTEBRATES
As mentioned in the introduction to thii chapter, we will desuibe the associa-
tions between parasiac mites and vertebrates rather superficially, as acarines of
medical and veterinary importance are well covered in other texts. This, howev-
er, docs not makc them any less Fascinating.
6 example of this is h n y which is found in a wide range of mammal nuts
Mammals and their homes
As clothes make the man, so hair makes the mammal. Some mammals are hairi-
er than others: heavily furred artiodaayls have 233-6916 hairs per square cen-
timetre, while otters have 35 000-51 000 (Kim 1985a). Hair provides a
wonderful dimatcc0nmUed environment fbr the mites that swarm over and in
the skin surfices of most species of r n a m d . Although sweat glands are lack-
ing in rodents and elephants, most mammals have numerous skin glands that
have been invaded by mites. According to Kim (1985a), bats have perhaps the
most diverse array of both sudorikrous and sebaceous glands fbund within the
M a d This rich diversity of glands harbours a s i m i i d i m i t y of mites.
although apparently no inseas have invaded the glands of mammal. The coo-
logical and evolutionary relationships betwen this class of vertebrates and their
acarine associates are thoroughly discussed in the book edited by Kim (1985b)
and much of what kUows comes from thii source.
fa)Mites i n mammalirzn nests and la&
Akough we consider birds to be the quintessential nest builders among verte-
brates, most mammals also live in nests of some sort. Such abodes range from
long-term colonies of thousands of bats to the mats of boughs built nightly by
chimpanzees. Nests and dens are places to rest, to give b i d and to nurse young,
and to eat. So nests accumulate such potential foodm&i as arthropods, tbod
bits, fungus, b, skin flakes and blood. As well, nests are warm and humid
when the host is home.
Among mammal-associated mites, everything fiom free-living nidicola to
- - o h co-sdst in the same nest (Radovskv 1985). For
oblimte haemophages
e.xaGple, various species of N'prupis (Laelapidae) occur fhz~-li&~ predators
s Andtvhh~s
as well as nidicoles in vertebrate and invertebrate nests. S ~ e d e of
and Haemogm~nrr(Laelapidae) vary in their requkment'br blood fbr suc&-
ful development and this rcquiment appears to vary with the specid abiity to
draw blood. Evolutionarily speaking, nest mites may acquire a 'taste' fbr blood
by initially preying on blood-Wng parasites and then moving onto fiesh
sources of blood
For humans and some rodents (e.g. squirrels) and hgomorphs (eg.pikas),
allspuction activities are not confined to nest making but include the manu-
Faaurc of larders fbr storage of food. To our knowledge there haw been no
derailed studies of mites of rodent larders but there is a large body of literature
on human stored-pmdw mites (e.g. Hughes 1976, OConnor 1979, 1982).
Species in 34 genera in 10 h i l i e s have independently invaded stored products
andlor house dust (OConnor 1979). Most of these mites are astigrnatans that
fecd on Fungus also infesting the stores.
OConnor (1979) fecls that because man has been storing food in quantity
for only about 10 000 years, this is insufficient time to d o w the cvolurion of
such a large number of taxa purely through association with man. Rather,
scored-product Astigmara have repeatedly invaded human habitations from sim-
ilar n a d habitats. OConnor divides these mites into four groups. Some are
ancestrdly associated with a specific product that humans bring inside (e.g.
C;iupoglypbzuoocurs on rotting fruit). A second group is associated with wide-
spread 'field' resources, e.g. Tyrophagur spp. arc widely distributed in grassland
and litter habitars. The largest group is that associated with mammal nesa. An
including bat roosts. Finally, there are those originally associated with btd nests
such as Dm~tophgoia& the h h n o u s housedust mites. T u b is not the only
rckshment sought by astigmaeans. Quintcro and Acevedo (1991) bund
Cz~ogfyphusin 33% of 84 samples of pulque, a beverage made h m the fer-
mented sap of agave.
Not ali mites associated with human habitations and stores arc astigmarans
interested in feeding on our f$odstu&s. Siha (1979) notes that approximately
50 species of prostigmatam, mesostigmacans and astigmatans are associated with
stored grains. These mites may indude granivorcs (although only a kw acarids
directly eat the kernels), others fked on non-grain parrs such as leaves and stems
in hay, and some are predators and parasitaids of other grain inhabitants.
W e , van Bronswijk (1979) vims domestic dust as an ecosystem. House
dust is composed ofskin flakes,cotton fibres, paper fibres, wool, synthetic fibres,
mite droppings and crtuviae, etc. between 0.01 to 1 mm in diameter. Dust
together with dust-associated b g i are eaten by a number of astigmatan species
in the genera Dm~tophagoidu,Hitrtia and Eumgiphus (Pyroglyphidae). These
mites are preyed upon by C h e y h , pseudoscorpions and probably silvufish and
psocopurans ('book Lice'). Other mites common in house dust include
Giycyphup, Cbartaglypphur, Bhmia, Cosmochrhonius and Amnenwchthonius,
which probably f;ml on fungus or food scraps rather than dust per se. Van
Bronswijk (1979) notes that the suucnue of the arthropod community in bird
nests is similar to that of house dust acept that species richness is higher in bird
nests than in human dwellings.
Dust mites arc the mos<infamous of nidicolous acarines because of their
association with 'dust allergies'. Arlian (19893 describes the biology of these ani-
mals. Dust mites belong to the astigmatan M y Pyroglyphidae, with 14species
reported from house dust in various parts of the world The three most common
species are Dermatophagoicin pmysdnus, D. @rime and EumaryPhus maymi
They live in our rugs, furniture, rnatucsses, bedding and other areas that accu-
mulate organic detritus and maintain a high I d of humidity. Proglyphid
mites feed on cast skin flakes (h = skin, phagm = eat), hair and other detri-
tus, together with the microbes thar grow on this minute rettsc They are the
most important source of allergens in house dust. Allergens produced by these
mites cause severe allergies, rhinitis, -ma and asthma that affect 50-100 mil-
lion people worldwide. These allergens are contained primarily in dust mite he-
ces. These are dry pellecs 20-50 pm in diameter that are covered with a
peritrophic membrane (a membrane produced in the gut of the mite). On aver-
age, about 20 pellets ate produced by each mite each day and they readily
become airborne. Other allergens arc present in the skin of the mite; so atuviae
and bits of dead mites also cause reactions.
 MITES: ECOLOGY.
EVOLUTION
AND B E H A V I O U R
The phrase 'dry as dust' suggests that house dust may be an arid environ-
ment for tiny animals. Dust mites have an ingenious solution to the problem of
water balance (shared by numerous other Astigmata). A small gland opening at
the base of the first pair of legs (supracoxal gland) secretes a solution of sodium
and potassium chloride into a gutter that runs to the mouth opening. T h e salt
solution is hygroscopic and absorbs water from the atmosphere, down to a
species-specific critical threshold of relative humidity (often 70-75% R H at
25°C). At lower humidities, the solution crystallises and blocks the gland open-
ing, preventing water loss. So, dust mites obtain water from the aunosphere at
228 relative humidities above the critical threshold but are unable to 'drink' at lower
relative humidities and will desiccate and die if low RH is maintained for very
long. Any conditions that help to maintain high humidities may encourage
house dust mite populations. Poorly ventilated homes, those with furnishings
that retain humidicy (deep rugs, upholstered furniture) or those chat use humid-
ifiers or evaporative coolers will tend to have high average relative humidities,
especially in the arms where the mites live. In extreme circumstances, densities
can reach as high as 3500 mites per gram of dust (Kettle 1995).
(b) Mites on and in mammals
An intimidating diversicy of mites are permanendy associated with the bodies
of rnammals (Kim 1985a. OConnor 1994). No group of mammals. nor any
part of the body, is excepted from this acarine onslaught. For example, the
Halarachnidae live in respiratory organs of pinnipeds and primates, Hystri-
chonyssidae in ears of porcupines and the Demodicidae in the hair follicles of
just about all rnammals. Perhaps because they tend to roost in large aggregations,
bats arc host to a large array of parasitic mites. In the Mesostigmata, Spinturni-
cidae, Spelaeorhynchidae and Macronyssidac have bat hosts. Among the Prosti-
grnata, representatives of rhe Myobiidae and Trombiculidae attack chirop-
terms. In the Astigmara, four h i l i e s - Chir~rh~nchobiidae, Gastronyssidae,
Rosensteiniidae andTeinocoptidae -are exclusive to bats. In fact, epiwic mites
of bats include 18 families and more than 1000 species (Morales-Malacara
1996).
Various parts of the mammalian skin are consumed by the different groups
of parasitic mites. Kim (1985a) states chat parasitic mesostigmatans, such as lae-
lapids, dermanyssids, macronyssids and spinturnicids, are basically polyphagous.
Haemogamarur ambukzns and Brcvistrrna utabmis utilise both fluid and dried
blood of vertebrates, flea Faeces and living or dead arthropods but rarely d o they
penetrate the skin. Erhinokukzps crbidninw and Haemokulaps glargowi are also
general feeders but usually penetrate the skin. T ~ c k sfeed on blood and lymph,
halarachnids feed on mucous tissue. Sarcoptids, psoroptids and lisvophorids
feed on epidermal detritus and secretions of dermal glands, and some may feed
on blood. Sarcoprcs burrows into the cornified epidermis by attaching itself to
the substratum with ambulacral suckers and cutting a channel into the skin with
its cheliceme and edges of the foretibiae. Nutting (1985) mentions chat prostig-
matans on mammals can be found clinging to hairs (e-g. myobiids), penetrating
the epidermis (e.g. trombiculids) or dermis (e.g. psorergatids) or be semi-
endoparasites (e.g. demodicids) in the sebaceous glands of hair follides.
Humans are fascinated and appalled by the idea that they may be infested
with almost invisible mites. DemodncjXlicuhrum and D. brcvir (Demodicidae)
inhabit the follicles and glands of the human Face where they feed on subcuta-
neous secretions and interstitial fluid. Although widespread, Dcmodex mites are
1 not necessarily found on every individual. Sengbusch and Hauswirth (1986)
/
I
examined 370 human volunteers for the two species of anthropophilic
Demodoc. About 55% had one or both species. 3 1% had D. bnvis only, 1 1%
1 had D. filficuhrurn only and 14% had both. Humans appear to accumulate
mites over their lifetimes: 29% of volunteers aged 25 and younger had mites,
53% of those aged 2 6 5 0 had them and 67% of those 51-90 had them. There
appears to be an effect of host sex on Demodoc infestation, as 198 of 327 males
(61%) were infested vs. 5 of 43 females (12%) (x2 = 13.16, P = 0.0003). The
authors note that sebaceous glands, the site of D. bnvis, are differentially affect-
ed by hormones. 2
Humans are not alone in this infestation. Approximately 150 species of
Demodexhave been collected from more than 35 families of mammals (Nutting
1985). Hosts include both marsupials and placental mammals but demodicids
have not been collected from monotremes, despite much searching. Every
species of (non-monocreme) mammal may host at least one specific demodicid
and myobiid ( ~ 3 0 0spp. described) (Nurting 1985). In contemplating the pos-
session of numerous species of host-specific mites on most rnammals, Nutting
(1985) comments: '[blecause of the variety and often disjunct distribution of
habitats on one mammal, we can look on the mammal as a wandering Galapagos
archipelago with each island (c.g., an eyelid) having several differing habitats'.
The variety of 'habitats' occupied by astigmacan associates of mammals
serves as a good example (Fain & Hyland 1985). Gastronyssidae live attached to
the gastric mucosa, corneae and nasal cavities
of bats. Rhynwptidae are fixed in the hair fol-
licles of their hosts (hysmcid rodents and both
neotropical and afrotropical monkeys).
Audycoptidae are in hair follicles of cebid mon-
keys, ursids (bears) and procyonids (raccoons).
The Listrophoridae - 'fur mites' - are per-
manently attached to the bases of hairs
throughout most of their life cyde using a
membranous anachment structure on their
'sternum'. They probably eat Fatty substances
produced by hair follides. The Chirodiscidae
and Atopomelidaeare also known as 'fur mites'.
They are laterally compressed and attach to the
hair shafu of their hosts with modified first
and second pairs of legs (Figure 9.3). The
Myocoptidae also attach to the hairs of their
hosts using their legs, but use their second and
fourth pairs. The Psoroptidae are skin mites
that live on the surface of the skin at the base of
thick crusts of exudates produced by the hosr in
response to irritation caused by the mites. Skin
ailments resulting from infestation by these
rnites are known & psoroptic mange. l%e most 1
I
infamous mange mites ire in another astig-
Atoporneiidae) from a k o a l a k well a
matan family, the Sarcoptidae, or scabies mites. fraving rwo of legs
Sarco~tidshave chelate-dentate chelicerae for -ping hair+. &is - - ~ n also ha
and spines on their fore tarsi that allow rhem to ( a ve&l g&vc rhar c!a& rhe hair shaf
MITES: ECOLOGY,EVOLUTIONA N D BEHAVIOUR
burrow in the corneous layers of the skin. The skin disease that Sa~copptcsscabiei
causes in humans is termed 'scabies'. Sarcoptu is thought to contain only one
-
species the human itch mite, S. scabin' -and the other 30 species previous-
ly described in this genus are considered host races or varieties (Fain & Hyland
1985; Arlian 1989b). This mite has beem collected from the epidermis of more
than 40 di&nt hosts representing seven orders of mammals. Fain & Hyland
(1985) beliewe that the variabiiry of S. surbin' is the result of continuous inter-
breeding of the strains living on man and on domestic and wild mammals. Even
such recently encountered mammals as ko& and wombats ham become i n k -
ed with scabies. Morphological variation between the strains is small or absent
However, there is some evidence of physiological diffetences among scabies
-
mites from &rent hosrs. Experimmtal attempts to tran.& scabies from d o g
to mice, rats, guinea pigs, pigs, cattle, cats, goats and sheep were unsuccessful,
although most of these hosts ate parasitised naturally by S. s d i t i . Oddly, sca-
bies from dogs could be aansfkrred to New Zealand white laboratory rabbits.
although scabies b m humans and pigs could not Humans ofien contract sca-
bies through infested dogs, pigs and horses (Kettle 1995). Mites may live and
reproduce for up to 13 weeks in the 'wrong' host but these infactions a m usual-
ly self limiting. However, appropriate control studies arc and one won-
d u s how o h infkaions on the 'right* host am & self limiting.
Sickness and poor growth of the host appear not to be due to the direct loss
of energy to the mites as food but to toxic secretions fiom the mites together
with the host's immune responses. Secondary bacterial infixtiow are also com-
mon. In immune-compromised humans, untreated scabies w e n d y leads to
scaly skin and the production of skin austs from hyperkcratosis. Arlian (1989b)
notes that hypukuatotic crusts may be up to 2 un thick and can be easily pried
off the host's skin. Mites are fbund in their greatest densities on the undersur-
face of the crusts; in an inf;caed laboratory rabbit, thut were more than 1400
mites per a2 of skin s&
Mites on, in and around birds
Mitcs are associated both with the homes and the bodies of many b id. Avian
mites are currently of p a t interesr to behavioural ecologists as potential agents
of serual selection (see page 245); however*in this section we will discuss bird
mites, not as evolutionary intermediaries, but as products of selection themselves.
Many of these mites are also found in nests of other vertebrates, including those
of humans. The most obvious of the shared taxa are speck in the a s t i p m a
b i l y Pyroglyphidae, which includes the human 'housedust' mites (OComor
1982). The best studied nest mites are me& of the maosagInatan f b d y
Dumanyssidac. Dmnanymrt gallinac is a ubiquitous pa&# of domestic fbwi
and is also commonly bundon wild b i such as pigeons,-s and sparrows
l mammals
(K.ct& 1995). When these hosts arc not available D. g a l l ~ w i t bite
and, as these birds are often synanthropes, this ofien indudes humans. The mites
tied on roosting b id at night and hide in CttVices in and around fhe nest by day,
where they also &posit Masan (1997) describes the population dynamics of the
Dm~nysm hirundinG in ngts of the penduline tit, R c m i t p A n m
As in house dust (see page 227), whole f w d webs of mites can inhabit nests.
B u m et rzL (199 1 ) used Tn
- funnels to extract the &pods fiom nets of
ANIMALS
AS HABITATS
tree swallows, h o w wrens and eastern bluebirds. A species of detritus-feeding
dust mite, Dm~tophagoidcFrvanri (Pyroglyphidae), occurred in all nuts of all
three species. The predatory mite Chrletom'pbd kpiriopmrurn (Pkgmata.
Cheyletidae)was the least widely distributed (none in bluebii nests, and inhab-
iting 3346% of the other species' nests); however, it sometimes occumd in
large numbers (up to 4000 per nest). It preys on mites and other arthropod ncst
inhabitants. The blood-feeding Drnnanysnrz hirundinis (Mesostigmata:
D~znanyssidac)was ubiquitous in ntsts of all t k b i d . The mean number of
D. hinrndiniz per ncst ranged f k m 5384 fbr eastern bluebid to 12 675 b r the
house wren. In nests with C Icpiriopmnrm mean popularion sizes of other
mites were typically lower than in nests without this predatory mite.
w i d ticks arc aIso nest parasites, visiting the hosc at night, feeding for a
few minutes and then retreating to a nearby nook in or near the nest. licks arc
the most conspicuous group of ectoparasites of seabird colonies (Duffy 1991)
and also arc abundant around colonies of b id such as d o m (Chapman &
Geow 1991).
(6) Mitespnmdnetzt& emprlrusitic on b i d
The northern hwl mite, Omitbonyuur syluktum (Mesostigmata: Macronyssi-
dac), is a haematophagous pest of poultry and a great many species of wild birds
rhroughout the world Thc add= remain on the host except during oviposition
and in heavy infestations can give the bird's plumage a blackish appearance.
Birds am i n k e d with many species of astipacam that Mon various bod-
ily exudaaons (OConnor 1982, 1994). Most Hypoduatidae arr subcurancous
parasites as deutonymphs bur are nidimles in other stages (making them prote-
lean parasites). The life cycle of the best known species, the pigeon-associated
H$o&c#s pmpw is highly c o m p d , with only eggs, deutonymphs and
adults known. In this species the females have reduced mouthparts and do not
M, while males have huge chelicerae that W y have a sexual rather than a
feeding function. T h e deutonyrnph, like all astigmatan deutonymphs, has no
obviously hctional mouth. Nevertheless, once embedded in the skin of a
pigson, it increases hugely in size. Presumably, nutrients are absorbed directly
through the deutonyrnph's integument, as has been proposed for deutonymphs
of Hrmkumptcr coonmcmi on ladybird beetles (see page 204). Thus in this
species, the instar that lacks both mouth and gut obtains the nutrition for the
entire M e cycle.
The KnemidokoptiQr are also astigmatan burrowers in the skin of b i d .
They often cause a pathological condition in domestic poultry called 'scaly-leg',
in which the skin of the legs swells and crusts over. bminisoptidae are aLo skin
burrowers and cause nodules in the flesh of the host. The respiratory passages of
b i d contain the Turbinoptidae, which inhabit the dry regions of the upper res-
piratory naa. Thc Cycoditidae inhabit the lungs, air sacs and tracheae where
they can cause some pathology.
Pmstigmatans a m also represented among the avian parasites. The chigger
Nmscbongartio anmicama (Trombiculidae) is a serious pest of domestic turkeys
(Kettle 1995). An intcrsang prostigmatan parasite is heurnophap bubonis
( C L d d a c ) &from h e lungs of the e t homed owl (Fain & Smilcy 1989). The
h d y was originaty named for a number of genera bund in the cloacae of tur-
tles but as these mites have since been collected fkom the connective tissues of
rodents and insecdvores, as well as from owl lungs, the name 'Cloacaridad seems
increasingly inappropriate.

