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Biology and Evolution of the Mollusca
Winston F. Ponder, David R. Lindberg, Juliet M. Ponder
Shell, Body, and Muscles
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Winston F. Ponder, David R. Lindberg, Juliet M. Ponder
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3 Shell, Body, and Muscles
In this chapter, we provide an overview of the external body on the taxon. In swimming Nautilus and crawling octopods,
of molluscs, comprising the mantle, the shell and its forma- the ventral axis is rotated about 60°, while in cuttlefish and
tion and growth, the epidermis and associated structures, the squid, the body axis is rotated a full 90° in its life orientation
foot and operculum (of gastropods), mucoid secretions, loco- (Figure 3.1).
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motion, and general information on cartilage and muscles. Early molluscs were probably1 bilaterally symmetrical,
Some external structures, such as the suckers found in many although the adult orientation of the anterior-posterior axis of
coleoid cephalopods, are also important external features, but the early mollusc is less certain and largely depends on the
as they are confined to a single group, we deal with them in putative sister taxon and outgroups. If the traditional mollusc-
the appropriate taxon chapter. annelid relationship is favored, the adult orientation of the
early molluscan body extended along an anterior-posterior
axis with a low dorsoventral axis, as in chitons, aplacopho-
3.1 BODY SYMMETRY AND AXES
rans, and monoplacophorans (Figure 3.1). In most of these
Molluscan body axes are complicated, and there can be up animals, the ventral and dorsal orientation of the body is
to three distinct body orientations which transform dur- maintained throughout life.
ing ontogeny. As described in more detail in Chapter 8, in Besides anatomical and ecological changes in body axes,
most bilaterally symmetrical animals the embryonic blastula molluscan evolution has been characterised by organ asym-
has an animal-vegetal polarity, and during gastrulation, the metry and displacement. The rotation of the viscera on the
blastopore forms at the vegetal pole (Biggelaar et al. 2002). head-foot in gastropod larvae during torsion is a famous
In deuterostomes, the blastopore becomes the anus, thus example of twisting. Numerous additional changes in body
establishing the vegetal pole as the posterior (P) of the embryo axes occur in gastropods (Figure 3.2), including detorsion,
and the animal pole as the anterior (A). In protostomes, the which results in the movement of the mantle cavity posteriorly
initially posterior vegetal blastopore is rotated from its ini- along the right side of the body. Some ‘pulmonate’ gastropods
tial position to an anterior-ventral position where it typically have a posterior opening to the modified mantle cavity (as a
forms the mouth opening (Biggelaar et al. 2002). In molluscs, lung), and this cavity is lost in some other heterobranchs (see
this reorientation of the embryonic A-P axis during the forma- Chapters 4 and 20).
tion of the trochophore larvae is driven by cell proliferation Bivalves have also undergone considerable modification.
and migration on the embryonic dorsal surface which dis- Their shell is divided into two valves, accompanied with con-
places the blastopore ventrally and then anteriorly (Biggelaar siderable lateral compression, and the mantle cavity typically
et al. 2002; Wanninger & Wollesen 2015). Thus, by the mol- surrounds all or most of the body. Changes in orientation
luscan trochophore stage, the original embryonic A-P axis is largely result from byssal, as in mussels, or cement attach-
no longer linear, and the originally posterior blastopore has ment, as in oysters (see Figure 3.3 and Chapter 15).
shifted approximately 90° to the ventral surface. In shelled In chitons, aplacophorans, and monoplacophorans the
taxa, further cell proliferation and migration resulting from viscera (visceral mass) is distributed along the body, but in
the formation of the dorsal shell gland displaces the second- bivalves, it is compacted laterally and dorsally, allowing
ary anal opening ventrally and anteriorly. This produces the space for an expansive mantle cavity between the enclosing
characteristic U-shaped gut indicative of ano-pedal flexure shell valves. In scaphopods and cephalopods, it is elongated
and obscures the original embryonic body axes. A third reori- dorsally. In Nautilus (and many fossil cephalopods such as
entation of the body axes may occur after metamorphosis the ammonites) this elongated tube has been coiled to enable
when the animal assumes its adult life orientation. Life (or more efficient packing of the viscera. In gastropods, the dor-
‘ecological’) orientation often differs from the anatomical sally extended body is also coiled, but usually asymmetrically
axes in molluscs (Figure 3.1). Some caudofoveates burrow in into a helical coil.
the sediment with the posterior end dorsal, while scaphopods
burrow obliquely to near vertically in the sediment with the
head and foot positioned ventrally. In living cephalopods, the
ventral axis is typically rotated from 45° to 90° depending 1 Not necessarily true if Brachiozoa are the sister taxon.
55
56 Biology and Evolution of the Mollusca
Polyplacophora Monoplacophora Aplacophora