(c) Mites o n a n d i n featbers
The mites that live anlong feathers are perhaps the most fabulously ornamented
of all Acari (Figure 9.4). Their bizarre beauty has led to much taxonomic study
(see Gaud & Atyeo 1996) but surprisingly little is known of their basic biology.
Although members of many major taxa occupy this habitat, 'feather mices' is
often used to refer to certain feather-dwelling taxa in the Astigmara and it is on
this diverse group that we concentrate.
Gaud and Atyeo (1996) have produced a massive two-volume work that
summarises the biology and taxonomy of the asrigmatan feather mites of the
232 world. They note that plumage has been invaded by a wide range of both insects
(fleas, hcdbugs, hippoboscids, mallophagans) and mites (ticks, mesostigmatans,
prostigmatans, astigmatans). Some are in the plumage for only a short rime, oth-
ers live there for all of their lives. While Nutting (1985) draws an analogy
benveen the surface of mammalian skin and the Galapagos Islands, Gaud &
Atyeo state thar '[iln the jungle of feathers there swarms a complete fauna'. Some
inhabitants of this jungle live in the branches (feather surface), some on the
ground (skin), others in the tree trunks (feather rachis) and finally, others infest
the roots (the father follicles). Some arthropods eat the plumes, some graze on
the detrital 'epiphyrcs' of the feathers, som;suck blood and lymph, an2 others
act as predators.
Astigmacans constitute the most numerically important inhabitants of the
plumage. There are more than 2000 named species in 33 families in 3 super-
families that are collectively termed 'feather mites' sensrc stricro. They inhabit the
surface of the feathers (plumicoles), the skin under the feathers (dermicolu)
and even the interior of feathers (syringicoles). Feather mites are on every order
of birds except for Sphenisciformes (penguins), Rheiformes (rheas) and
Casuariiformes (cassowaries). It is understandable why penguins, with their
aquatic lifestyle and highly modified feathers, might lack feather mices, bur it is
Figure 9.4
An elaborate feather mire (Opisthocornoconrs umbellfer. Pterolichidae).
(After Gaud & Atyeo 1996.)
not clear why the other two groups are mite free. It is not beause they are ratites
(flightless, running birds) because there are feather mites on Srruthioniformes
(ostriches) and Apcerygiforrnes (kiwis). So, perhaps we just have not looked hard
enough for mites of rheas and cassowaries.
Living on or in feathers requires some special morphological adaptations.
For plumicoles, especially those on flighc feathers, there is a great danger of being
dislodged by the bird's movements. So feather mites often have biwzre body
shapes and strange setal appurtenances that allow them to wedge themselves
securely between the barbules (Figures 9.0, 9.4). Aweo and Gaud (1979) note
I
that unhealthy birds unable to flaptheir wings may take on a brown cast b;cause 233
feather mites, normally displaced from much of the plumage by flight, can
swarm with impunity over all the feather surfaces. Eggs are safely glued to the
feather substrate (PCra 1996). Moulting often occurs at particular sites of safe-
ry on the feather or even within the casr skins or egg shells of other feather
inhabitants, a behaviour thar P t r n and Aryeo (1984a) call thanatochresis: 'the
utili7ation of cadavers, secretions, skeletal pieces, excrements and other products
of one species by living individuals of a second species, but not for food ....'
Sometimes feather mites moult inside the cast skins of other members of their
species, building up long exuvial chains. Feather mires also moult inside the
empty eggshells of feather lice. Why engage in thanatochresis? Perhaps as pro-
tection from predation, as fragments of feather mites can often be observed in
the guts of lice. It is also possible that moulting inside the casr skin of another
arthropod reduces loss of moisture or provides a frictional surface to moult
against (like snakes rubbing off skins against rocks).
Are all feather mites parasites? Although they may be referred to as such
in the literature, there is actually little evidence thar mites living on feathers
damage the host. The generic name of one group of plumicolous species, Anafges
(Analgidae), means 'no pain' and is based on the observation thar a heavily
infested bird usually appears quite healthy and happy. But another analgid,
M e p i n i a , may cause financial losses in poultry industry because heavy infcsta-
tions cause birds to pull our their feathers and leads to a decline in weight
and egg production. Similarly, large populations of Dubininia melopsirtari (Xola-
Igidae) may cause the host budgerigar to pull out its feathers. Syringicolous mites
ofien feed on the medulla, or pith, of the feather shaft. Perhaps this weakens the
feather but it is nor clear.
So, if most feather mires d o not harm their hosts, how do they make their
living? Astonishingly, only one published study appears to have dealt with this
vital topic (Dubinin 1951). As it is printed in Russian, most citations of
Dubinin's work by western researchers are probably based not on reading the
original paper (which is not readily available) but are citations of previous cira-
tions. Neither of the present authors has access to Dubinin's original public~tion
and so we must also follow this path. According to OConnor (1982, 1984a),
Dubinin only occasionally observed tiny feather fragments inside feather mires.
Instead, the guts of a large number of species contained fun& spores. OConnor
confirms chis with his own observations that mites ofien have guts packed with
fungal material, .and we have also seen this in many Australian species.
It may be that feather mites deliberately pick off fungal hyphae and spores
from the host's feathers or they may feed on feather oils and only accidentally
ingest these particles. An unpublished experiment by John Clark in New
Zealand (pers. comm. Promor) provides tantalising evidence of deliberate
 fungivory in one species of feather mite. He dusted the wing feathers of a
chafinch with spores of the inky top mushroom (Coprinus sp.) and later
removed the feather mites and observed that their guts were black with the
fungal particles.
Some observations suggest that feather mites may benefit their hosts by
cleaning feathers of fungus. Blanco et aL (1997) looked at Gabucinia drfibata
(Gabuciniidae) on the red-billed chough, 1.yrrhocorau pyrrhocorar Rather to
their surprise, they found a positive relationship between the number of mites
I
234
aer bird and the bird's bodv condition. The authors concluded that mites had
no detrimental and possibly had positive effects on the hosts. So most feather
mites would appear to be commensals at worse and fungus-eating m u d i s c s at
best; however, this hypothesis should be tested experimentally.
Transmission of feather mites appears to be through direct physical contact
between mite-bearing birds and their o s p r i n g or mates, or through other social
contact (e.g. communal roosting). Mire transfer usually occurs in the nest.
When the flight feathers of young birds are 50-7596 developed, mites transfer
from the parents to the fledglings (Atyeo & Gaud 1979). According to Gaud
and Atyeo (1996), parasitic cuckoos whose young are raised by small passerincs
do not acquire the feather mites of the foster parents. Rather, they pick up their
acarofauna later in life through sexual and social contact with other cuckoos.
However, the African diederic cuckoo, Chrysococcy: capn'w, has been recently
found to acquire feather mites and lice typical of their ploceid weaver foster par-
ents (Lindholm et aL 1998). Adult cuckoos additionally host four species of
mites and lice specific to them that are presumably contracted socially.
Plumicolous feather mites can move among fathers on the same host with
relative ease. However, many syringicolous species are too large as adults to move
out of the quill of a feather. Rather, they have modified migratory stages that
move from their natal feathers to colonise new sites. In the Ascouracaridae, the
skinny larvae are the dispersal form. They escape from the quill of wing and tail
feathers by chewing through the feather wall, travel on external feather surhccs
and enter the superior umbilicus (a small hole at the partway up the feather) of
developing feathers (Gaud & Atyeo 1996). Adult ascouracarids, in contrast, are
dumpy, weakly sclerotised and have no means to escape the quill. Not all bird-
dwelling mites travel between hosts under their own power. Some species in the
dermicolous Epidermoptidae have females that are parasites of hippoboscid flies,
themselves parasites of birds: nymphs and males remain on the host.
Atyeo and Gaud (1979) calculate that if every species of bird has an average
of two mice species there must be at lcvt 18 000 species of feather mites. This
may be a conservative estimate, as some species of birds have many more than
two feather mites. The green conure, Arutinga hofochlora, is an extreme example,
hosting at least 25 species of mites (PCrez 1997). Although there may be many
species of mites on one species of bird (Figure 9.5), any given species of feather
mite tends to be host specific. Part of the reason for host-specificity must be the
mode of transmission, which is typically betwecn socially or genetically related
individuals. But another answer lies in morphological adaptation to feather
structure, which differs greatly between bird species. Feather structure also varies
within an individual bird. So, it is not surprising to find that when different
species of feather mites share a host, they each occupy a limited area of the
plumage. This partitioning into microhabitats allows many species (even con-
generics) to co-occur on the same individual bird (PCrcz & Atyeo 1784b).
Acyeo and Perez (1988) examined site specificity in three species of
RhYtidekzsmu (Pterolichidae) from the green conure. They found that R.
mesonzcx~'r~m~ was most common on primaries 7-10 and had smaller 'popula-
tions' that coexisted with R cornigera on the inner primaries and secondaries; R.
urophila was restricted to the retrices of the tail. Eggs are glued to species-spe-
cific locations on feathers (PCrez 1996). Likewise, Choe and Kim (1989) exam-
ined how microhabitat selection allowed coexistence of analgoid feather mites
on seabirds. Different inscars and sexes of a given species also occuav different
microhabitats, e.g. in kiwi-dwelling fiwiufgc~(~nalgidae),
the feathers and female nymphs live in cutaneous pores.
male nymphs live on
'2
I
235
Habitat partitioning occurs inside feathers as well as on them. Kethley
(197 1) was intrigued by the h c t that a single bird specics may host four species
of quill mites (Prostigmara: Syringophilidac). Syringophilids live inside quills
and feed by piercing the wall of the quill with their long needle-like chelicerae
to feed on tissue fluids on the other side. In small feathers of the house sparrow,
Parser domesrim, Kethley found on average 120-130 Syriingphiloides minor. In
the large covert feathers there were only 90-95 mites, although one would
expect more because there is more room. Primary feathers are even bigger and
they contained no mires or only dead ones. Kethley felt that the answer to this
nlysrery and the explanation for multiple species of syringophilids on one host
lay in the rhicknw of the quills. Primary feathers have the thickest walls and, if
the cheliceral stylets of the mites are coo short to reach through the walls, then
the population will fail, leaving only corpses to record their attempt. However,
quills too thick for mit:orwould be suitable for syringophilids of a different s h .
Kethley noted that across different species of birds, large mites live in large quills
and small mites in small quills; if large and small quills occurred on the same
host, there were oken two sizes of quill mitcs. Kethlcy concluded that variation
in quill wall thickness probably accounts for the diversity of quill mite sizes,
which range from 0.0014 mm3 to 0.0866 mm3 in volume: a 61-fold range.
. Figure 9.5
The anay of feather mites 3 , --- -
I
lathornr. Megapod~idae).From l e k t o right- Ascetolrchus ruidus. Gontoduws sp.. Letpobtus sp.. Ech,nozonus
leurophylfus. E. longtsetosus (all Pterohchidae). 1
 Although some feather mites leave the bodies of dead hosts, many remain on
and in the feathers until they themselves expire. Because of this tendency to stay
on the host's body, much taxonomic work on fiather mi= has been accom-
plished through the examination of museum skins. To collect syringicolous
species one must cut open the feather shaft As museums frown on the dcsauc-
don of fiathers, it is typically only the plumicolous mites that are extracted fmm
prepared skins. Gaud and Atyeo (1996) mention that plurnicolous mita can be
collected from live b i d by placing the bird in a bag and shaking it together with
diatomaceous earth or by dipping individual feathers in ethanol. Walther and
6 Clayton (1997) suggest dusting birds with pyrethrin to agitate their anhropod
symbionts and then ruffling the bird's fkathers over a collecting surface. One
feather mite w o k seams living birds on their backs and examines the wings
under a portable dissecting scope.
Fish, amphibians, reptiles and the mystery of mite
pockets
In contrast to warm-blooded vertebrates, fish, amphibians and reptila do not
host a huge diversity of mites. Perhaps this is a reflection of the watuy habitat
of the first two groups and the relatively low diversity of integuments modifi-
cations of all three.
..
Mat, if not all, reports of mites on fish represent incidental associations. Water
mim some'timessurvive ingestion by fish (Cupp & W i 1982) and may be mis-
taken b r internal parash. Water mite larvae havc been illustrated attached to
young fish (Soar &Williamson 1925, plate III) but this appears to be a very rare
occurrence,as Smith and Oliver (1986) do not include fish in their exhaustive list
of host-larval associations. Proctor ctaL (1997) discuss the numerous observations
of fish-associated acarids and histiostomatids (Astigmata), spurred by their discov- are popular hosts of chiggers (Trombiculidae). V a t a r a r specialises
uy of Himortornu unguilLuum and a member of the acarid genus Schwiebca on
leeches sufkring from parasitic water mould (Oomycom). Nisff'osfw~ mguidrum
had also been recovered fiom eel tanks in Europe and some other munben of the
same subgenus (Icht~octur)h m fish aquaria. Schwirbco anrrdai was collected
fiom wild and &med trout in Spain Proctor ct aL (1997) suggest that fish-asso-
ciated astigmaans may be attractad to animals of any sort that are parasitised by
water moulds. However, it may also be that mites turn to fish when their normal
tbod supply runs low. Unterglasser (1989) notes that the aquatic oribatid
Tn'rnaCacoonotbr~~(Malaconothridac) is found on the skin of aquarium fish when
their normal fbod of algae, fungi and deuitus has been depleted fbr several weeks. chigger inthstation in order to concentrate and minimise the damage caused by
(b) Mita associated with amphibians
There are a number of mite associates of amphibians. Species of the ixodid tick
genus A m b f p m a and argasid genus Ornithodom will fixd on a m p h i b i i
( h a1978, Klompen ct aL 1996). Larvae of the water mite T h r r m a ~ ~ ~ ~ hrest floor and three that were arboreal. All had poplitd folds but only the ter-
m&is (Thermacaridae) parasitise t o a b (Smith & Cook 1991), making it
the only parasitengone other than chiggers (Tmmbiculidac and Lecuwen-
hwkiidae) to fbod on vertebrates, Among terrestrial parasitengones, larvae of
Hannrmania (Tmmbiculidae) arc intradermal parasites of frogs and salamanders
(Kranu 1978). Ercynetidae (Prostigrnata) occur in the respiratory passages of
toads and frogs as wdl as of birds and mammals (Krane 1978).
(c) MitcJ arsoriatcd with rcptih
Snakes, Lizards and turtles have an interesting array of ecto- and endoparasitic
mites. Terrestrial rcpdes are often heavily parasirised by ticks and there are some
ticks on marine snakes and iguanas (see page 134). Hoogstral and Kim (1985)
feel that the Ixodida evolved as parasites of Reptilia in the late Paeowic or early
Mesowic era, about 225 mya; however, thii is questioned by Klompen et aL
(1996). The fgct that some ticks are specific to particular species of reptiles pro-
voked a lament from Durden and Kcirans (1996) on the diminishment of ti&
diversity concomitant with the potential extinction of Komodo dragons and
Galapagos rortoises. One of these tortoise ti&, Ornithodom ha-, 2