Scaphopoda
Gastropoda Bivalvia
Cephalopoda
dorso-ventral axis of body gut

antero-posterior axis of body, including viscera
FIGURE 3.1 Anatomical axes in Mollusca. All animals in life orientation. Some aplacophorans are buried in an inclined or near vertical
orientation, others lie horizontally. Original.
Patellid (Patellogastropod) Vermetid

Early planispiral (Caenogastropod)
gastropod Trochid (Vetigastropod)
Olivid (Caenogastropod) Heteropod Cephalaspidian (Heterobranch) Doridid (Heterobranch)

(Caenogastropod)
--- dorso-ventral axis --- axis of volution --- life-orientation axis
FIGURE 3.2 Axis of symmetry in Gastropoda showing body and shell axes relative to life orientation. Redrawn and modified from
Morton, J.E. and Yonge, C.M., Classification and structure of the Mollusca, pp. 1–58, in K.M. Wilbur and Yonge, C.M., Physiology of
Mollusca, Vol. 1, Academic Press, New York, 1964.
Shell, Body, and Muscles 57
INFAUNAL EPIFAUNAL
Mytilid (Pteriomorphia)
Pteriid (Pteriomorphia)
Venerid (Heterodonta)
Solenid
(Heterodonta)
Pectinid (Pteriomorphia)
--- dorsoventral axis

--- anteroposterior axis
Ostreid (Pteriomorphia)
FIGURE 3.3 Axes of symmetry in bivalves. Original.
3.2 SHELLS AND SPICULES single shell (univalved), and the shell is secondarily lost in
some members of the latter two groups.
Molluscan shells have attracted the interest of a wide range of While most gastropods are univalved, a few secrete
scientists from many disparate disciplines as well as natural- an accessory shell valve after the primary shell is formed
ists, artists and collectors, and the public. (e.g., hipponicids and bivalved sacoglossans). Like the oper-
A calcium carbonate shell or spicules is the most obvious culum, these second shells are not true valves because they
molluscan marker. Whether these shells were formed from are not secreted by the shell gland.
fused spicules or not is still debated (see Chapter 13). In living In aplacophorans, the body is covered by spicules embed-
molluscs, only aplacophorans exclusively have spicules, while ded in a cuticle covering the epidermis. A cuticle also cov-
chitons have eight shell plates surrounded by a girdle covered ers the dorsal surface of chitons and the girdle ornamentation
with spicules, scales, or hairs. (spines, scales) is embedded in it, and in some taxa it is devel-
The earliest putative mollusc shells (Rostroconchia) in the oped into hairs. Calcareous dermal spicules are also present
fossil record are from the early Cambrian (535–530 mya). in some heterobranch slugs (see Chapter 20).
Disarticulated plates, cap-shaped, and simple curved or The molluscan shell is a calcareous structure that covers
coiled ‘shells’ are also present during this period and have some to all of the upper surface of the animal. It is generally
been interpreted as being shell plates of chiton-like animals, covered by a thin outer organic layer, the periostracum, which
monoplacophorans, or early gastropods. Bivalved shells also is composed of sclerotised proteins and is at least analogous,
appeared in the Cambrian (520 mya) although not all of these if not homologous, to the cuticle of chitons and aplacophorans
were true Bivalvia (see Chapter 13). (Checa et al. 2017). The hard part of the shell is comprised
Bivalves have two hinged shell valves, while monopla- of layers of calcium carbonate comprised of the polymorphs
cophorans, scaphopods, gastropods, and cephalopods have a calcite and/or aragonite. A small part (0.01%–5% by weight)
called the brachiophore. In the Inarticulata, the shell is com-

posed of calcium phosphate and chitin, but in the Articulata it
is made up of proteins and calcite. As in molluscs, brachiopod
shells have an outer organic periostracum which seals off the
crystallisation chamber. Many articulate brachiopods have
two shell layers, an outer cryptocrystalline layer and an inner
secondary fibrous prismatic layer. Other shared shell charac-
ters include three calcitic shell microstructures (also shared
with Bryozoa), vesicular wall structure, shell pores, and mus-
cle attachment scars (Vinn & Zatoń 2012). Annelid calcar-

eous tubes, like molluscs, have both aragonitic and calcitic
shell structures, but typically lack an organic matrix.
The chemical machinery involved in calcification is
complex, but, surprisingly, the ability to produce a skeleton
FIGURE 3.4 Accretionary shell trajectories in bivalves and gas- evolved in many groups in less than 30 million years, in the
tropods. Original. early Cambrian (544 mya). This can only be explained with
any credibility if the required chemical pathways for biomin-
eralisation were already in place and serving other purposes
of the shell is organic (Lowenstam & Weiner 1989) and, apart (Marin et al. 2000) (see Chapter 13).
from the periostracum, mainly glycoproteins.
All molluscan shells are produced by incremental addi-
tions to their edges and inner surfaces (Figure 3.4). The grow-
3.2.2 Shell Geometry
ing edges of the shell are enlarged by shell material formed at The growth and shape of most shells conform to a few basic
the mantle margin (at the edges of the aperture in a gastropod mathematical principles. Shells grow by differential growth
and the edges of the shell valves in a bivalve). The organic around an expanding aperture and, while most maintain the
periostracum is secreted first and forms the outermost layer of same shape from juvenile to adult, others can change slightly
the shell, and may be mineralised (Checa et al. 2014). Unlike or markedly as they grow. The limpet shell form is a simple
the rest of the shell, the innermost shell layer is not secreted cone which may or may not be symmetrical. The apex of
by the mantle edge, but deposited by the outer surface of the some limpets is curved and an extension of the curve results
thin inner (or dorsal) mantle that underlies the shell. Growth in a spiral which may be symmetrical (i.e., isostrophic or
at the edges ceases when the mantle margin is withdrawn planispiral – in the same plane – as in Nautilus and many
from the shell edge, but deposition of the innermost shell layer ammonites; i.e., it is bilaterally symmetrical), or asymmetri-
continues. cal (i.e., anisostrophic or conispiral – as in most gastropods).
The multiple plates of chitons may have been indepen- Shell coils approximate a logarithmic spiral (Figure 3.5) in
dently derived from a single subdivided shell so cannot nec- which the distance between adjacent coils increases by a con-
essarily be regarded as primitive (Lindberg & Ponder 1996). stant factor. A small factor results in a spiral shell, while a
Reduction and subsequent loss of the shell, notably in some
cephalopods and gastropods, is a derived condition.
While shell morphology can often be correlated with
lifestyle and habitat, this is by no means always the case as
similar shell morphologies do not necessarily indicate similar
α
habits or habitats (see Section 3.2.3). r
3.2.1 Comparison with Outgroups θ

The ability to secrete an exoskeletal structure composed of
calcium carbonate is common in the animal kingdom. Among
the lophotrochozoans which secrete shells, the most mollusc-
like are the Brachiopoda with their bivalve shell, while a few
polychaetes secrete calcareous tubes and some bryozoans
(Ectoprocta) have calcareous skeletons. Brachiopod shells
superficially resemble bivalves, but differ from most bivalves FIGURE 3.5 A logarithmic spiral is generated by a curve deter-
mined by r – the distance from the point on the curve to the centre
in having two morphologically different valves which are
(origin) and θ, the angle between a radius and a horizontal line to
bilaterally symmetrical through their dorsoventral axis, while the right of the origin. α is a constant, the angle between the radius
most bivalves are symmetrical through their anteroposterior and a tangent to the curve. Redrawn and modified from Vermeij,
axis. Articulate brachiopods differ markedly from bivalves in G.J., A Natural History of Shells, Princeton University Press,
having a fragile internal shelly skeleton for the lophophore, Princeton, NJ, 1993.
large factor produces a slight curve, as in a scaphopod shell. If