oviposits on its host, making it the only member of the Ixodida to spend its
entire life cyde on the host (Klompen eta[ 1996).
A number of fhiiics and subfamilies of Mesostigmata specidise on reptiles.
Members of the Ixodorhynchinae, Omentolaelapinae and Entonyssinae
(Laelapidae) are parasites of snakes (Domrow 1987). The first rwo subfkilies
are external parasites, while the enronyssines live in the lungs of their hosts.
Ophionysnu (Macronyssidae) and Ophiomegisw (Paramegistidae) fied on the
blood of snakes and lizards.
Within the Prostigrnata, mites in the W y Pterygosomatidae parasitise
lizards. 13tclygosoma mutabiCiz, a parasite of agamid l i , has a l l of io life stages
on the host except for eggs, which arc deposited on the lizard bur roll off
( M o d 1974). N c d y hatched P. mrrrpbicir larvae dimb aboard a passing lizard
and race randomly over its body, evenrually crawling under a scale and feeding
on blood. Himtie& pyn$irmir, a pterygosomatid parasite of the chudcwalla
lizard Sauromnlus variur, may transmit haemogregarine blood parasites (Newell
& Rydcman 1964). A number of genera in the Cloacaridae inhabit the doacal
mucosae of freshwarer turtles as well as the connective tissues of rodents, insec-
tivores and owls (Camin ct ! a 1967, Fain & Smiley 1989). Lizards and snakes
.
~~ on the respi-
ratory passages of marine iguanas and sea s n k , where it undergoes remarkable
neosomatic growth.
Lid-associated chiggers were the subject of a recent heated debate. 'Mite
pockets' are small invaginatiom in the skin around the neck, axillae, p i n and
postfemora of l i d s that are often packed with chiggers ( h o l d 1986). These
podcets are present in a wide range of taxa including the Iguanidae, Chamae-
leonidae, Gekkonidae, Lacerridae and Scincidae. Arnold (1986) noted that the
skin of the mite pockets is elastic, rapidly healing and is subtended by dense con-
centrations of lymph cells. He felt that these skin folds evolved in taxa prone to
the keding mites.
Bauer et d (1990) tested Arnold's hypothesis with the gedw genus
Rbacoahglrrrlrrr These lizards havc pockets at the backs of their thighs termed
poplittal folds. Bauer et d examined fbur Rh-h species, one from the
restrial species had chiggers in them. They that thc folds were phyloge-
netic baggage (or spandrels srnru Gould & Lewontin 1978) rhat were
opportunisticallycolonised by the chiggerswhen gcdros inhabited mite-infated
terrestrial habitats. Arnold (1993) responded to their criticism by suggesting that
Bauer rt d ' s sample sizes were hr too small to demonstrate the absence of chig-
gers in arboreal species of R h u c o ~ l u cAlthough
. Bauer rt at! (1993) admitted
M I T ~ECOLOGY,
~ : EVOLUTION
A N D BEHAVIOUR
that sample sizes of 1-5 individuals were indeed too s m d to statistically back up
their claim, they argued that phylogenccic constraint was d the best ~ p l a n a -
tion for mite pockets in lizards. They point out that Arnold has no evidence that
concentration of chiggers reduces t o d damage incurred by infested lizards and
ask whether he would consider that scales evolved to shelter the ptcrygosomatid
mitesthatasoinklizards.
Humans who have e x p u i c n d chigger infestations will have o b m e d that
the subsequent itchy welts are concentrated around waistbands, & of socks
and elasticid smp of undergarments. Like mitc pockets, these areas am pro-
teaed from abrasion, sheltered fiom direct sunlight and maintain high humidi-
ty. So, although it is possible that sequestering chiggers in a rapidly healing
region may be better than having them attach everywhere, this idea is unproven;
it seems more likcly that 'mite pockets' of lizards have evolved for sauaural rea-
sons unrelated to mice parasitism and only coincidentally provide an ideal habi-
tat for the l a d mites.
EFFECTS O F PARASITIC MITES ON THEIR
HOSTS
Parasites gain their livings from their hosts and, if the cost to &.host is high
enough, reciprocal changes in both host and parasite over evolutionary time
(coevolution) may take place &fore dealing with any evidence of wcmlution.
however, we present an overview of host susceptibilityand the damage that mites
can inflict.
Differential host susceptibility to parasitism
Hosts may vary in rheir resistma to parasitic mites for a rang of reasons, some
rcprrsenang adaptations and same that may be pure happenstance Mites them-
selves may avoid certain individuals or some potential hosts may escape para-
sitism through behavioural or morphological characteristics that discourage
mites.
(a) Mi@ choice of hosts
It would obviously be advanmgeous for a mite to choose the best host. In the
most geneal and trivial sense, this involves choosing a host of the correct taxon.
More specilically, a mite may be hced with choosing among a number of wn-
specific hosts, some of which may be 'better' than others. We have already dis-
cussed how water mitc larvae rdy on their host returning to water so that they
may drop off into an aqueous medium Funale hosts are thought to be more
Likely to return because they must oviposit on or in water, however, there is no
dear evidence that water mite larvae discriminate between host s w s (Smith
1988). However, in both water mites and their terrestrial parasitengone relatives,
the distribution of larvae on hosts is typically a negative binomial: many hosts
have no mites and a fiw hosts have many. How does this dumping come about?
Although much of it is likely to be phenologid or environmental (see fi]
below), thcrc is laboratory evidence that parasitengone larvae prefer already par-
asitised hosts. This congruence of choice may occur because such hosts are dose
to moulting (Smith 1988) and so reducing the waiting time until a new, sofi
integument is presented. It may also be that larvae are trading off a possible loss
in nutriaon due to overcrowding with the inumscd probability of finding a
mate at the end of the journey (Zhang 1992). In this latter case,it is the fact that
the host already carries a conspecific mite that makes it attractive to other larvae.
Stronger evidence f$r adapavc host choice comes fiom mesostigmatans
phoretic on bumble bees. AU stages of Pa1yuitcllurfircorum(Paasitidae) live in
nests of Bombus species (Apidae). Huck et af (1998) h n d that phoretic deu-
tonymphs would switch fiom male bea to queens but never from queens to
males. Deutonymphs also appeared to pr&r queens o v a worker-caste f k d e s .
Because bumble bee colonies are annual and young f6.sdlised queens are the only
overwintering stage, chis prcfirrndal attachment makcs sense
(6) EEobgkal avoidance of mites
Although-tempting, it is o L specious to postulate that ecological characteris-
tics of a host species (habitat p&ct, phenology) are adaptations to avoid
mite parasitism. The bllowing examples involve characters that a i k t the prob-
ability of encountering parasitic mias, with no imputation of adaptation.
Pruett-Jones and Prum-Jones (1991) examined ko& (Ixodidac) tick infes-
tation of 115 species of New Guinean b i d . Non-passcrines (161 individuals)
had a very low infbtation rare (only 1 individual of 1 species) but passcrines
were higher (385 of 2496 individuals). Those passerine species foraging on or
near the ground wem harder hit, suggesting thac species foraging higher in the
canopy were able to avoid qucsting ticks, which tend to stay on the ground or
in low vegetation. Smith and Mdvcr (1984) d c d factors influencing host
selection of Acdes mosquitoes by Amnun*r water mites. As well as behavioural
fittors (see [dl below), thcy fbund that two species, A. cornmum3 and A. punr-
tor, wue much more susceptible to parasitism in the lab than thcy wur in the
field; this was because in the fidd, the mites and mosquitoes did not overlap
temporally. Smith (1988) describes patterns of parasitism by larvae of Eylais
water mites on water boatmen (Hemiptcra: Corixidae)).Cmwrnrixa arpkta and
C b$Mz inhabit inland saline waters, the £irst species occurring in d t i a water.
Smith mgpts that C acpkta may be restriacd to these habitats because they
s&r more when parasitised by Eylair c1ctyhPlina and the mite cannot deal with
very high sdinities. In a rare test of ecological avoidance of parasitism, Som rt
at! (1997) examined whether the lizard Lucerta Yivipana avoided either wn-
specifics para~itisedby 0phw"yw or resting sites previously occupied by para-
sitised lizards. Convary to their expectations, they found that unparasitiscd
lizards did not discriminate against individuals or sites associated with mites.
(4 Pbysiologicdl * C S against mitm
Davids (1973) n o d that when larvac of the water mite H w h cbnjc~ta ~ bite
bQdcswimmers (Notonectidae) that arc not their normal host, the bug's
haemolymph reacts so strongly to the d i v a that the mites' mouthpam arc
obstructed, they cannot feed and soon die. Pruetc-Jones and Pructc-Jones (1991)
fbund that non-passerine birds had lower inkstation rates by ticks than passer-
ine~.They believe that non-passerines, b c i i on a v e w longer lived than passer-
ins, acquire a greater immunity to cidrs and thus s&r lower tado ow. This
is not a h-k&cd hypothesis. %he study of host immunity to ti& is a growing
field Brossard and Wikel(1997) and Wikel and &reman (1997) discuss innate
and acquired host d&cA ag& ti& and the coLtCrmCaSUICS mounted by
these parasites. The world's first vaccine against an ectoparasite, the cade a&,
Boophifns microph (Ixodidae), is being uialed in Australia (Willadsen 1997).
As well as their obvious practical value to grazius and veterinarians,
interactions between the host immune system and ectoparasitesare of great inter-
est to behavioural ecologists working on tradeoE between sexiness and survival.
The 'immunocompetence hypothesis' predicts that males producing a high level
of testosterone s d k a tradeoff becwecn expression of secondary sexual characters
and exposure to parasite infksrarions. Salvador et d (1996) tested this hypothesis
in a population of the lizard l3atmwdromrcs &rus during its mating season.
They found that males i m p l a n d with testosterone devdoped larger patches of
orange colour and behaved more aggressively than did control males. Although
the tick load of all individuals i n d over the season, testosterone-implanted
males s d k d a p t u increase than did controI males. Weatherhead et aL
(1993) kund a positive comlation betmcn the number of D m ~ ~ l y z n r z
(Dermanysidae) mites on male red-winged blackbirds (AgeLu'~~phomiccuz) and
both testosterone level and the length of the d e s ' epaulets (the red shoulder
patches that giw the bird itp name). However, similar correlations were not fbund
with any of the other parasites (lice, gut flukes, blood protozoans), nor was there
an overall e l k t of testosterone I d on male secondary sexual characters.
Saino et aL (1995) manipulated testosterone levek in male barn swallows
( H i d h a ) to determine its &on tail length and burden of parasites.
including the nest mite Omintbo"ym*cbwsa (Macronyssidae). Resulcs were
unclear due to small sample siza but testosterone implanu did not seem to
affkt nest mite numbers. This is not surprising, considering that 0.bursa prob-
ably ficeds primarily on ;chicks rather than on male parenu. One major problem
with studies linking parasites, testosterone and plumage in male birds is that
testostuone does not determine showy male kthers. A castrated peacock is just
as elaborately plumed as an entire one (Owens & Short 1995); however, spurs,
wades and combs are under testosterone's control and would make better sub-
jects for such studies.
Another possible effect of hormones on ectoparasites is mediated through
differential moavation to groom. Mooring et at! (1996) found that territoria
male impala had higher tick loads than either Rmales or non-territorial males
and that they groomed themselves less assiduously. They were not sure whether
the reduction in grooming was the result of territoria males having less time to
groom or if higher testosterone levels physiologically suppressed oral grooming.
S c M k and Forbes (1997) tested the testosterone hypothesis by surveying the lit-
erature for male biases in parasitism of mammals. Their meta-analysis found that
it seemed to hold fbr arrhrapod ectoparasins. However, they did not appear to
control fbr body size and males may often be l q e r and hence have greater sur-
f i e area for parasites than females.
(4 Behavioural w cesagainst mites
Anti-ectoparasite behaviour is well known in vertebrates. Mites, especially ti&,
are removed by auto- and dogrooming among conspecifia (e.g. Mooring et aL
1996), and relationships with parasite-eating tick-birds. Certain avian behav-
iours such as sun-bathing and ancing, in which a bid flops on top of an anthill
and allows the insects to patrol through its kthers, are thought to help rid the
birds of ectoparasites (Brooh & Birkhead 1991).
Nesting behaviour may also have its and-mite aspects. Bum et aL (1991)
suggest that the tight weaw of bluebird nests may limit occupation by nidi-
colous mites. Clark (1991) discusses the 'nest protection hypothesis' for the
commonly observed inclusion of fronds of fresh plancs in the nests of many
species of birds. Clark manipulated starling nests by removing already included
green vegetation h m some nests (which he replaced with equivalent volume of
dry grass) and by adding some vegetation (wild carrot, which was commonly
chosen by starlings) to others. By the end of the tirst breeding attempt, nests
with wild carrot contained an average of 3000 Ornirhonyssus syiviamm
(Maaonyssidae), whereas nests without contained an average of 80 000 mites.
By the end of the second breeding attempt in June, nests with wild carrot con-
cained an average of 11 000 mites, whiie nests without contained approximate-
ly 500 000 mites; this is strong evidence in &our of the nest-protaction
hypott~esis.
Anti-mite behaviours as0 ocau in invertebrates. Cowan (1984) notes that
femae larvae of the cumenid wasp Ancirtronn*s antilope kill the hncchirCl;r
nirct~saWi&dtiidae) in th& brood cells prior to pupaaon so that they
emerge as mitc-fcee adults. However, as the male larvae do not kill their mites,
W e wasps end up being inkted by K sctosa through venereal transmission
during mating. Cunliffi (1952) discusses the interactions of the pacasite
Pimeliapbilut podapohpopbagus (Pterygosornatidac) with its cockroach horn.
Cunliffe observed up to 25 mites, each up to 1 nun long, on the body of a sin-
gle coach. After about one hour of such heavy parasitism, the roach ML over on
its back and thrashes about h r several hours befbrc dying. He notes '[ilt has been
observed that roaches engage in apparent combat with the mites. Fifeaen or so
mites have been seen h d i or riding along on a roach when suddenly the
roach will succeed in grasping some of &e mites with its front legs and mouth-
pa-. One or two, or somctima thm, mites may become involved, until either
they escape or the roach finally manages to swallow them.'
Water mice larvae are ofcen the catget of anti-parasite behaviour. Wdes
(1987) observed adult CbtmbonrrfLu,icrrm(Diptera: Chaoboridae) under attack
by Hydrodrormr dcrpicimr larvae. The flies kicked, stamped, jumped, combed
and b d their wings. Once f e d flies began ovipositing, however, they
ceased their anti-parasite behaviour and mite larvae mounted them with
impunity. Baker and Smith (1997) observed that larval damselflies may resist
pa&tism by Amuruswater mite h e by grooming, crawling, swimmihg and
s d n g at the mites. Smith and McIver (1984) found that pupae of the culicid
h C s c i n m were able to avoid or dislodgc mite larvae before pre-parasitic con-
tact was established by vigorously straightening their abdomens or by swim-
ming. When t h e pupae were anaesthctised with COZ, the proportion of
suaesfU wncacrs rose from 0.013 to 0.499. Other culicid pupae which did not
exhibit avoidance movements were more likely to be parasitiscd
The evil that mites do: adverse effects of acarine
symbionts
It is o h stated char a wd-adapted pansite does not harm icr host (Toft &
Aeschlimann 1991). Numerous studies of thc effbrrs of mite symbionrs on their
hosts have shown no or little negative impact. This has led some to daim chat
such mites are the ones 'best adapted' or 'longest associated' with the host: in
Nutting's (1985) words, 'least damage, longest domiciled'. Generally benign
symbionts include dunodicid mites of mammals (Nutting 1985) and most
mites dwelling on the external surface of feathers (e.g. Gaud & Arym 1996).
However, if a symbiont's goals am best met by an action that harms the host,
MITES:ECOLOGY,EVOLUTION
A N D BEHAVIOUR