the aperture is not offset, a planispiral coil results, but if it is TABLE 3.1
inclined toward the right of the animal a dextral (right-handed) Calculation of Raup’s (1962) Four Parameters of Shell
coiled shell results, while a sinistral (left-handed) coil is pro- Coiling Based on the Measurements in Figure 3.6
duced if the aperture is on the left (Table 3.1; Figure 3.6).
Parameter Measurements from Figure 3.6
The mathematics of shell coiling has been studied by
numerous workers (e.g., Raup 1962, 1966, 1967; Raup & a1
Apertural shape (S)
a2
Michelson 1965; Savazzi 1985; Illert 1987, 1989; Ackerly
1989; Stone 1996; Rice 1998; Noshita 2014; Urdy 2015) and w 2 w3 wn
+ …+
Whorl expansion rate (W) w1 w 2 wn − 1

much of the early literature is neatly summarised by Vermeij
n −1
(1993). Most shell shapes result from variations on these
d1
themes, and much of that variation is summarised in Table 3.2 Position of generating curve (D)
d2
and illustrated in Figure 3.7. Attempts to correlate actual shell
y
geometries with theoretical possibilities (e.g., Hickman 1985a; Whorl translation (T)
r
Schindel 1990) have shown that some parts of the ‘theoretical
morphospace’ are not occupied by living taxa, but have been Source: Lindberg, D.R., Malacol. Rev., 18, 1–8, 1985b.
by extinct taxa, whereas other morphospaces have never been Note: a = apertural dimension, w = whorl expansion, d = position of gener-
occupied (Raup & Michelson 1965; Schindel 1990). ating curve, y = translation, and r = radius.
radius
translation
ape
rtur
1
e2
e
rtur
w3 w2 whorl 1
a pe
w5 w4
d1 position of generating
curve (d2)
FIGURE 3.6 Shell measurements required for the derivation of the Raup (1962) four parameter model of shell coiling. Also see Table 3.1.
Redrawn and modified from Lindberg, D.R., Malacol. Rev., 18, 1–8, 1985b.
TABLE 3.2
Shell Shape and Coiling Parameters
Simple Cone Planispiral Conispiral
Growth rate Low High Low High Low High
Apertural Narrow cone Broad cone Loose coiling Tight coiling Loose coiling Tight coiling
expansion
Curvature NA NA Loose coiling Tight coiling Loose coiling Tight coiling
Aperture NA NA NA NA Low spire High spire
moving on
Z-axis (spire)
of the shell edge grow relatively faster, with points further

away from the apex usually growing fastest.
In many bivalves, the valves become inflated as growth
is slows with increasing age so that older, larger individuals are
ax
In
cr
m more inflated (Vermeij 1990).

fro
ea
sin
ce Various shell shapes have evolved multiple times in gas-

an
g
ist
ex
d tropods. For example, the limpet and conical shell shape have

pa
g
ns
in often evolved in many lineages. In most gastropod limpets

as
io
e
n
cr ‘anterior’ (i.e., post-torsional anterior) dilation exceeds (or in a