then there will be little selection for benign behaviour (Herre 1993).Some of the
negative e f h of symbiotic mites are easily predicted, e.g. one might expect
chat a heavy load of blood-sucking ti& would cause anaemia in their host. But
many of the side &cts of carrying mites are not as obvious. It is not only the
nasty parasites that can harm their hosts but also seemingly benign phoretic and
nidicolous mites (Table 9.3). In many of b e latter cases, it seems likely that
the mites receive no benefit from their inadvertent negative impacts.
(a) Eficts ofnon-parrzzfrrZZftic
nidicohus mim
Nidicoles associated with stored products may spoil food through their excre-
dons, increased humidity or dispersal of fungal spores. The &ces and bodies of
these pests can result in allergic skin and respiratory reactions in humans.
 I (b) Effects ofphoretic mites
Carrying one or two phoretic mites is probably no great hardship for any ani-
mal; however, heavy loads or mites lodged in inconvenient locations can adverse-
ly affect the carrier. Inhibition of movement -walking or flight -due to mite
burdens has becn documented for beetles, gnats and a lizard (Table 7.3). In the
lizard's case, an encrustation of hundreds of uropodine deutonymphs resulted in
its eventual death (Domrow 1981).
Other activities may be made more difficult by the presence of phoretic
mites. Moya Borja (1781) documents the effects of phoresy by Maerocheks mus-
244 caedornesticae (Macrochelidae) on the human bot fly Dermatobia hominis
(Cuterebridae) in Brazil. Larvae of this fly are serious parasites of mammals,
including humans; however, they do not oviposit directly on their hosts. Rather,
female D. horninis capture other mammal-associated flies (mosquitoes, house-
flies) and oviposit on the belly of the press-ganged insects. When the egg-laden
fly lands on warm mammalian skin, the eggs hatch and little D. hominb larvae
drop onto the skin of the host. Moya Borja found that hitchhiking M. muscae-
dornesticae interfered with the reproductive success of D. hominis in two ways.
First, because the mites tended to cluster around the venter and genital regions
of both male and female, they hindered copulation. Secondly, they affected the
female fly's ability to capture and oviposit on other flies. Similarly, Iverson et RL
(1996) found that deuronymphs of Lardoglyphus zacheri (Lardoglyphidae)
attached to dermesud beetles in such huge numbers (>500/beetle) that the hosts
were incapable either of mating or of feeding, resulting in the eventual extirpa-
tion of beetle colonies. A more indirect effect of phoretic mites on their hosts is
the competition for food between hummingbirds and the Proctokzekzps mites
(Ascidae) they ferry between flowers (Colwell 1775).
(c) Effects o f parasitic mites
These range from the mildly irritating to the horrific (Table 7.3). Like phorecic
mites, a heavy load of parasites can hinder host movement. This reduced motil-
ity can affect mate-searching ability (Forbes 1991). Effom to avoid parasitism
can also have ill effects. Baker and Smith (1777) found that the anti-mite
grooming activity of larval damselflies put them at greater risk of predation from
visually hunting fish. Feeding activity can cause local tissue damage. For exam-
ple, pedipalps of the water mite Unionicokz intmnedia are sunk deeply into the
underlying connective tissues of the gills of its mussel host causing edema of the
gill filaments (Baker 1777). Mitchell (1765) mentions that Najadirkz ingens,
which can grow up to 64 mm3 in volume, commonly destroys host mussel tis-
sues and causes the mollusc to generate papillate grow&. Feeding by the uropo-
did Furcouropoda murgimtaon the epidermis of slugs reputedly causes wounds
that become necrotic, eventually killing the molluscs (Raw & Panigtahi 1771).
Parasitic mites may remove a large amount of nutrition from their hosts, as
exemplified by the degree of engorgement attained by some larval water mites
(Figure 7.6). Parasitism of juvenile hosts may be sufficiently intense as to slow
their development. This has becn demonstrated in a variety of aquatic insects
parasitised by water mites and in birds besieged by nest mites (Eablc 9.3).
However, other studies of nest mites have shown no clear effects of parasitic
mites on nestling growrh or survival (e.g. Bauchau 1997, Pacejka et al. 1778).
Water mites in the genus Hygrobates attach to the skin of adult midges by biting
through the integument of the pupa into the skin of che developing adult and
are pulled through the exuviae when the adult emcrges. Ullrich (1976) noted
chat heavy loads prevented moulting because the midge lacked the strength to
pull so many mites through its skin.
Fecundity of adult female hosts is reduced by parasitism in a wide variety of
host taxa from chickens to mosquitoes. Male reproduction may also be affected,
through lowered sperm count (Clark 1771), smaller testes (Polak 1998) or
reduced mate-searching ability (Forbes 1991).Adult lifespan has been shown to
be reduced by mice parasitism for many groups of insects (Table 9.3). The effect
is usually dependent on mite load. Larvae of the trornbidiid Aflothrornbiumpul-
vinum kill their aphid hosts when the mite load is two or more (Zhang 1798).
W ~ t honly one mite larva per aphid, development is halted for nymphal hosts
and reproductive rate slowed for adult hosts.
Finally, parasitic mites can be affected by other mites on the same host. The
'crowding effect', first noticed in tapeworms (Read 1751), is the reduction in
mass and size of individual parasites with the increasing number of parasites per
hosc. The crowding effect has been observed in water mite larvae. Davies (1959)
noted that Sperchon larvae are larger when fewer are present per black fly hosc.
Lanciani (1784) d s o observed this in Hydrachna virefkz larvae parasitising back-
swimmers. The size of the host affected this relationship in rwo ways. First, the
larger the host, the smaller was the crowding-induced rate of decline in mite size.
Secondly, the larger the host, the larger was a given larva at any number of mites
per host. I t seems likely that crowding-induced
" decreases in nymphal size result
in a smaller reproductive output when a mite
reaches adulthood. However, crowding in
the l a n d stage may not he selected against if
the loss of fitness due to the inability to find
a host is greater than that caused by feeding
from a crowded host and reaching less than
maximum s i x (L~nciani1976).
Parasitic mites and mate choice
by hosts
Female animals often appear very particular
about which male they will accept as a mate.
The rationale behind this choosiness is likely
to vary among taxa. If a male provides sole
parental care for the young (as in many fish),
females may choose on the basis of the qual-
ity of the male's spawning grounds. If males
provide tasty nuptial gifts as a maung incen-
tive (e.g. scorpionflies, many orthopterans),
females may choose on the basis of the gifr's
size. But if the male offers no obvious service
or goods (most invertebrates and many ver-
tebrates), why should females care about
whom they mare with?
The 'good genes' hypothesis suggests that
females may choose among males on the
basis of the heritable rndowmcnt passed on
MITES: ECOLOGY,EVOLUTION
AND BEHAVIOUR
to their joint oflipring, i.e. high-quality males should sire high-quality oflipring.
Many studies have shown 31at finales tend to choose the brightest and most
ornamented of males but it is unclear how this reflects good genes. Hamilton
and Zuk (1982) s# that showy ornaments in male birds reflect an indi-
vidual's genetidy based resistance to the current array of parasites afkaing a
population. By choosing the bsightest male, a f&de selects a genotype that,
when confkrrcd to her oflipring will protca them from parasites. Although
osigkdy proposed for internal parasites, the Hamilton-Zuk hypothesis has
been extended to include ectoparasitic anhropods.
Tests of the parasite hypothesis have involved both comparative multi-
species approaches and single-species studies. Pruett-Jones and Pruett-Jones
(1991) surveyed 115 species of birds h m New Guinea to determine whether
there was a correlation between male showiness, blood parasite count and id&-
tation by ticks (kodcs spp.). Neither kctor correlated with ti& load and they
n o d that sexually dichromaticand monochromatic species sufkred simiiar lev-
els of parasitism. This is not an uncommon finding in comparative tests of the
Hamilton-Zuk hypothesis and may stun h m a basic uncertainty on what the
hypothesis predicts (Harvey et aL 1991). Should species with showy malts have
mure associated parasites (indicating currently acting selection fbr resisrance) or
should they have j b e r (indicating succtssll past selection for an d k t i v e
immune system)? A dearer prediction is that within a given species, highly oma-
mented males should have fewer parasites; conversely heavily parasitid males
should show poor development of secondary sexual charactus.
Mallet (1991) studied the relationship between Omitbonym b u m
(Macronyssidae) and 'attractiveness' of mak barn swallows. One measure of
acaactiveness is whether a male is successfid in attaining a mate. Msller found
that mean mite load for males with mates was 5.7 compared to mean of 10.7 fbr
unmated males. Male barn swallows display a presumably sexually selected traio
tail streamers longer than those of the female. Meller also states that mite loads
were negatively correlated with male tail length. Darolova er aL (1997) observed
a negative &tionship between mask width of male pcnduline tits and loads of
mites in their nests (Dmnanyrnrshirundinis and Otnithonyrnrs sylyiarum). Mask
width expresses age and dominance, and female tits tend to choose wider
masked males. Darolova et al conclude that the sexually dimorphic trait may
indicate male quality, including the ability to avoid parasites. In contrast, Burley
et aL (1991) fbund a positive &tionship between brightness of bii in zebra
finches and their loads of lice and mites. Thcy suggest that birds with brighter
colouts may have more social contacts and get more parasites or chat parasites
do better on brighter birds for unknown reasons.
Females may be interested in knowing male parasite load, not for the bene-
fit of their o@ring, but to avoid contagion themselves. Sexual uansmission of
mites has been observed in wasps (e.g. Cowan 1984) and Hum e t d (1995) sug-
gest that the ohen vigorous male-spumingbehaviour of funae ladybird beeda
(Co&ellidae) is to avoid transmission of the parasitic mite Coccipolipw
(Podapolipidae). Thompson et al (1997) bring up an interesting point in their
study of B ~ ~ ~ ~ p h y I lfiather
o d e s mites and showiness of male house finches. The
authors examined mite load and plumage brightness in males before and afkr a
moult. Males with no or f k mites pre-moult increased in rank of plumage
bsighmess a f k moult, while heavily laden males decreased in rank They argue
that many studies that correlate parasite load with current male condition are
flawed because the plumage developed under previous, not current, mite condi-
tions: '[tlhus, females that avoid males for a direct reason such as fear of conta-
gion would not find male plumage adour at the time of mate choiu in spring
to be an accurate indicator of pat.asicc load at that time'. As mentioned previ-
ously, it is not clear whether fkather mites like hc~ophyICodcrare parasites, com-
m e n d or mutuaists, although there is more evidence fbr the b two
relationships (see page 234). As Thompson et rrl. (1997) found that mite load
was positively correlated with avian pox, it may be that the pox rather than the
mites were responsible fbr altered plumage condition.
A negative relationship between mite load and mating frequency may not
indicate that parasitised males are chosen less often by fkndes. Rather, it could
be that parasitised m& have l o w e d testostcmne (eg. roosters, Clark 1991) and
hence axe less motivated m mate, they may be sGed and have less energy to
u p a d on mate-searching (e.g. damsdies, Forbes 1991) or the presence of mites
may physically hinder copulation (e.g. drosophilid flies, Polak & Markow 1995).
A reant h i in evolutionary biology is the use of morphological syrmmeqy as
a measure of an individual's genetic health and hence desirab'ity as a mate.
Fluctadng y e t r y (FA) is a m M u r of a d , random deviations b m per-
k symmeay m a b W y or radially symmeaic charaarc. Asymmeoy is prc-
sumad to be the rcsult of 'urors' during the development of a structure. The 'less
fit' an individual's genome, the more errors it will make during development and
the more asymmetricalthe organism wiU be FA is a population-Id measurement
but is o h mistakenly used to & to asymmetry in an individual organism.
A number of studies have indicated that males with more symmetrical oma-
ments are more successfd in attaining mates (summariscd in Polak 1997).
Parasitic mites may have two roles in asyrnmeuytrelated sexual selection. First,
less symmetrical (= less fit) individuals may be less able to prevent infestation by
parasitic mites. Second, parasitism by mites may k the development of a
juvenile so that it grows into an asymmetrical adult. Maller (1992) d p u l a t -
ed loads of u o p i d hwl mites (Omithonyuu~buna) by adding or moving
mites from nests of the swallow Hirundo lUStjCa Asymmeay was measured in
the subsequent year A e r the swallows had grown new tail ornaments under the
altered parasite regime. Asymmetry was larger at i n w i n g levels of parasites fbr
male tail length but not h r the length of the shortest tail feather or for wing
length. Parasite load did not &'tail or wing length in W e s . Msller suggests
that the degree of asymmeay in tail ornaments reveals the level of parasite id&-
cation in males and so it can suvt as a vehicle fbr female choice (but see the com-
. ment on moulting phenology by Thompson et al (1997) above). However,
Dufbur and Weatherhead (1998) fbund no relationship between symmetry and
quality of male red-winged blackbirds, except that symmetrical males carried a
higher load of Ornitbo'fyuuzsyfviatl(m(Macronyssidae) than did less symmetri-
. cal males, exactly the opposite of what Meller (1992) predicts.
Bonn et d (1996) fbund a comktion between asymmetry of fbrc wing
length in damselflies and load of parasitic Amnuru~mites. There was no corn-
lation between mite load and cell number in the fore wings. They fbund no evi-
dence tfiat 'fitter' (= larger) individuals had lower mitc loads. The authors
suggest chat stylostomes may interfk with blood pumping into the wings at
adult edosion but that mite parasitism would not alter cell number, which is
determined befbre the parasitic impact, They point out that while most -la-
nations fbr increases in 'FA' implicate environmental sness combined with the
 I
MITES:
ECOLOGY,
EVOLUTION
AND BEHAVIOUR
I
inability of the genome to stabilise the phenotype, their results suggest that
asymmetry a u l d result from very short-term impacts due to chance parasitism.
However, there is evidence that mites & symmetry through very indirect
mutes. Polak (1997) bund that female drosophilid flies parasitised by
M ~ o c h e k subbadills
s produced sons with more asymmetcid bristle-placement
relative to sons of non-parasidsad lknales. He suggests that mite parasitism may
alter provisioning to eggs during ova development However, Polak found no
evidence that bristle symmetry &ed male mating success.
The effect of parasites on sarual selection, host development and host
immunology are kcinating to contemplate (e.g. MeUer & Saino 1994).
248
However, because parasite load may be the result, rather than the cause, of
differences in host morphology and physiology, and may even result fiom
host mating success (e.g. transfer of mites during mating in birds and insects),
these hctors seem impossible to tease apart purely by correlational studies.
More strictly controUcd experimental approaches, such as those of Clayton
and Tompkins (1995) on nest mites of rock doves (Columba liuia), are
essential.
MITE-HOST COEVOLUTION: ANY EVIDENCE?
'Coevolution'was coined by Ehrlich and Raven in 1964 in a discussion of the
influences that plants and insects have don each other. Their origins def-
inition was somewhat vague and authors using the word thereafter have given it
their own spins. To fbresd semantic arguments, Janzen (1980) defined tocvo-
luaon spec if id^ wevolution occurs when a trait in one species evolves in
response to a trait in another species, whose uait itself evolved in response to a
trait in the first species. Thus coevolution is a reciprod microevolutionary
process involving a pair of species each adapting to the other. Thii pairwise inter-
action appears to be very rare among animals, or at least hard to prove; howev-
er, there are numerous examples of gene-for-gene coevolution among plants and
their pests (Thompson 1989). A more relaxed 'diffuse coevolution' occurs when
a trait in one or more species evolves in response to a trait in one or more oth-
ers. For example, a group of flowering plants and a group of bees may be mum-
ally adapted fbr pollination interactions. The important thing is the mutual
nature of the changes. If one taxon shows adaptations to characteristics of anoth-
er, but not vice vusa, this is not coevolution but simply evolution (Furuyma &
Slatkin 1983).
Another use of coevolution has been to describe matched speciation events
between two ecologically associated taxa. For example, speciation in fig trees
may be matched with that of their pollinating fig wasps (Feinsinga 1983) or
that of pocket gophers with thcir lice (Hafner etaL 1994). Thii phenomenon is
morc precisely termed 'cospadationB.
Among parasitologists, the expectation of a match between host and parasite
phyiogenies is termed FPhrrnhold Rule (Brooks & M h 1993). Like dif-
fuse coevolution, uxpeciation may not occur on a one-to-one basis. Hosts may
speciate first, carryin% their assodated symbionts wirh them, and syrnbionts may
or may not develop into new species subsequently. This, too, has a parasitolo-
gist's mdnikec Manter's F i i Role is that parasites evolve more slowly then
their hosts (Brooks & McLennan 1993). As Brooks & McLennan point out.
many of these 'rules' are statements of belief that have little empirical support.
Coevolution by mutual adaptation
There is no evidence of gene-for-gene coevolution in arthropod-hon relation-
ships as there arc for plant-pathogen interactions (Kim 1985~).However, evi-
dence of coadaptation at the microevolutionary level may be the
endocrinological battle between ticks and their hosts. W~keiand Bergman
(1997) describe how acquired resistance to tick infestation can be countered if
ti& suppress antibody production in the host. More tentative support for phys-
iological madaptation is the often violent reactions exhibited by hosts when they
arc inlsted by mites they would not normally encounter. Nutting (1985) notes
that bird and reptile chiggers may cause more severe tissue reaction in humans
than do mammal chiggers, suggesting that diffuse coevolution may be at work
Eidcwort (1983) states that the miUcweed leaf beetle, Labidomera clivicouis, the
normal host of Chryomelobio Iabiriomae (Podapolipidae), can carry large num-
bers of mites without ill effect; however, the Colorado potato beede, Lq~tinotd~a
dccrmIineara, has higher mortality and lower fecundig when infested.
Deliinado-Baker et af (1992) note that the honey bee, Apis mc&j€m, has much
greater difficulty grooming off the mite knuajmbsoni than does its congener,
A. ccmna, which likely has had a much longer evolutionary history of contact
with lCjacobsoni Mosquitoes that are rarely parasitiscd by Amnunu in nature
because of phenological separaaon arc hardest hit in the laboratory, apparen!y
because they lack d&nce mechanisms against these water mite larvae (Srmth
1983). Eidrwort (1983) suggests that transplanting mites fiom one region where
they are apparently harmless to sites where their hosts have not adapted to them
may provide better biomntrol.
Such observations lead to the prediction that the greater the pathology
caused by the parasite, the more recent the association. For example. Nutting
(1985) suggests that myobiid mites are likely to be men+ or weakly coevolved
with their hosts because they tend to be more pathogenic than demodicid mites.
Considering haematophagous mites in general, Radovsky (1985) contends that
trauma associated with the site of puncture is generally not found in more high-
ly adapted groups of ectoparasites. Kim (1985~)qualifies the value of this gcn-
e d i t i o n , stating that the '[ilntimacy of host associations indicates that they are
either very old in the evolutionary sense or relatively recent but with rigorous
mutual selection and stepwise madaptation'.
While it is easy to show that a parasite is adapted to its host, for example by
the structure of its grasping appcn* or general body shape, it is dif6cult to
show the opposite. A single species of host often has many difirent parasites; so
an anti-parasite behaviour like 'scratching' is u n l i i y to be a spacific adaptation
against one parasite (Kim 1 9 8 5 T ~ i & Clauson 1985). As we& some species
of mites have more than one host, so their morphological or behavioural adap-
tations fbr parasitism or p h o r q are unlikely to be suicrly coevolved. Examples
of the first situation include the green conure with at least 25 species of fcather
mites (Perez 1997) and the scarab Copris &anus with 19 species of acarine
symbionts (Hunter & Rosario 1988). Examples of multi-host mites are: the
water mite Pro& aim& on 25 species of insect hosts, including Simuliidae,
Chironomidac and various Trichoptera (Ullrich 1976); Sarcopm stnbin' on 40
'
species beJonging to seven orders of mammals (Arlian 1989b);and m o m ym-
mmcosuz on 139 species of insects in six orders (Eickwom 1983). Any coevolution
, in these cases would have to be very d i h e indeed.
1
I
MITES: ECOLOGY,EVOLUTIONA N D BEHAVIOUR
I
Cospeciation
Kim (1985~)notes that two processes can result in association of groups of relat-
ed mites with groups of related hosts. The resource-trackhg model suggests
that the parasites track resources (types of food, types of fkeding sites) regardless
of the rdatedness of hosts. Because related species ofien share morphological,
behavioural and ecological characteristics, particular clades of mites may appear
to track particular ciades of hosts. Phylopnetic tra&ng, or cospeciation, sug-
gests that parasite dadogenesis occur in parallel with host phylogeny. To di&-
entiate between the processes, one would need to construct independent
dadograms h r host and mites and compare the branching patterns. If they show
a great deal of congruence, as in the well-known example of pocket gophers and
their lice (Hafner ct aL 1994), this supports the cospeciation hypothesis. If not,
or if obvious host-switching across completely unrelated host taxa is apparent,
then the resource-tracking hypothesis is supported.
U&rtunatelYs to o w knowkdge there are no rigorous dadistic tests of
cospeciation using rnites and cheir hosts. Claims of parallel histories are usually
supported by observations of host specificity at the species level or by higher-
taxon congruity (e.g. 'all mites of genus A are found on hosts of f$milyB'); nei-
ther rules out r e s o u r c e - d n g as a cause. Sometimes authors appear to be
selective in their observation of relationships. Fain and Hyland (1985) note that
mires of the W y Lemurnyssidae are found in the nasal cavity of the galago in
Madagascar and in noses of South American monkeys 'The presence of very
dosely related rnites ...suggests the existence of some relationship between these
primates'. But when they describe how Rhyncoptidae are found on hairs of hys-
uicid rodents, neouopical monkeys and afiotropid monkeys, and that
Audycopddae are in hair hllides of cebids, ursids and ptocyonids, there is no
suggestion that monkeys arc related to porcupines, bears or raccoons.
In fict, it is easier to find strikingly disjunct patterns of host and mite phy-
logeny than to find parallel ones. In host-switching (or -jumping), symbiotic
mites are trans- h m their n o d host raxon to an ecologically associated
but phylogenedcally distant one. After transfer, the mite may develop into a new
species and wspeciaaon with the new host mxon may occur. For example, lar-
vae of the water mite genus h u w (Arrenuridae) parasitise Odonata if in the
subgenus Amnurus but parasitise Diptera if they are members of other subgen-
era. As dragonflies and damselflies are about as phylogenetically distant fiom
mosquitoes and midges as insects can be, the association must be an example of
host-switching. An even more extreme example is pterygosomadd mites parasitic
on cockroaches, reduviid bugs and lids (Cunliffe 1952). Living in the same
habitat might have ficilitated the above host-jumps. Another way to achieve
such phylogenetic leaps would be through transfer fiom a prey animal to a pred-
ator. Gaud and Aeyeo (1996) suggest that the feather mite genus Falcolichu~,
which is hund on five species of Afiican Fako and is morphologically similar to
pterolichines that inhabit gallibrms, is derived h m a prey-t*predator transfer.
Is there microevolutionary evidence of cospeciaaon? Newell and Ryckman
(1964) note that H i d I l a p $ n n i s (Ptcrygosomatidae) fiom populations of
chudcwalla l i d on two islands near Baja California were morphologically
indistinguishablefiom those coUected on the mainland; however, populations of
the host showed marked changes.This supports 'Manter's First Rule*,that para-
sites evolve more slowly then their hosts (Brooks & Mdrnnan 1993), but
provides no evidence of incipient cospeciation. The mite Poecilochim carabi
(Parasiddae) appears to be in the process of speciating on the basis of host pref-
erence. Mites at one location in Michigan show no host preferences while at
another site they exhibit clear genetically based prefirencts between beetle
species (Brown & Wilson 1994). This difkcnce between nearby populations
suggao that the prcfkences ace evdutionarilyrecent. A similar sinucion appears
to exist in Germany (Schwan 1996). Athias-Binche n rrL (1993) report poten-
d host-based sympanic speciation in the utopodine mite Neosni*r noyus, also
phoretic on silphid beetles. However, these authors do not imply that cospccia-
tion is oearfring.as they do not stare whether the silphid bade a m each othus
dosest relatrves. So resource-tracking rather than phyiogenetic-tracking may be
the driving b r a . A more promisii example is described by Lombert (1988).
In a study of morphological difFerentiation in subspecies of the silvereye,
Zbzkrps hen&, he also perhnned a multivariate analysis of the bird's kather
mice, T ~ ~ C Cmcgadirtz
~ G I I The
I ~ rnites
Z showed morphological diffirences asso-
ciated with host subspecies, suggesting cospeciation may be in progress.
If one were to embark on a quest for cospeciation, what groups of symbiot-
ic mites would be the best candidates?Taxa containing species that have broad
host tolerances are probably poor choices (e.g. @ m o r n vcnrricosru on 139
species of insects [Eickwort 19831). Likewise, all 155 Hizemap&saliz species
(Ixodida) have a Life cycle in which hosts of immature ticks and adults are ofien
hugely different, e.g. hedgehog and fbx, shrew and yak, mouse and lion, rat and
boar, lizard and ibex, bird and bison ( H o o g s d & Kim 1985). Although these
associations might makc h r tangled cladopms, they are good names for pubs
(which are possibly the best places f$r such speculation).
Mites with less catholic tastes are more likely to show cospeciation.
Terminology for host specifiaty is prolific. Monaxcny means that a symbiotic
species fioquents only one host species, whereas polyrmy means it infists two
or more hosts. If the hosts are in the same genus this may be termed oligoxcny,
and if in f i r e n t genera in the same W y termed pleioxcny. Kim (1985a)
states that host associations of mammal-parasitic acarines are usually oligoxe-
nous or pleioxenous but that three families - Demodiddae, Myobiidae and
Derrnanyssidae - are usually monoxenous. Even in these groups, host-switch-
ing may occur. For example, predator-prey trans& of Prcltumyobia clbpamdci
may have occurred between So= cinema and its predator BlbtriM brcllicawk
(both shrews) (Nutting 1985).
Another potential clue is in the intimacy of association between host and
symbiont. Temporary parasites are associated with the host for only a short peri-
od in the life cyde (e.g. parasitengone larvae), while permanent parasites spend
their entire life cyde. on the host. Permanent parasices are more likely to be
monoxenous (Kim 1985a). Athias-Binche (1991) hypochesises that in mites
such as Adancylidiunt and Acamphmax, in which males tend to mate with their
sisters, generic d d i by &under e&cc should result in monoxenous specificity.
Any study of host specificity of parasitic mica should take the fbllowingcau-
tionary & into consideration. Downes (1990) aansplanted nymphs of the
mussel-dwclliig water mite Unionuoh CasaUci into the gill tissues of a mussel
typically occupied by a closely related species, U.poundri. Adults of these mite
species can be difhentiated on the basis of leg and seml morphology. When the
deutonymphal U.I;uaCli transfbrmed into adults, Downes fbund that they had
the legs and setae of U.poundri. Her observations appeared to represent an
 example of host-induced morphology, a phenomenon displayed by many par-
asitic trematodes, cestodes, nematodes and protozoans. Downes suggested that
host induction might explain the large number of host-specific species in the
subgenus Utrionicoliu'es. However, recent electrophoretic studies by D.D.
Edwards and his student M. Labhart revealed that U. poundti and U. Lrcaflri
exhibit futed allele differences at three enzyme loci, strong evidence that they are
indeed distinct species rather than host-induced morphs (D. Edwards, pers.
comm.). The conflict benveen their results and Downes' observations suggests
that the host mussels in Downes' experiment may not have been completely
252 cleared of their original U. poirndti nymphs. Edwards and Dimock (1997) sug-
gest that sibling species of Unionicoh such as U. h a & + and U.poundri may be
the products of host-based genetic isolation but they do not consider them to
represent host-symbiont cospeciation.
It is easy to understand why rigorous tests of the phylogenetic tracking
hypothesis are so rare. Deriving and comparing cladograms both for host t&q
and for their symbiotic mites is a daunting task, as systematic expertise in dif-
ferent classes or phyla would be required. A single person is unlikely to be, for
example, both an avian and an asrigmatan systematist. So, Mironov (1991) pro-
vides a cladistic analysis of the feather mite family Avenzoariidae but, in the
absence of a host cladogram, can only conclude that 'there are observed some
features of co-evolution of some genera of mites with some families or with
group [sic] of closely related families of hos ts...' So an acarologist interested in
testing cospeciation hypotheses would either have to team up with an expert in
the host taxon or opportunistically pounce on host cladograms if they happen
to be published. OConnor (1984b) borrowed a previously published cladogram
of primates and constructed the cladograms for their parasitic mites; unfortu-
nately, the resolution of the host phylogeny is too coarse to serve as a test of
cospeciation.
Is there any easy way of testing some broad prediction of phylogenetic tmck-
ing! O n e might predict that if mites cospeciate with their hosts, the species rich-
ness of a host taxon should correlate with that of its associated mites. If mites
evolve more slowly than their hosts (Manter's First Rule), then the correlation will
not be one-to-one but the pattern of high host richness and high mite richness
should still occur. Data from Eickwort (1994) allows for a simple examination of
numerical correlates benveen numbers of bees and their acsociated mites. It does
not support a cospeciation relationship (Figure 9.7). Eickwort (1994) suggesrs
that differences in bee ecology and nest structure may explain these discrepancies.
O f course, this may also be a reflection of the relative degree of effort expended
I Figure 9.7
1 10 100 1000
number of mammalian species per order
10000

on the bee taxa; honey bees, with 8 species, have 14 associated mite genera, while
the economically less important Halictidae, with 5000 species, have only 13 mite
genera. In contrast, if one looks at the number of mite taxa associated with mam-
malian orders, there is a positive relationship with the number of species per order
(Figure 9.7). Perhaps this is because, being mammals ourselves, we have searched
even the most obscure species for mite associates.
SUMMARY
Because of their relatively small s i x , mites tend to treat other animals as habi-
tats. All taxa larger than mites have been colonised: insects, arachnids (including
other mites), rnyriapods, crustaceans, molluscs, annelids and all orders of
Relationships between species nchness of host taxa and the diversrty Of their mite
associates: (top) bee families (or rubfamilies for the Apidae); @orrom) rnapmalian
orders. (Dam from Eickwort 1994 and Appendix B in Kim, 1985.)
terrestrial vertebrates host symbiotic mites. Mites may be temporary or perma-
nent symbionts and may act as commensals, mutualists, parasites or parasitoids.
The causes and effects of evolutionary transitions between free-living exisrencc,
phoresy and parasitism are subjects of much interest. The parasitic habit appears
easy to evolve but returning to a free-living lifestyle is a more difficult affiir.
Among invertebrate hosts, beetles associated with rotting wood and social
insects arc particularly popular with mites. It is easy to understand why the
 food- and host-rich nests of social bees, ants and termites have been colonised
by numerous lineages of mites but the attraction of the beetle family Passalidae
- which hosts more than 20 families of acarine synibionts (0.Seeman, pers.
comni.) - is not immediately obvious. Mammals and birds are host to a greater
diversity of mites than are the other terrestrial vertebrate classes. This may be
because of the greater diversity of habitats offered by h r and feathers in com-
parison to reptilian scales and amphibian skin. Certain individual hosts may end
up more laden by mites than others, either through direct selection by the mites
or ecological overlap between the two taxa (the 'right place in the right time'
phenomenon). Active avoidance of mites through grooming or evasive actions
has evolved in a number of host groups. Effects of mites on their hosts range
from beneficial (a seldom-proven interaction) to neutral, to mildly deleterious,
to deadly.
Behavioural ecologists are turning to mites as potential agents of sexual selec-
tion on their hosts and as causes or correlarcs of developmental asymmetry. The
ideas of coadaptation and cospeciation pervade literature on mite-host associa-
tions but support for either phenomenon is circumstantial at best. At the
microevolutionary level, endocrinological battles between ticks and their verte-
brate hosts provide evidence of a coevolutionary arms race. At the macroevolu-
tionary scale, we must concur with Brooks and McLennan (1993) when they say
'[allmost all of the traditional generalizations about parasite evolution are myths,
nietaphors, and misconceptions unsupported by data and based on a lack of a
robusr analytical method for reconstructing phylogeny'. However, there are a
number of relatively host-specific mite taxa that would be candidates for derailed
host-parasite cladistic studies. These include Myobiidae and Demodicidae on
mammals and numerous lineages of astigmatan feather mites on their avian hosts.
 'u biquitous' is a much abused adjective that literally means 'being
everywhere' but in practice it means considerably less. The word is
often trotted out by ecologists and systematists to justify their
working on a particular group of plants or animals (cg. 'rodenrs
makc good bioindicarors because they are ubiquitous in t c r d ccasystems'),
sometimes with little support fbr their assertions. However, mites have a fair daim
fbr being truly omnipresent. With h e exception of the warer column of the open
ocean, they exist in every sort of aquatic, timuial, arboreal and parasitic hat&.
In spite of this, mites rarely appear in biodiversity surveys. Data on mite divcrsity
in u o p i d ecosystems is especially rare. Two inter-related reasons for this neglect,
shared with other ubiquitous and 'hyperdiverse' taxa such as nematodes, are small
body size and difficulty of identification. Small-bodied organisms are ofien over-
looked in rapid assessments of biodiversity, pardcularly when samples are s o d
with the naked eye. Even if mites are seen, it is almost irnpossiblc to identify than
to species in the field; instead dissection, slide-mounting and microscopic exami-
nation arc required.
Although the number of described species of mites is similar to that of spi-
ders (between 40 and SO thousand), recent estimates of global acarine diversity
reach as h i as one million species: about five times as high as the most opti-
mistic spider claims. Why would mite diversity be so much greater than that of
their more f b m i h datives?Trophic diversity is certainly one contributing fic-
tor. Except h r fi?edin% on nectar by hunting spiders and consumption of pollen
by webspinners when reingesting their webs, spiders f;ccd only on fluids h m
animal prey (Pollard a PL 1995). A few spiders are kleptobionts chat steal dead
prey from other spiders but, by and large, spiders capture living prey (WE
1993). Trophic flexibility alone, however, docs not seem enough to explain
acarinc succcss.
The species richness of any site results from a complex interplay between
evolutionary, ecological and stochastic fictors. Despite this, assessing local diver-
sity is a simple process at first glance - species are identified in collections of
organisms from local habitats. For example, determining the species richness of
birds in a patch of rainforest would not be an especially daunting task Three
major habitats immediately come to mind: the leafy canopy, the understorey and
the ground. Binocular SUN-, mist nets and song identification are obvious
assessment methods. However, attempts to t d y mite species in the same forest
patch immediately &under on this question: what are the major habitats con-
mining mites?
MITES AND MICROHABITATS
For very small organisms such as mites, there may be no simple answer to the
question of mire habitats. For example, it can be convenient to write about 'rain-
fbrcst mites' and this concept may be appropriate b r plant parasites and for
those that Mon leaf Litter, however, the immediate habitats of many 'rainfbr-
est' mites arc only rangentially tree-like. For example, any species of bird, beetle
or butterfly inhabiting the rainforest may act as home for one or more mite
species (e.g. Treat 1975, Colwe.11 & Naeem 1994, Brown & W h n 1994.
Seeman 1999).
Consider b i as one obvious mite habitat in a forest patch. Birds represent
not one but at least three complexes of mitc habitats: nests, outer surface,
internal body. O n doser examination each of these may be hrther divi~ible,,e.~.
the outer body can be divided into skin, leg scales and feathers; feathers lnto
body contour, wing and tail; each father into quill and barbules. The more
dosely one looks at a presumed mite habitat, the more miuohabitats one finds
- a kind of tcducrioa d a b s d u m m n i n i i n t of Zeno's story of Achilles and the
Tortoise.
Zeno of Elea was a Greek philosopher of the f i f i century BC who was inh-
mow &r serting paradoxes that quesrioned the d i t y of motion (Faris 1996).
Perhaps the best known of these is a hypothetical race between a fleer-boted
hero, Achilles, and a plodding tortoise. The tortoise was granted a head start but 2
whenever Achilles reached the tortoise's previous position, the tortoise had
moved ahead Therefore, Achilles might spend an infinity narrowing the dis-
tance between himself and the tortoise, but he could never catch up.
Zmo's paradox of Achilles and the Tortoise depends on the infinite divisi-
b i t y of space and seems an appropriate analogy for any assessment of 'micro-
habitats'. The term i d i s ambiguous but then again, so is 'habitat'. Consider a
mitc that spends most of its We under the elytra of a passalid beetle. If we con-
sider the subelytral space on these beetles as this mite's microhabitat, then is the
beetle the habitat?What of the log the beetle lives in? The floor of the fbrest on
which the log wts?The fbrest itself)
In the following discussion we will use microhabitat as the elemental com-
ponent of the habitat hierarchy and w habitat in a general sense that includes
the more inclusive components. Undoubtedly there arc limits to the degree that
mites can parridon habitat space but these may be pre-empted by the limits of
the investigator's imagination. Unal they were first discovered, who would have
thought to look for mites inside k t h e r shaftr, r u d e cloacae, crab gills, bee tra-
cheae, moth ears, the stink glands of bugs - or any of the myriad other unexpcct-
ed microhabitats exploited by mites?
MITES A N D COMPLEMENTARITY
Assessment of the species richness of any group requires two measures: the local
richness of collections and the com~lementaritvbetween collections. where
complementarity refers to the distinctiveness of species assemblages across two
or more sites (Colwell & Coddington 1994). Both of ehese components are
influenced by recent historical Factors (dispersal events, extremes of weather,
etc) and by longer term evolutionary h a o r s (age of habitats, geographical dis-
mbution, coevolutionary interactions). If mites are megadiverse on a global
scale, then they should also tend to be highly diverse at a local scale. This local
richness will be a function of both microhabitat diversity and microhabitat
specificity. That is, both a large number of local miuohabitats must exist and
mite species must tend to be restricted to particular microhabitats
Loca microhabitat diversity is not enough to p d u c e global megadiversity.
Them must also be a high level of complementarity fiom site to site. Consider
the fauna of predatory mesostigmatans found on the leaves of rainfbrest ws in
temperate s o u t h ~ a ~ t e rAustralia
n (Figure 10.1). In these Collector's Cums,
some measure of collection effbrt is accumulated on the x-axis and total species
richness is accumulated on the y-axis. Collection effbrt is commonly measured
in terms of accumulated sample number, sample area or time spent sampling.
however, perhaps the dearest measure is the number of individuals identified to
MITES:ECOLOGY.
EVOLUTION
A N D BEHAVIOUR
species. Although the logkd sequence to accumulate sampling e&rt is the order
in which samples were taken or p d , multiple randomisations of collection
order produce a smoother line that is easier to interpret. The lines in Figure 10.1
were produced using 50 randomisations of sampk order and were calculated in
EstimaeeS 5.0 (available from RK Colwell. Department of Ecology and
Evolutionary Biology, University of Connecticut. U-42, Storrs, CT 06269-
3042, USA).
More than a dozen species of mesostigmatans were found in temperate
Australia and most of these species were common in many areas. So, the
Collector's Curve in Figure 10.1 quickly reaches an asymptote (i.e. flactens out),
indicating that about 14 species of mesostigmatans live on leaves in temperate
forests and that most of these species were collected in the first half dozen sam-
ples. The additions! samples added no more information about species richness.
HOWCVCC, compare this to the curve for collecting foliar mesostigmatans fiom
tropical rainforest in Far North Queensland. In this case the curve shows no sign
of levelling o$ meaning that the t o d number of mite species is much higher
than the maximum colIected.
It seems chat many tropical mite species are distributed over relatively small
geographical areas (Walter & Proctor 1998b). Stanton (1979) also found a high-
er rate of turnover among tropical compared to tunperate litter mites and that
tropical mites tended to be more habitat restricted and had higher proportions
of rare species. The image of Achilles endlessly narrowing the gap between hirn-
self and the Tortoise, but never catching up, seems especially appropriate when
chasing species richness in tropical rainforests.
SIZE AND BIODIVERSITY
Robert May (1978, 1988) speculated that one reason for the high diversity of
insects was their small size. Logically then, very small species su& as mites may
be even more diverse than insects. May noted that on a log-log scale, the num-
ber of terntrial animal species declined sharply above the modal size class
d-e -
(3.16 mm-1 cm)so that a 10-fold innease in length resulted in a 100-61d
in species (i.e. S L - ~where
, S = size and L length). Although it is
I
likely that this simple s i d v e r s i t y relationship is an metact (Loder cc aL
1997), a dedine in diversity among animals larger than the modal size dass is
understandable in terms of habitat theory and common experience (May
1978). We all know that there are more species of mice than elephants, and
more fish than whales. However, May's size classes below 1 crn also dedine pre-
-
cipitously. W h y this happens is not so obvious, unless rhii small- ecies deficit
-2'
resuits from a b i against ideneitying small species. So, if S L is a reason-
able approximation to the distribution of species by s&, then the shoddl of
small species might be filled by the study of mites and othu very small animals.
To test thii hypothesis we estimated the size disuibuaon of 4 15 species of
mites from subtropical forest in the Green Mountains (28"15'S, 153O08'E) sec-
tion of L a m i i o n National Park, Quccnsland (Figure 10.2). Only adult mites
were used, and body size was estimated to the nearest 5 pm by measuring along
the midline of the idiosoma wirh an ocular micrometer at x100. If a series of
specimens was available, then the median length was used. Mites were collect-
ed over a 10-year period using a variety of collecting techniques including
pyrethrum knockdown, bark spraying, leaf and stun collections, rearings from
h g a l sporocarps, hand collection of large arthropods, kick sampling in a
stteam, and berlese funnel extraction of litter (Kitching et aL 1993, Walter &
Proctor 1998b, Walter ct a!1998).
Parasidform mites were significantly larger than either sarcoptifom or
trombidiform mites primarily because of the relatively large size of ticks and of
beetle-associated mesostigmatans. For example, the six largest species of mites
were equally divided between the passalid-associated genus M+thanw and the
tick genus I&. Only one of the 27 species less than 250 pm in length was a
mesostigmatan, the remainder were Eriophyoidea, Tarsonemidae and
Oribatida. Overall, more than half (52%) of all mite species are 4 0 0 pm in
length but the smallest size dass shows a relative decline in diversiry.
Although mites are very small, species in the very smallest size dass are not
as common as the next largest size class. So even though we were fareful to
identify even the smallest mite, our data suppom a dedine in diversity of very
small species. Part of chi decline, however, may still result tiom collecting b i .
For example, only five species of Eriophyoidea (tiny gall mites) were collated,
although more than 70 species of woody plants occur on just one plot in the
Green Mountains (Kitching ct af 1993) and an estimate of one species of
Eriophyoidea for each species of woody plant is conservative. More intensive
collecting of plant parasites, however, is also likely to uncover numerous addi-
tional species of Tenuipalpidae, Tuckerellidae and Temychidae - most of
which would belong to the next larger size dass. Additionally - and conclu-
sively -the smallest size dass in Figure 10.2 was not even considered in May's
gering diversity of the smallest mites.
-
original scheme. To raise this size class to the S L -line ~ would require a stag-
 TABLE10.1
MITE ORDEbS. SUBORDERS A N D MAJOR UNEAGES W T H THE NUMBERS OF MZCRI6ED
FAMIUES. GENERA A N 0 SPECIES

Species Guesstimates
Families Genera Species Minimum Maximum

Opilioacariformes 1 9 17 85 170

Parasitifomas
Hdorhyrida 3 9 32 160 320
Ixodida 3 I2 880 IMK] 1200
Mesosugmau
Sejina I 4 55 550 1 100
Microgyniina I 2 4 20 40
Uropod~na 7 75 2.500 10.oOO 25,000
D~arrhmphall~na I 2 60 600 1200
Ep~cn~m 2 3 19 25 50
Zerconma I 26 110 550 1.100
Cercornegisnna 5 9 17 170 500
Anrcnnophonna 21 76 250 2.500 5.000
Lop (icngth in mm) Heterozcrcon~na 2 9 14 100 500
Arcracarina I I 3 5 10
Figure 10.2
Body-ssze dtsmbuoon of 4 15 speues of mkes from Lamingmn Nauonal Park. Paraslum I 100 600 3.000 6,000
Queenslandhstraha ( ' l t c r ) .
Dermanysstna 30 330 8.m 80,000 160.000
Total 79 5 88 12,544 98.680 202.020

HOST SPECIFICITY, SIZE A N D DIVERSITY

Because mites are much smaller than most other organisms, larger animals and
plants represent cornucopia^ of microhabitats to mites. Even the feathers of a Sarcoptiforrncs
single species of parrot can provide specific microhabitats for more than two
dozen species of feather mites alone (PCm 1996). Many host habitats have been Oribauda IM 1,100 1 1.000 33,000 1 10,OOO
colonised repeatedly by different lineages of mites, which have then undergone Anigrnaa 70 627 4.500 90,000 180,000
extensive radiations. Therefore, the species richness of symbiotic mitcs will be Tmmbidrformes
largely a function of rhe current diversity of hosts, the success that mites have
had colonising those hosts and the host specificity of the mites. For example,
most species of bees (Apoidea) are host to several species of symbiotic mires and
at least 31 lineages of mitcs have independently colonised the bee habitat.
Individual bee-mire species rend to be geographically restricted in their distri-
bution and to be host specific at the species, species-complex or generic levels
(Eickwort 1994). About 25 000 species of bees have been described and perhaps
40 000 currently exist; d~erefore,the diversity of bee-mites alone is likely to
exceed the current described diversity of the Awri.
In Table 10.1 we present our hypotheses about the likely diversity of major Total Acari 43 1 3672 45.23 1 540.215 1,132.090
mite tam. The Opilioacariformes, which show no associations with animal or Note-The last rwo columns are our minimum and mnxlmurn expectations as w the uue d i i r s i t y of
plant hosts, are the least diverse of the major mite lineages. Few species have living mires.

been described and we doubt that more than a few hundred currently exisr. The
Parasitiformes lineage is perhaps ten thousand rimes as rich in species as that of
the Opilioacariformes. Thc resolution of this guesstimarc depends on hoar and
microhabim specificity, cspccially within demanyssinc lineages symbiotic with
insects and vertebrates. The Acariformes lineage is by far thc most divcne major
group, primarily because o f a number of symbioric radiations. For example, the
Asrigmara include the common mange mires of domestic animals, and span-
thropes such as the housc dust mites, cheese mites and scabies. However, most
asrigmatan habitats are nor of such immediate economic interest and the bulk of
2 the diversity in the Asrigmara consists largely of undcscribed uarasires and com-
mensals than live on and in cconomicallfu&nporranr birds,amammals, reptiles
and insects. Similarly, the Parasirengona include a vast array of chiggers, velvet
mites and water mites that require a vertebrate or invertebrate host to complete
- . ofacariform mires
their life cycle. But in all likelihood, the most diverse groups
arc those associated with plants, including the spider mites and thcir relatives in
the Raphignathina, and the gall and erinose mites in the Eupodina.
Repeated colonisation and diversification by lineages of symbiodc mites has
occurred in association with many species-rich groups, e.g. wasps, ants, bccdes,
termites, orthoptcrans, myriapods, spiders, reptiles, birdz, mammals, conifers,
angiosperms and so on. Many of these mites are parasitic on rheir hosts but oth-
ers are commensals (e.g. phorctics, feather mires) or mutualisu (Eickworr 1994,
Walter & O'Dowd 1995). Regardless of the nature of the association, a tendcn-
cy towards host specificity appears to be common in those mires char spend all
of thcir life on the host (see Chapter 9). If hosr specificity is common in ~ b i -
otic mires, then the maximum guessrimares in Table 10.1 may prove too con-
Figure 10.3
MITES& BIOLOGICAL
DIVERSITY
SUMMARY
The rpccrrc of mite megadiversity haunrs estimates of global biodiversiry bur
more noise than hard data exisrs to supporr rhac claims. In temperate regions,
the acarofaunas are cerrainly divcne bur not exceptionally so. For example,
Canada is admared to have less than 10 000 spccia of mites (Lindquist 1979),
and America n o d of Mexico only 30 000 (OConnor 1990). If the Acari is a
hypcrdivcrsc group (5- ~ a m m o n d1992). then the bulk o f acarine biodiver-
siry must raide in the acarologically unarplorcd tropics. B u d on rmdia in sub-
tropical to tropical rainfornu in Australia, this does appear to bc true: both rich
and complemcnrary asscmhlaga of mites arc charactcrirtic across sires and
among microhabitau within a rite (e.g. Figure 10.3). Even cxtcnrive collections
within strictly defined habitats fail to adequately arimarc local spccia richness.
The helief that small si.z is posidvcly correlated to high divcnity has hclped
to sustain thc hypothesis of hypcrdivcniry in the Acari. M~cmhahitatuse and rhc
small ri2e of most mica (c.6 adults of 52% of 415 suecia from a s u b t r o n i ~ l
rainforest were l a than halfa millimetre in icngrh) ap& ro bc associated k h
the succas of tropical mites. Although we have boldly hypothesised high diver-
sity in many mite taxa (Table 10.1). hosr and microhabitat specificity in uopi-
cal mites must be addrascd before any accurate esdmatc of global acarine
divcrsiry can bc amcmpted.
 Ichough mites arc intriguing animals worthy ofsrudy in their own right, d ~ c y

-A& are also excellenr models for addressing questions of more general interect.
Advantages of using mites as model organisms include their small size and
horc generadon times (making them good laboratory animals), multiple
independent evolutions of suucrures and behaviours (making them a t d e n t t a r aces
for evolutionary theories) and their diversicy of interactions with other omnisms. With
'2

the exceptions of active flight and maintaining complex societies, there are few areas of
animal bchaviour where mires have not ventured. In this final chapter, we review some
of the many theoretical areas in ecology, evolution and bchaviour for which we recorn-
mend elucidation through the liberation application of acarines.

THEORETICAL A N D APPLIED POPULATION

ECOLOGY
We start our prospectus o f mites as models with population ecology because 40
years ago Carl HufFaker (1958) proved our point with a few trays of oranges,
some toothpicks, vaseline and mites. Studies of enemy-free space, predator-prey
interactions and the population dynamic, of plant-inhabiting mites continue to
be a major emphasis in the field (e.g. see Erl,rrimr~zttzlar~dAppliedAcamlO~, vol.
14: 179-422 & vol. 21: 321-520). More recenrly, the work of Maurice Sabclis,
Marcel Dicke and their colleagues has been at the forefront of exploring the com-
plex world of chemical interactions among plants, their herbivores and their prcd-
ators (see Chapter 8). But with rare exceptions (e.g. L a n a et aL 1996), the
population dynamics of mites that d o not inhabit the leaves of agricultural plants
remain unexplored. We find this surprising because many currently contentious
hypotheses could be put to the test using mites in simple experimental units.

The hottest of all ecological topics must be 'what is biodiversity good for?'. Are
most species redundant, performing the same 'service' as dozens of ocher species,
or does each additional taxon improve 'ecosystem functioning'? Perhaps the only
way to directly test the value of biodiversity is through the creation of assem-
blages that vary in species richncss and con~position.Such experiments are most
readily accomplished in isolated, climate-controlled facilities. A now Famous
example is that of Naecm etaL (1994), who used the Ecotron to show that plant
species diversity could directly influence ecosystem productivity.
Although the use o f small experimental units (microcosms)that mimic larg-
er natural units is often questioned, there is no other approach that offers as
much potential for discovery. When considering organisms to use in a micro-
cosm study, what better inhabitants could one desire than mites? They fill all
trophic levels above primary producers and seem to exhibit a profligate and
excessive diversity, particularly in soil systems (see Chapter 6). It seems like that
mites and other soil microarthropods have valuable roles to play in maintaining
ecosystem producrivicy. Recently, oribatid mites have been shown to enhance the
recovery of soil communities after severe disturbances by dispersing microbial
spores (Maraun rtaL 1998). Richard Fortey remarks in his Lifr: An Unaurhorised
Bios~nphy,"But alas for d ~ world
e if the n i i t a and their diminutive allies failed
to prosper!' (1997, p. 171). To make this more than rhetorical one must
compare the functioning of microcosrt~swithout mites to those with them.
MITES: ECOLOGY.EVOLUTIONA N D BEHAVIOUR
Transgenic releases
Whether we f;sar or applaud the widespread release of genetically engineered
creatures, transgenic organisms will soon be an everyday tool in Integrated Pest
Management. Microbes are the easiest oqpisms to engineer and mass rear for
release but exploring their fite in the field is fir from easy. Determining their
&on natural systems is even more difficult and t h u r ace justifiable worries
about unforseen &. Many mites, however, r i d microbes tbr ease of rearing
and are fir simpler to monitor. Additionally, many species of predatory mites
have been introduced repeatedly into countries around the world with no ill
&m to agricultural or natural environments. We suggest that rhese mites
would be excellent models for testing the a t e of released transgenics (see page
195). They are far more vagile than microbes, and hence a better test of a
released organism, but chey can be monitored using simple sticky traps or trap
plants infested with preferred prey. Safery, ease of rearing, ease of monitoring and
importance: all argue fbr the use of phyroseiid mites as models fbr transgenic
releases.
Biomonitoring
A final point about mite populations is that they ofien display high densities and
diversities in small volumes ofsoil and aquatic substrates, and so art well-suited
fbr biomonitoring Studies. A.ithou$~ soil ecologists have long induded mites in
their enumerations of soil fauna, determination of species-specific habitat pref-
erences is just beginning (eg. van Straalen & Verhod 1992. van S d c n 1997).
In contrast, most fitshwdter ecologists ignore mites campletcly or lump them
together with osuaaob, nematodes and miscellaneous small creatures as 'others'.
This is not a wise move, b r there is growing evidence fiom European studies
that water mites are sensitive bioindicators, and population densities of some
species may serve as bioassays for particular chemicals or disturbances.
Additionally, I&-history characteristics of soil mites are proving useful as indices
of disturbance, with I-selected species dominating on disturbed soils and K-
selected species in stable habitats (Ruf 1998).
THE EVOLUTION OF HOST SPECIFICITY AND
VIRULENCE
Although one might have the gut W i n g that symbionts have their evolutionary
origins as generalists and over time become more host specific, there have been
few tests of this hypothesis. The acarine symbionts of mammals and birds would
seem especially suited tbr such studies because thcy range h m generalists to spe-
cialists (see Chapter 9). Extant Dermanyssoidca, for example, run the gamut of
possible associations, fiom nest-inhabiang predators to obligatory internal par-
asites (Radovsky 1985, 1994).Another appropriate model may be @ mites 'in
the Eriophyoidca (Chapter 8). Some major agricultural pests are h u n d in thir
supcdbily bur the vast majority appear to be host-speci6c parasites that cause
little or no loss in fitness to their host plants.
Factors that promote the evolution of virulence (the degree of damage
caused by a parasitic organism) are a hot topic given current fears of 'emergent
diseases' and the sad history of AIDS (Garrett 1994). How many more 'Lyme
diseases' are lurking behind the cheliceae of ti& and other biting mites? How
MITES
AS MODELS
important are neutral symbiona (e.g. phoredc mites) in preventing colonisation
by antagonists?Art novel parasites invariably more harmfi~I?Does a long histo-
ry of association berwccn parasite and host guarantee low virulcnce?D o parasites
transmitted vertically (from parents to offipriog as in many ticks and chiggers)
produce more benign effbcts than those transmitted horizontally (between unre-
lated members of the same age cohort)? These ace major gaps in current para-
sicological theory (Ebert & Hem 1996, Sober & Wilson 1998) that could be
narrowed through studies of interactions befween mites and thdr horrs,
SEXUAL SELECTION AND DIVERSIFICATION
Sexual selection is thought to be a driver of both micro- and m a u ~ e ~ l u t i o n a r y
change At the microevolutionaryend of the scale, Gross and lkpka (1998) used
data on fighter and non-fighter morphs of acarid mites (Radwan 1995) to
test thek model of how alternative male tactics can coexist within populations.
Holland and Rice (1998) suggest that intersexual conflict results in cycles of
male ' a d and female 'dcbcc'; the shifdng copulatory p o w in thc Derm-
anyssina (see Chapter 5) would seem to support their belid. O n the macro-
evolutionaryscale, a common bur seldom tested belidamong evolutionary biol-
ogisrs is that the intensity of s d interactions in a taxon is positively associat-
ed with speciation rate (cg. Kaneshiro & Boake 1987, Carson 1997). Mites
show such an enormous range of conga between the sacs, from intimate to
none at all, that they arc ideal subjects fbr sexual selection studies at both e m -
lutionary levels.
THE DEVOLUTION OF SEX
In convast to che diversity of mating behaviour in some groups of mites, w y
others have abandoned sex altogether (see page 86). We would be hardly going
',
out on a limb in saying that sex has been lost far more than 100 times in the
Acari. These repeated losses of sexuality and its potential resurgence in the
Astigmata (see page 91) are reflected in numerous dosdy related pairs of sexual
and a s d taxa. This is an ideal situation for tests of hypotheses about the costs
and benefits of sex. Does sex c o n k a competitive advantage in complex envi-
ronments? Does asexuality provide an advantage for colonking species? Can
asexual spccics'maintain genetic diversity, and if so, how? The roles of holoki-
nctic chromosomes and inverted meiosis are only two of many unexplored ques-
tions in the evolution of acarine d c y .
Another u n a d question relates to the influence of the endosymbiotic
Wolbachia p u p of alpha proteobaaeria on skewed sex ratios and thdpky in
mites. To date, WoIbachia and its effbns on host rcproduaion have been stud-
ied primarily in insects whur they cause post-zygotic ncproduetive inampati-
b i t y and all-&male parthenogenesis (O'NcilI ct d 1997). Mites, however, ace
comparable to the inxas in diversity of reproductive systems and many inde-
pendent origins of thelytokous parthenopuis have been demonstrated in var-
ious acarine lineages (Norton eta! 1993). Studies of specific mite systems may
also eventually help to clarify the population dynamics of Wolbaehia inticdons:
b r example, if there are fimess costs associated with various strains, whether
multiple infmions spread at the cost of single infC4ctions and if Wolbachia
dynamics can lead to speciation events.
PUSHING THE LIMITS OF PHYSIOLOGY A N D
MORPHOLOGY
Two of the major themes in mite evolution have been to press developmental rates
and body size to their limits. Extmordinary rates of population increase dependent
on rapid development, mating systems that assure short generation times and high
reproductive ourput have cvolved again and again within the Acari. Thii wealth of
analogous systems is perfect for testing hypothexs and is matched by the relauve ease
of culturing many of these m.Ik'ccnt advances in undersranding the developmen-
tal genetics of mites (e.g. Telford &Thomas 1998) suggest that the size of mites is
no impediment to their use as models for understanding much larger organisms.
All mites are small in an absolute sense but both the largest and the smallest
size classes of Acari appear to be less diverse than intermediate size classes. This
is a generd pattern in terrestrial animals (May 1978, 1988) but a confwsing one.
W h y are the largest mites so small? W h y has not at least one lineage of giant
mites evolved? Conversely, what limits the evolution of small body size? Mites
less than 100 p m in length as adults are known but seem to be very rare. Mites
smaller than half this length appear to be impossible - but why?
O n e intriguing question that combines these evolutionary patterns is that of
the apparent dissociation between body size and developmental time in some
Mesostigmata (see Chapter 4). Given that theory to explain constraints on devel-
opment in most animals appears to be progressing rapidly, this failure of mites
to conform is especially interesting.
SELECTION AT MORE THAN ONE LEVEL
As well-indoctrinated individual sclcctionists, many of us become alarmed at the
faintest whiff of group selcctionist thinking. This hypersensitivity sometimes pre-
vents us from contemplating how selection a n act at different levels of organisa-
tion (Sober & Wilson 1998). Mites are often members of tiny communities
demarcated by their location on the bodies of larger organisms (e.g. mites, h n g i
and nematodes on burying beetles; mites, Fungi, lichen, small insects on leaves).
Their fates are linked with that of their bearers, conditions ripe for selection for
genes within spccics that support the functioning of a community of species as an
evolutionary unit (e.g. Wilson & Knollenberg 1987, Sober &Wilson 1998). As
well, subdivided populations founded by single females provide opportunities for
group selection for fcmale-biased sex ratios (e.g. Wilson & Colwcll 198 1). When
moving from dieoretical models of multi-level selection to natural systems, mites
probably offer more opportunity for enipirical tests than any other taxon.
SUMMARY
The average mite is a tiny animal, scarcely visible to the unaided human eye. Because
thcy are literally bcncath our notice, we are often able to forget mites - unless they
cause problems that cannot be ignored. Wairing for a pest outbreak o r a new disease
to take mites seriously, however, is a serious mistake. In fields as current, and as dif-
ferent, as group selection tlicory and genetic engineering technology, mites have
proven useful experimental models. We hope that some readers will realise the poten-
tial of mites as experimental organisms in their fields and take advantage of them. In
these lives lived at a rnicrosdc dierc is much left to discover.
Publications on the taxonomy, biology and ecology of mites are scattered
throughout the primary literature. However, two quarterly and three less fre-
quently published journals currently emphasise the systcrnatics of mites.
QUARTERLY JOURNALS
Acarologia (French, German or English)
In publication since 1959, this was the only major acarological journal until
1974. Primarily morphology and systematics but often with cxtcnsive descrip-
tions of biology and behaviour. For further information contact: h4ichel
Bertrand, Laboratoire d e Zoogeographic, IJniversire Montpellicr 111, route de
Mende, 34199 Montpellier cedex 0 5 France (email: bertra~ld@bred.univ-
montp3.fr). General enquiries acarolog@.mnh~i.fr
ofAcarology (English)
Irzternario~mfJorrr~zaf
Systematics, taxonomy, morphology, behaviour m d physiolohy ofnlttcs. In pub-
lication since 1974. For furcher information: Dr V. Ptasad, Incernat~onalJournal
of Acarology, Indira Publishing House, P O Box 250456, West Bloomfield, MI
48325-0456, USA (email: V.Prnsad@ix.netco~~i.corr~).
ANNUAL O R SEMI-ANNUAL JOURNALS
Acarina - The Russian Jottr~zrzlof Acarology (Russian)
Semi-annual. For further informntion contact: D r O.V. Voltzit, Zoological
Museum of Moscow L.omonosov State University, Hcrzcr~str. 6, K-9 Moscow
103009, Russia.
Journal ofAcarofogy (English)
O U T O F P R I N T For further information contact: 7'hc Acarological Society of
India, Department of Entomology, University of Agricultural Sciences, GKVK,
Bangalore 560065, India.
Journal of the Acarofogicnl Socieq ofjapan
Semi-annual. For further information contact: T h e Acarological Society of
Japan, c/o Faculty of Horticulture, Chiba University, Matsudo, Chiba, 271
Japan.
Systematic and Applied A c t z r o f o ~(English)
Annual. For further information contact: D r %hi-Qiang %hang, Systematic and
Applied Aurology Socicty, c/o Dcpartrnent of Entomology, 'l'he Natural
History Museum, Lmndon S W 7 SBD, United Kingdom (email:
Z.Zhang@nhm.ac.uk).
NON-SYSTEMATIC ACAROLOGY
Fzperimmtnl nrrd ApplicdAcardqev (English)
Primarily biology and control of tickc and plant-p-iric mircs bur occasionally
with a more gcncnl paper on mire biology. For Further information contact: Dr
Leo van der Gecst, Experimental & Applied Acarology, Section Popularion
Biology, Univcrsity of Amsterdam, Kruislaan 320, NL-1098 SM Amsterdam,
The Nethedands (email: geesr@hio.uva.nl).
ACAROLOGY WEB SITES
~carologyhome pagc: http://~uww.nl~m.ac.uWacaroIogy/
Tree of Lifc, Acari home pagc: htrp:l/phylogeny.~rimnil,edu/treeleukaryotes/-
a n i n ~ a l s l a r r h r o p o d a l a r a c l ~ ~ ~ i dhtml
ala~i
ACAROLOGY COURSES
Arumlogy Sum,rrer Progrnm
For further information contact: Dr Glcn Necdham (email: gneedham@mag-
nus.acr.ohio-srate.cdu) or Dr Hans illompen at cbc Ararology Laboratory, T h e
Ohio Scare Univcrsity, 484 W. 12th Avenue, Columbus, Ohio, 43210, USA
(emnil: klompen.l@posrbox.scr.ohio-stace.cdu).
h r c r n a t i m d Coum ofAc~rology
For furrher informarion contact: Dr H. M. Andre (email: henri.andre-
@infohonrd.be) or Dr Micl~clBcrtraud, Zoogeographic. Univ. Monrpellier 3,
RP5043, 34199 Monrpellier ccdcx 5, France (cmail: bertrand@bred.univ-
montp3.fr).
Abbocr, D.T., 7:R S-rcdr & D A Cmrrlq, Jc. 1980. Abundascc, disrribution, and clfccu of
durcurring on Crypcarrigmaca i n rhc Soulhcm App&dxians. Enuironmrntol Enromo(ogy9:
618623.
A t r , 1:. S.A. b i n & M. Higarhi 1997. Biodivrnir)r an rrolo~iiiilprrpcctivr Springer: Ncw Sork.
Abm, A 1982. Thc c f h of parasitic warcr rnirc l r m c (Amnurwspp.) on rygoprcran imago-
( O d ~ m n ) /oumnl
. of1nvc~tdmtr Pdology 39: 373-381
Abro, A. 1984. Thc inirid srylorromc formarion by pamitic lrrvac o f rhc warcr-mirc gcnur
A m n v n u a n zygoprcan i n q i n c r . Acamlqiin 25: 3 M 4 .
Abm, A. 198R. Thc mode o f arndmcnr of mitc inrvac ( L r p m ~p.)ro harvcatcncn (Opilioncs).
jovmdl ofNamrd Hiriory 22: 123-130.
Abm, A. 1791. The incipicnr rrylorcomc d p d k warcr m i x l r m c (Amnunrrrpp.)./oumnlof
P m ~ i r & ~ 7 7313-314.
:
Adir, j. & G. Krmn 1985. Norcs on rhc n a n d history o f M r r o r h c L r (Awri: G-arid*:
Macmdxlidrc) sssocirrcd wirh 3-tocil sloths Bimiypur rpp. (Erlcnrara: Bradypudidad i n rhc
,ntnl Amamn. Zonlo@& Anzzicr 214: 222-224.
~ ~ ~ h l i r n aA. n n1984.
. i n Azarnlogy C7.
Whar is our current linowlcdgc ofarsrinc c r n b ~ o l o g y ?
..
uol. 1. on. 90-99, cdr DA. Grifirhr & C.E. Bawmm. 1;llir Horuood: Chicharcr
~ c u h l i r n m n .A. 1971. T i c k r n d di.-: surccpriblc horcr, rcscrvoir hosu, and v m n r s . in
Pmmicchorr nrsocinrionr: mrnrzcnrc or ron/7id pp. 14b156, c& A. Ibh, A. AoJ~limann &
1. Unlir. Oxford Scirrncr Publiurions: Oxfird.
-
~~ ~~
Agward. A.A. 1997. D o lcaf dornarix mcdiarc 3 plan-mitc n~urualirm!An orpciimcnrrl ccsi of
chc cffrcrs on prcdaton and hcrbiv<rrcs. EcclokirolE~~ome1o~22:371-376.
Agwrnl. A.A. & R Karban 1797. Ilonmci= rncdiilrc p l a n - d > r o p u d rnurualirn~Narvrr 387:
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 MITES: ECOLOGY,EVOLUTIONAND BEHAVIOUR

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Y 179-183.

lhgc r~umbcrlin bold
rcfcr to illustrations.
Acari 4
Auriformc~ 4, 25-27
aquatic 136-37
associations with
invcrtcbratcs 209-10
divcrsiry 261
gcnctic rncchanisrtu 8 7
mating bcttavioirr ~CF-72
onrogcny 37
Acarina 4
acarinaria 223
karinomorph;l I8
aurologisr, first usc of tcrm
...
Vlll
:rcarology
dcfincd viii
journals 269-70
acan~phagy 12 1
Acarophrrtux muhunkui 48,
25 1
Acarur 68-69, 227
Arcria. in bioconrrol of
wccds 196
actirtopilin 25
Anrlw. ntatirtg 71
Aduc'ylidiurn 222, 25 1
Adbacsozcrrr pohp/IyNor 190
adlcrocysw, in rick spcr-
rnaropltorcs 73-74
acdcagus 6 8
AfroTpho(ar/apr 179
Apz~~opsir1 5.3
Aglaspidida 11
ALIS~OZTIC~ unrarrri~l~~
97-100
Alicorha@ 29. 39. 1 I 0
allcrgics 227-28. 243
AIIorhucrophora 175-76
Allodinycbw 2 14
Allor/~mmbiurn 69, 205. 245
Allod~yridac 24
dcfcnccs 1 18- 19
ANorlyrus 24
Ahcormrris, sizc 46
A I p r 39, l I 0
arnbcr 170-7 1
Amblyntrrnzn 134-35, 236
Anrb!ysci~u,mating 6 5
antbush prcdation
srr prc&tion
amcnsalism 199
Anicroseiidac 179, 192
amphibians
as hosts of ntita 236
as prcdators of mitcs
123-24, 158
amphipods srr crustaceans
amphiroky 8 7
Arwlgrr 233
AndmLzcInps 226
arrdropoly~norphism79-80
anirogamous 58
Antarctiw 97-102
antennae, abscncc in the
Chcliccrata 3
Atrrcntro(ar(apr, mating 6 5
Anrcnr~ophotur 2 15
Arrrrrrnorciru 2 13- 14
Anthocoridac,
rcr Cirnicoidca
ants
:IS hosts of mitcs
200-201.208-209
LS mirc prcdators 121-22
Anystidae 113. 180
apo&rm 39
aquatic habitats 132-4 1
adaptarions to 141-55
Arachnids 4, 11
fossils 8-16
in aquatic habitars
133-34, 135
origins I2
tdariva of mircs 16-18
Archararanu dubinin; 15
Argymnrru 133
Aribatcs jawnrir 209. 216
armour. as a dcfcncc in soil
mitcs 118-21
armourcd mires 121-22
Arnold, on mite p c k c r s
237-38
Amnunu
cuc for leaving host 214
egg size and numbcr 36
gas cxchangc 142
in trccholcs 137
marc choicc 83
mare-guarding 7 5
parasitism by 218-19.
239,24 1 , 2 4 7 , 2 4 9
p H 167
pupulation gctictics 207
sexual dintorphism 85-86
arrhcnoroky 87
arthropods, body organisa-
rion 9
Arca 181
axwual, rrc panhcnogcncsis
asscmbly phcrornoncs 64
~&ZCO~SI)/?R~IU 138, 154
Astigrnara
aquatic 135. 136, 1 4 3 d 4
as prey of phytosciid mitcs
182
associations with invcrtc-
bratcs 210
gcnctic mechanisms 8 7
in rrceholcs 144
loss of phorctic stage
207-208
mating bchaviour 68-69
relationships ro Oribatida
26.91-92
rcc aLo feather mitcs
asynlntctry 68,79, 247-48
Ar/~iarcl(a,mating 6 5
autapamorphy 7
autotomy 118
Balaurrizrrn
as prcdarors of burtcrfly
eggs 181
l a d fccding on pollcn
and plant fluids 205
bark. as a habitat 191-93
bats 200-201, 226.228-
bcdbugs scc Cimicoidca
b c a srr Hyrnenoptcra
bccrlcs
as hosts 222-23, 246.
249,25 1
as prcdators of mica
121-22
phorctic rnitcs. and 194,
208-10,214,244
biodiversity, 256-63,
25841
collccror's cuwcs 257-58
complcnicn~arit~ 257-58
enigma in soil 124-3 1
atimarcs 170
low divcrsiry in agricultural
fields 197
mica as a hypcrdivcrse
taxon 256
trophic divcrsiry 104-1 5,
256
bimomh 79
bioindimtors, mites ;cr
in aquatic habiratc
164LGX. 266
in rcrrcstrial habirats
129-30, 266
biological control agents.
m i t e as
of inscnr 193-94
of mica 181-83, 186-88,
193-95
of wccds 195-196
transgenic mites 195
biramous appcndagc 10
birds
as mirc habitats 198,
200-201. 230-36, 239
as prcdators of mircs 123
dcfcnccs against ntires
240-4 1
ntita and marc choicc in
birds 24&48
BLmironnur 204, 2 14
bodyguard hypothesis 186
Bohortak 207
bolus, food 3 1
book gills 12
book lungs 12
Boophilur 239
bothridial wnsillus, rcc rri-
chobothriurn
box mires 120
brackish watcr 1 3 9 4 0
Rrrn&ndarria 2 14
Brryistemn 228
brooding 59
Brooks and McLcnnart 254
butrcrflics, prcdation on eggs
180-8 1
buttcrwons 189
Cacculidac, as ambush
prcdarors 1 13
Gcnorhubditis r(rgartr 5 1
GrlogIrphw (= Sancmraniu)
d c polymorphism 79
pborcry 21 1
sperm con~pctirion 80-8 1
ulypcostvcs 39
Cambrian E x p l o h n 9
GmincUa prruphoru 138
campodeid diplunns, as mite
prcdarors 12 1
cannibalism l l C-1 7
wpacitation of spcrm 6 2
capitulum 15
carotcnoids 158-59, 182
Carpoglyphidac 227
carrier 202
carrion, as a mirc habitat 127
centipcdcs 121, 209
cephalothorax 10
c7co&+w 222
ccrotcgumcots 1 19. 190
Churlcroniu, as predator of
butterfly eggs 180-8 1
Chawrinia, clarrosratic
prelarva 40
Chtirorriru 135. 137
chdarc-dcnrarc chcliccrac
26-27
Cbrkomorpha Irpirioprcron~m
23 1
chcliccrae 4, 10, 26-29
Chcliccrata 3, 10
chcmiul defences 1 18
Chcylcridac 16, 177, 180
Cbcyktru mIdiru.r 3 5
chigger 43. 2 3 6 3 8 . scc NLO
scrub ircli
Chilorom 205
Ch'ysomrlob 249
Cimicoidea, hypodermic
insemination 8 5
cladc 7
cladogram 7
Clark 233-34
Cloacaridac 232
Corcipolipw 246
cocvolution 248-52
Colcoptera. scr bcctla
cofroscim 1 14
Collcmbola. srcspringrails
Collohmnniu. mating
-7
commensalism 199.
215-16. 234
wrnmuring 5 3
cornplctc dissociation, rcr
sperm transfcr
Canioprcrygidac. as rnirc
prcdators 122
Copci rule 14
copcpodr. srr crusraccans
coprophagy 106
copulation 5 9
Cordylocbmrr rcorpioides
21 1
Cosm~~hrhoniw 120
c o u 10
crabs, rcc crustaccans
crayfih. srr crustaceans
Cmu& 161
crusracc:t~ts
.u ltosts 61r rnircs 1.jX.
152-54. 209-10
as prey of ntircs 1 4 6 4 7 .
1 4 8 4 9 , 153
in functional groups
107-108
tcrrestrid 13
crypric fcmalc choicc 82
Ctyptognathidx 117
Cryptognomac 18
Cq~propygusurrrarcricm 100,
315
115
Ctyptostigtnara, r r c 0 r i b a d d ~
cryptomic 96
Cunaxidae 25, 1 1 1,
113-14. 180
Cyntbacrcnracidac 171, 190
ryphophthalmid opilionids,
similarity ro mitcs 18
Cyu Lrimrmi.SI . a prcdator
of oribatid mires 121
Cmspinrkia rrur;rvcnorxriura
186. I90
flnnrucur ucrriciI1I)er 35
L)anvin, uo scxiral cclcction
75, 8 2
decomposition 96, 124-27
cffccts of grazrrs and
browsers 105-1 O X
deep sea rifLs, mitcs in 140
dcfcrtcc against predation
117~21
DCIIIO~S200-201, 228-29
Llcnrfrolurlupr 16. 40. 222
Dr~r~lroLtrLupis1, 63, 9 4
Dcntranyrrw 23 1. 240. 246
Dcrlr~zropJ~~~~~oidrr 227-28,
23 I
dcrniicolcs 232
derritus, XY anccsrnl Ii;tbit;rt
170
deep soil 7 6
clcutcroky 8 7
dcvcloprncnt 36-46
dissociation bcrwecn s i x and
rarc 51-52
eKcccts of tcmpcraturc
48-50.49
gcrwxics of 268
in Oribatida 50
D ~ o m c d n uI 5
Diaprrmbara I92
Dicmchck in moth cars
214.220-21
digation and acrctiort
31-32
Diniock, on harcms in water
mircc 78-79
IXr~ogmr~mu~. 011 c;trpcrttcr
 -
bees 223-24 -on 5554 123-24. 158 b r sex mio 89 Huochinson. G. Evdyn incurticid frrshwater 139
Dino&mmbinm 46.158 s k 46-47 fruit 177-78 Cmmph,74iorha~~ssrhry5n' 127-28 in+d predation
diplodiploid 87 Ehgduna~s5uw mating h n a i d p u p s 104-1 5 215 H-prclvn 39 115-117
dirsaspamtnnrfv 60.w 66-67 digestin capabdides of ori- guildr 10%104 Hy.'ssrirt asrirt
scrwuer a
mires inuvenul competition
akospermmash Ewp- 23.65 barid mites 106-1 07 digenin apabiitier of ori- HydrecJ,~ 75-82

-
ditpe+sPI 52-55 -ui& 411-14 dtm plant parasites batid mim 106107 engod 245 invasion of land 14
d i p o c t c o d ~ ~ E u r t y 177 108409. 171-79, w ah functional groups &position in plants 31. I p n n u r 222
60. see ah sperm cya 19S% 166 W?-Y 58
mfrr
divusiry. see species richness
h a in halaamids
140
film-feeding micmbivorcr
lo8
parasirism by 219.239
pmhtion by 145
+@, see
~ t c hm t e 230. wr d o
I d 183-89 Arui 21.24.25 i n k plant pamites spamatophorcs 74 PVnno~
addingdoma& 188 c h d i ~ f ~compound
te 10S108.109-110, -- - H ! iumparity 35
asaplant&cc 186 cpes-12 111-17, 171 Hacmqansanu 226.228 fading 165 f w h . 16.239.259
bcncfits mmiro 188-89 s v h m q , and 163 Funaional morphology of H ~ ~ h r &hp pi 228 maring 7 6 7 5 sperm competition 80
inseCa in 185-86 Trigononrbida 14 mim 26-32.61-62, hkhmllurbamri. 70 parasicism by 206.24 1 Lxodih 16s23.64.73-74.
Icktionship benveen aombidioid mice 28 73-75.171 H&ida 136,140, Nvimming 163 80. 134-35,208. 231.
number and number of 4h funSi 192-93 153-54.210 & & p m a s e k 102.115 236-37,239-40.246,
mim 187 &ding 148 fur mires 229-30 H&ydorz&anuzm 34. H$wcm 142.16544. 251.259
Iype5 18-4 pv.SitLmby 239 F w o ~ m p o hm n g t g t ~ i244
x 173-74 I n
what kVCS in Mdomaria swimming 162-63 Ha&- 173-74 hydmmam or a habitat for J 1 larva 39
185-86 Gabudnia & f i b 234 H u n i l t o ~ s e latios
r mires 140, 153 jobnsrontmrr
Dubininia m r b p i ~ n 223
' /. WMN 74
dragunflies, ICC donates
dudcwmd 177
FaJucnholu' rule 248
I i i n 8r Hyland on
cospcdption 250
C;rrlmdronuu coridmixlir 47,
182-83.188-89. 195
$ mim 172-73. see 4150
89-90
H d t o n - U r hypothesis
246
HsE 149-50
andpollution 16768
j. mpar 205
j u j m m w f i o l a ~171
~
dung, as a mite habitat 127 Fnlrotj~huc250 Eriophyoida haplodiploidy 87 parasicism by 218,239, jumping 118
dust mi- 227-28 h d b d e n c e 113 Gdnuucllodcr 40 hvtms 77-79. 152 244
D y u s consrvlt 128 fbthcr mircs 59.68.198, G.vmniuomy dcvelopmen- He~~ahmIh &u&s 23 swLnming 163
200-201.232-36.235, tal rate and generation Hnnichcylctia w&ti 35 Hymenopma 208.210,
earrh mites 173-74 24617,250-52 k c 48-50.49 Hcmirarpta 193-94205 215,222-25.249.252
Eberhard, on sexual selection kcdingguilds, see Functional GamascUy~jX-igrr1 19 herbivory, seeplant pansites and mite diversity 260
73,8243 groups G.nuoui&.ai 98-102. 1 1 1 heruomorphic sage 38,213 seahano
ErhimCaclaps c c b ~ i n u s228 female choice 82-84, G. mghm?, mating 65 hctuomorph 68,79 H p q t 23.226
Erhinownw 57.198 24546 Gaga, photo-prouccion Hetuorugmaa, lift cyde 42 Hpoukwpmpur 231
mospennatophorr 65.73 female-bid sex-ratios hyporhsis 157-59 hexapod mita 30 hypopus 38,42,213 Labidostommatidac 25
Eiiuvmivrn 98.136 86-93 &"-'=niF hippoboscid flies 233 hypostomc 23.27 labrum 31
34-36 ferns 196 Hirstirhpy+nnir 237. <
aquatic habiua 141--43 hypomchous 45 Lvnington National k r k ,
ejacuhmry complex 62 fedsation 59 cuticular 17 250 Qucucrland 2 5 9 6 0
elarronws -39 - fip 178 see d m book lungs, book Hirtistoma 213,236 immunommpeunce Lcrmbgluphus
6849,244komL mating
Elton on water mite colours fish gills. tracheae holokinetic chromosomes hypothesis 240
15657 Y mice habitats 144.217, Gaud and Ar)reo 232 88 incomplete dkxiation, wr -30
Endeosrianuca 25.87 236 generation time 48-50.49 Holorhyrida 23-24. 1 18 -fk h r d s u g e 39-41
cffms on mires 150, genmc m a d r v l i in mites Holorhyridac 24 incomplete juvenile, r# L v v v n i d a c 208
endospcmu.toph& 65.73 160-61 86-92 holomchy 45 larvipvity 36,140
Enicoccphrlidac, as miu mita in gut contents
? ! ?p
genital homeomorph 68.79 Indo- jumping 115 LP(io~iw27,40,52,63,
p d a m r s 122 155-59 urrabula 137 homcomo'phic stage 38 inducui mlavlcc 194-95 66,115,178. 181
entomophilous hypopi 213 fired digit 26 0
- 61.64.84-86 homology 7 inquiline 202,215-16 Mdomatia, wc domacia
Eo-hur u n h u r m flower mites 178-79 papihe 17 homopkFg 7 i n l u f d o d 18546
inraas Icafhlirs 184. 189
194-95 auid-fkding. as a G r o k u b (= C n r o w h o ~ o e c r a b swc Lrrhnurcufri4ur
Ephcmcropten, as non-ham pradapusion 143 116 xiphomida mice h a b i i 200-201.223 Eum'g~~lr
ofwatermites 217 Food wdx 98-103.100 gcologiclltimexale 9 hast-indud morphology pfcdamo of mira Icecha, as mite habitat 144.
cpistome 31 hngiug bchaviouf 52 G i s h a l e s 14 252 121-22.15960 210
Elryn#a 102 Fonnicidac, we ants Gier on maalr 124 hast &&city 249-52.262 prey of mira 14-47. legs of m i m 30
ErgimJvr clawn'bLz& Foruy. on mites 265 gLnduLrir 137 host swioching 250 149-50 lcwring 69
prrluM of 39 f b d mitcs 15-16.17&71 G 3 . r P h p 207 H o d and O c o ~ o r insmturion 60. sera& lenticulus 138
aina 172-73 in Rlaezok-ps 15 gnathobpxs 31 definition of p h o q 211 J p a r n d Lcpidogt).phurdmrurPor 215
Eriophpida 266 fizcalr 124-25 ~ O K ) 15.2G29.27
W evo~wion~ f p v v i d s r n hrpod* bocoelic, Lcpidopun, wc b u d i a .
as biomnml agents of frcrh water, wraquatic gnarhouaum 27 h m p h o q 205 m n c ) 8546 moth a r mites
weds 196 habhts good gales hypothesis, w h u m bot 6y 244 inscar 37 Lrpmkomia 17
as plant parasites 172-73 fnw female choice Humcm6ara 192 interscrual co&a 84-86 lcvitacion 163-64
diversity 259,261 as mite habitat 236 Grmdj-. Franwis 40 hummingbird-flower mites intasaual selection 75. l i i cycles. life sngcr 34-56
mating behariour 71.75 as pdators of mires group selccdon 268 178-79.244 82-86 Acviformes 37
 Pansitibrmes 38 associated with inverce- opinharoma 4 pH 16748
ANiteagona 43 bntcr 208-209 Oppk nivnr 30 Phakzngiumnu brwrrri.
fim- preduion 255 diversity 258-61 O p p e now 30 prrlvM 39
Limnorbarn %P 24 O r i h . ~crOribatida Phakngiourbida, possible
dLnstdulnas 157 fwsiLr 170 O n i d a 26 mice &onships 15
flxding 150 p a i c mcdranisnu Anrvcticl 97-98.100 P-bru 142
pH 167 87-88 ma, ~ o nwithr 209 pheromones 74,8142

-
p d t i o n by 149 Hall& o p 24 aquatic habitam 143-44 223 Philip 165
supunumary moults 44 m a k g bchaviour 62-66 Ymow 119-21.120 Pnmrhellvr 222.239 phoresy 54-55.202.
rwimming 162-63 morphology -24.27 as food b r intarr 121-23 Pvasitiformer 23-24 210-15
Limnohahmu -Am' 1% neauwphqp 110 PI food L r v c d m e s aquatic babicrp 134-35 cues for 214-15
Liadquist 213 oviwsition 35 122-24 diMsiry 261 lass of 207-208
finotctmnxs 175-76 ph&sy, moditied bioindic~mn 129-30 inverrcbnrcr, rrr0CLrion.s
litter, as mite habitat for 212 bothridid rplrillus 28 with 208-209
125-27 p&a of atduopods ~pmphP%y~ 106 madngkhrviwr 62-66 p& @tisin 204-205
I-, see reptiles 11 1-17 dorelopmeht 50 O n y Y 38 scaga modified for
I d matezompeticion rrachue 52 divusity 261 pvur- 212-13
89-90 aichobothrt 24 fsccPl pdlm and soil lor- mate choice 241-48 phorrcic 20
~undmt3m.Axel 183 mmmcrism 9 nest p;occaion h&rhais d o n 105 dcfinidon 199 phomomorph 213
mavOma 11 240-4 1 farcil 171 evolution of virulence phocopmtacdon 158-59
M d e h microbivo~mitivore,see neucnlinm 199 kmaic- 266-47 phototazis 163
m y an- and 208 functional groups Ncummrtr 87-88.91-92 evolurionvy mutes m phyllophc 179
mmmunal fkding 112 mi-M 265 nuring behaviour 69-70, guilds brredon di&ve 203-205 phylogcnctic rcconsvuaion
devdopntcnd rime 48 Mhmmbidiwn maorLuum 83 d i l i & r 106-107 hosts. m p k effects on 6-7
dung fauna 127 44 predation by 160 H u t c h i n r o b size ntiw 24 1-45 phy!ogenctic mdring 250
lprvipvity 36 migratory behaviour 52-55 Ncwdl, on levitation 128-29 hoa avoidma by mites phyGd gill 141
laving phorctic curia millipedes 209 163-64 incidcnml predomrs 192 239
214 mimicry 156-57.208-209 nidimle 202-203.22628. inmmcdLtc hosts for host choiee by pvrritic $ ~ . ~ k % r ~ /67 . k
p h o q on dmsophilib M i n o v , on f a d e r mires 24041 ~pewonns123 mim 238-39 Pby&nm,uspallidur 87-88
248 252 Nodnw 25, 129 .-I on 189-91 host defines against mires Phymgciidae 24.48,65,
p h o q on human bot fly mire pockets on liarb Notootignua 22 mating ~ v i o u 6 r 667 239-41 190.265-66
244 237-38 Nutring, on mammals a moss m i m 191-92 loss of 205-207 k d h g 182-83
prcwpuIatory mate guard- mice, word origin 3 habitat 229 mouthparts 27 plana 108409. 171-79. generic mcdunisms
ing 80 Mites of Mods and BurnjAk nymphal sngcs 37-38, ovipositor 28 195-96.205 182
male polymorphism, sn her- 2,220 42-43 phorcsy 209 pvasitoidism 199.209, induced resistance 194-95
emmorph, andropoly- Mixopmls 11 suppression of 4 2 4 4 prrdtcors of nematodes 221-22 leaf domaria 188-89
morphism modes of sperm uanshr. see 109 knsitcngoru 26 life cydc 181-82
mammals sperm mnsfcr OConnor 207-208 predators of mtifcrs 158 MCcyde4M4 on leaves 180
as mire habitat 226-30
-- - molluscs. as mire habitats odonares 2L&l9,24l, rockpools 138 maring behaviour 69-72 photoperiod 182
diversity of mite associates 152,203-204.2 10 24748 vamn of p h disease parasitism 205-207. P/yto~iJur
252-53 monophyly 7.14 omnivory IOelOl 192 209-210.216-19 devclopmend nu 48,
Man& First Rule 248 Monuignc 2 ontogtny Oribmulcr n'binlir 189 P-IYI rolcepmtonrm 182
marine m i m 135. 140 mars mites 191-92 Aaribrma 37 orlertes 183 54-55 infochemicals 194,265
marine scotpions see mouthpam Pu.siriformes 38 Omiahodoms 23637 parend a r c in mites 34-36 leafdomatt 189
Eurypterida aggressive ux of 29 suppreaion of nymphal Omi- 231,24041, krker 58-59.81 maring 65
mating bchaviour 62-72 ch&t&rarc 26-27, stages 42 2 W 7 ~hyrorclmau 134,137. 144,
hvuns 77-79 28.71 Ophiomgirtw 237 0nhog.ahmafamrbmntir 177 207-208
mate guuding 76-80 pictdngkudring 29. Opbbnymrr 237, 239 wmorephaon 1% pigments 158-59
May, on size and diversicy 171-75 Opilimcarida 15. 21 OS(MO~S.YCQUSPC~~~ piliwlous 213
259 spam uvlsfcr 29 O p i l i d 21 01 heidomcni&c 221 Pitgafumnq mating
Mayr, on unknown mire hu- moth- mites 200-20 1, Opilioacariforma 4, 15 r23Lwdqh mpmso- bchaviour 67
ms 127 204,214-15.220-21 dimity 260-61 35 Pimcliapbi&uspoakpolippba-
man chain l e d 10tH02 movablc digit 26, 28 morphology 21-23 ovip&tion 34-36 gw 241
hkgdopan. as non-hom of Mycl~norhm138-39, mourhpvrs 22 ovipositor P'nguiculi 189
watermites 217 14344 ~rcluvr39 Oribatida 28 P ~ M
M g i n i a 233 MilUcrian mimicry 156-57 rrhrionship to other mites wpm mites 31 egg sizc 207
MrrirtDCohm~nkmet*- mussels, scc molluscs 22-23 fish. and 16061
mida 20.27 muntdism 186-89. 199. sperm trnnrfer 23 p a e d o p a i i 44,177 mating 70
Maostomaca 1 1 222-26 Opiliona pacdomorphosis 44 parasitism by 219
Mcsostigmau mycorrhiue 109 parend care 34 Painc, on hod web science predation by 148
aquatic 135 Myi&cs mardonakii 20 relations to mites 18 103 swimming 162-63
 MITES:ECOLOGY,EVOLUTION
A N D BEHAVIOUR

pi& pha, prosonu 3 +h129

A%pmrnnir zizc Sm- 25 *mII'
see phyrotelmrp
P & ~ C U208 I
kosdgmaa RsI.il.k 235 and divcnity 259 scylophore 174 Thysanopren. Kcduips
(-Tmmbidibrmes) Ricinulei and relations to d i m known mim 14 srylastomes 218-19.245 ticks 23.87. ~c d o Ixodida
p h t parasim 108-109. duopods, predators of mites 18 largest and s d e s r sucking-miuobiioffi s u tocorpamy 64
171-79. 195-96.205 1 1 1-17.179-81.180 rianulei& 18 4647.56 funaional groups mchcac, independent evolu-
p h n apw 142 woditionr with invcrrc- mouthparts 22 pawcr rrlationship 51-52 supcrp;lrPrirism 212 tionsof 18-19
p~~ h@r 139 briar 209-10 mckpoob 138 nnge 32.4648.47 161-63 rnchdsysrems 141
Pbgs&'s I& divpsig 261 m k 146-47. 158 size ratios, Hunhinsoniul sw~lputghats162 cnnsgenic mircs 195,266
plsomorph 79 gamic mcchvlicms 87 M r i K i n r r 180 128 ~ b r m r 6 a u s67, 190 Treat 204
plumiwla 232 inamber 17&71 rust mites 172-73 skclcmn weed gall mitc 196 symbiosis 202 nccholes. see phytotelmaa
-hngrr bubonir 232 mating beluviour 63-72 ~ t d l ~15.=.25,27
m Sleeping Beauty M o r 96 symplcsiomorphy 7 uhypoch&onioid oribaddr
Podopolipidrc 30 piercing-sudring mierobi- slugs 200-201.210.244 ry~po-rphy 7 91
P0dm-y 64 vom 108 Sdto 78-79 Smith, on loss of pvrsirirm syringiwIer 232 mchoboduia
PaKilochinu 202,211,214, p h r puasires 109, 171-78 *dcrs 123-24 205 Syringophilidae 235 Acviforma 25
223.25 1 sa d o r 90-9 1 d u m r y x v c b 115-14 &s as hosts for mica 40. Syringcphiloida minor 235 rL camen- 12.189-90
pokn, &ding on 24, 178, a h Tmmbidibrma SmtMcnrirvnrotrr 1 1 200-201. botbridiJ seMillus in
205 Aataaorirpmni 15 s*p'ophagy 105 see 40reptiles agmau 10 Orilratida 28,189-90
polution I6748 p r o d u n Pvyice 44 Sarroptcr 230.249 snour mites 21 1 agmosu 10 defined 17
po~y&)my. =ham"s h ~ o n i r r r 15 ~ u h p r i f o r m e r 25 soil, as habitat 124-27 Tmonunellini 178 ma- 24
A~Lptmrononuc Irmcc h m g n m m r h 40.47 Samum+~ 207 solenidia 25 Tvtoncmidv 169 opilioaa&rmcr 21
p a a t i o n time 48 lhtonyabia 251 Smidmnurrdclaam salf-ugids. ocropod first bcnlcgallcria 193 Trigonirarbi& 14
rnatcguyding 76 249 &aDseiltic prdvva 40 ~
SIIUI 40 Ligs 178 ailobim larvae 17
polyphyletic 7 Pdaphidac as mite preda- mating 71 spvundry 92 laves 180.191 T w a k r r c r 136,236
PaFospMlY 64 tors 121 d y - l e g 231 spandrels 184 ma* TI rricasternum Z2-23.27
post-displacement 46 pseudourhmotoky 87 scabies 230 species richness. P - P ~ Y 215 Tmhommidinm mmbulanun
P - P ~ ~ Y--guudig pseudoPEorpions 16 sulpbcrymzas 190 rec biodiversity pvrsiroidism 209, 222
76 Psomptida 26 Schwubua 236 Sjxkorrhemr podrtmidn 40 221-22 T r o m b i i r m u 25-26, rrr

-
p d o n prtmmorphs 121 Schizomida 22 Sperm qui-t fcmda, caprure ako Prostigmata
ambush 113. 145. 148, P c q p m u mwrabdk mat- sb- 35.78-79 competition 58-59. of 30.76 uophicovcrhp 125
180 mg 72.237 -@r 223 80-82 Tmonuain;l. sa ratios rrophic spacia 102
vthropodr 111-17 Pdliidae. YS mire predators xolopenddid sym~phylvls of mires 30-3 1 -9 1 tmphyil& 215
cannibalism 116-17 121 121 prmdcncc 80-81.83 tcca 121 Tmpihchpr c&me 66
cruise 112 scorpions 11-12 uansfer 58-60. 155 telson (tlagellum) 9 Tmuasada 257
d & a . 117-121 ;g&y2;15
scrub itch 26,217, xenLo spermadun 68 Tcnuipdpidac 175-76 Tyckdka 17547,176
definition 199
hculrative 40.107, 179
inadend 192
rjYmots 213.221-22.249
wrub typhus 26
S~tacarwrrcamium 214
spernuchcca 61
spermatodictyl 29.62
spcrrmtophore 30.60.72,
T%z-
jumping 1 18
39
Tyda& 1 1 1. 171, 179.
186. 190
TdCY( 179. 190
Scydmunidac 1 2 2 73-75,8143, 155 turesaialcrurrawurr 13 Tpphegrr 107.
Tphlorbonnu 65136
s a sruks 40 spermarophoric organ 66 turcsmalisadon 12-14
hdknsitengona 205 ninforrzrs 126-27. 171, sea urchins 153,200-20 1 spermacornme 29.62 tares 61
~ a v c s179-83 184-8625742 regmenrs, suid reptition of spermamma 61 testosterone 240 U k eMDpM1S
mi= 121-24 m g h g behpviour 53 9 spider mim Teuuychidac Unwnicoh 31.70,77-78,
n d 109-11 d c g g c d aldl mim. see SliwbakIloida 16 as plant parasites 174-75 bioconml of w e d 152
prcccdespalasitlm 204 hkb#nsdemurmr r m d p u i t y 35 as prey of phytosciid mires 195-96 20S204
evolution of pansirism in
purrnit 112 reptiles sensillus. sre m&oboduia 182-83 m i p o t y bchaviour 53
dacorysarch 11S14 mite habicu 200-20 1, r e m i d recqradc 61 mare &ng 77 plans 174-75 kcding 149
sit-and-wait (ombush) 237-40.250 sex ratio manipuladon migration 53 Trnatychur &errorurn host specificity 25 1-52
113. 145,148, 180 p c a b r s of mites 123 89-9 1.224-25 silk production 29, 175 (=opu&) 195-96 pamsicism by 218
watcrmitcs 14-51 --sacking 250 sa-ncio thwry spider. mouthparts 22 tlinrcmiYI 196 s z g 162
p k 3-1 Rhagidin t k n d e - b i i --=ti05 sponges 152,205204 T.p+ 194-95 Umpod~dae123, 138,266
p m r d d i p t h 28.31. 143 mating 71 86-93 spomtheclc 222 TuniuK 175 umigmoa 154
prickly peu 195 R +ci 101 local muc competition spriogai4 thvurochrrr't 233 Usher rt al 95
Pridoli epoch. and the

-
fi*hurrobinii 89-90 Anrvfnc food webs drvramsis 119
coloniation of bnd 14 two-fold arra 86 99-100, 11 5 rhelytoky 87 V-jawbmni 205,249
hw '27.32.
178-79.244
posomp*ry nma-
guvding 75-76.79
size of sperm 8 1
Mnulumsr;lcr,snintcrrex- jumping 115
40
?&rmauanunnrcrknzir 165
Thompson et aL 247
V- mbiniae 77
Varauuur ipida 40,237
ual c0nAiff
M p L y U o d a 24647 &
- sdeaion 58-59.73. S l c r c o ~27.98.100. &ps vn*' rrichobochrl-likc
progeneris 45.46 245-48.267 102, 174 hom of mite p u u i m i h smc 24
h k o m m i a whceIm' 17 Rbodnca+ur 40.47 Soncnshinc 73 Stigmaeidae 1 8 0 4 1 v d m m i m 26
24VnmranrCurpynuhippcu1 Rhynic Chert, fb*til m i m silk 29, 175 stored-produa pera 226-27 virulena. evolution of
215 14 SiMOpc~r45,211.213 SrrrrtioLukyr 1 1 1 26667
MITES: ECOLOGY,EVOLUTIONAND BEHAVIOUR

v i m , mites as vectors 174. gas exchange 142-43 w u c r hyacinth 177

196 lasr survivors 165 Wheeler, on inquiliner 2 16
loss of pansitism in larvae widigig mircs 180
wandernymphen 54. 205-207 Wdrlanvln 205
Wu&k irr 206 purpitism by 132, WoUdia 267
Wasm~nntnmimicry 216-19
208-209 poUurion 16748
wasps, Hymcnoptul posclaml p a n s i b
water mi- 26,66,69-70, 151-52
72.91 predation on 1 5 5 4 0
and firh 150.16041 p&on rates 150-51
bioindiaroro 164-68 d t water 140
colour and caste 155-59 substrate e 5 166
defined 136-37 swimming 162-63
depth range 165 tempmure range 165