ra
In
te
few species equals) ‘posterior’ and lateral aperture expansion,

but in patellogastropod limpets the reverse is true with ‘poste-
rior’ dilation usually exceeding ‘anterior’ and lateral aperture
Increasing translation expansion. Also, uncoiled shells occur in several unrelated
groups, such as Truncatelloidea (e.g., Caecidae and some
cochliopids), Vermetidae (Vermetoidea), and Siliquariidae
(Cerithioidea). Very open coiled shells with the whorls wholly
or partially not in contact occur in certain taxa across at least
11 families of living gastropods (Rex & Boss 1976), although
no families are exclusively open coiled.
It is generally thought that, once completely lost, coiling
FIGURE 3.7 Shell models generated with different growth
parameters – whorl expansion (the shape of the generating curve
cannot be ‘reinvented’ so an uncoiled limpet, for example,
is equivalent to the shape of the aperture), translation (the height could not revert to a coiled snail. Collin and Cipriani (2003)
of a generating curve), and distance from the generating curve to provided an example in Calyptraeidae showing that coil-
the axis. Redrawn and modified from Raup, D.M., J. Paleontol., 40, ing was apparently reinvented in uncoiled slipper limpets
1178–1190, 1966. (Crepidula) when a lineage gave rise to the coiled genus
Trochita. This is at variance with some other results (Simone
2002), and these hypotheses remain untested with new data.
Small changes in growth parameters result in changes
In another case involving a vermetid, Gould and Robinson
in shell shape and coiling. Tighter coiling results in over-
(1994) found that the reinvented coiling differed from normal
lapping sutures and tall, conical shapes, while looser coil-
coiling. Some heteromorph ammonites are also hypothesised
ing forms a flatter shell with, at the extreme, open coiling
to have re-evolved tightly coiled shells, Scaphitidae perhaps
(whorls not touching) or even an uncoiled shell. Changes in
being the best known example (Landman et al. 2017).
shell shape also occur as growth changes throughout life.
Figure 3.8 shows how the timing of different growth factors 3.2.2.1 The Direction of the Coil (Handedness)
can alter the shape of a conical gastropod shell. For exam-
Although some gastropods have limpet-shaped or planispiral
ple, when growth is relatively rapid in early life, but slows
shells, it is more likely that torsion afforded advantages to ani-
down later, the spire has a dome-shaped profile, while if
mals with conispiral shells, enabling tighter coiling and hence
growth accelerates with increasing age, the spire is concave.
a longer spire. When a conispiral shell is viewed with the
A constant growth rate produces a convex cone, while an
spire uppermost and the aperture opening facing the observer
exponential rate produces a straight-sided cone. Thus, these
is on the left, the shell is sinistral, and if it is on the right, it
relationships are far from simple. There is also a relation-
is dextral.
ship between the growth rate and expansion – some parts
Shell coiling direction (chirality) is determined by proteins
(e.g., nodal) which determine the direction of cleavage dur-
ing early development (Figure 3.9) (Levin 2005; Kuroda et al.
2009).
In hyperstrophic snails, the shell coils in the opposite direc-
tion along the vertical axis of coiling (the Z-axis) (Figure 3.10).
Thus, if a hyperstrophic shell is orientated the same way as a
dextral shell, it would appear to be sinistral although anatomi-
cally the animal remains dextral, while the shell is apparently
sinistral when orientated with the spire uppermost.
FIGURE 3.8 Variation in spire outline in a gastropod results from Planispiral coiling is rather rare, particularly in living
different rates of growth. When exponential growth occurs a simple
marine gastropods (Vermeij 1975), although it was sometimes
conical spire results, as in the second figure on the left. If the growth
rate increases with age, a concave spire results (as in the left-hand common in the Paleozoic. Why the vast majority of modern
figure), while if there is a decrease in growth rate with age, a con- gastropods exhibit dextral coiling has long puzzled malacolo-
vex spire will result (as in the two right-hand figures). Redrawn and gists. The fossil record shows that although both sinistral and
modified from Rice, S.H., Paleobiology, 24, 133–149, 1998. dextral coiling were common in early gastropods, dextral taxa
Sinistral Dextral
FIGURE 3.9 Chirality in snails is determined by the early cleavage pattern. Redrawn and modified from Grande, C. and Patel, N.H.,
Nature, 457, 1007–1011, 2009.
Dextral Sinistral
orthostrophy orthostrophy
(dextral shell (sinistral shell
and body) and body)
Dextral Sinistral
homostrophy homostrophy
Sinistral Dextral
hyperstrophy hyperstrophy
(sinistral body (dextral body
dextral shell) sinistral shell)
FIGURE 3.10 Shell and body coiling. Diagram illustrating orthostrophy, hyperstrophy, and hypostrophy. Middle vertical row redrawn and
modified from Linsley, R.M., Mem. Nat. Mus. Vic., 39, 33–54, 1978c.
later became by far the dominant form with over 90% of liv- shell would be inherently less efficient than a dextral one in a
ing coiled gastropods being dextral (Schilthuizen & Davison dextral shell. It is, however, easier to imagine reduction in effi-
2005). Various authors have related this dextral bias to the ciency where the chirality of the animal and shell differed.
effects of torsion on the body, but in sinistral taxa with sinis- Hyperstrophy occurs in the larval stages of most marine
tral animals, torsion occurs in the reverse direction to dextral heterobranch gastropods and in the fresh-water caenogastro-
taxa, and it is difficult to see why a sinistral animal in a sinistral pod genus Lanistes (Ampullariidae). Heterostrophy occurs
Asymmetry of bivalve shell valves between left and right

occurs rather commonly and is roughly equally divided across
the class, but can be constant within a family. Asymmetry
may be minimal to extreme, with minimal examples includ-
ing small differences in inflation or one valve overlapping
another. More extreme examples are often associated with
cementation. For example, asymmetrical cementing pect-
inoideans are attached by the right valve despite cementation
FIGURE 3.11 Examples of heterostrophic protoconchs. Redrawn evolving multiple times within Pectinoidea, while oysters are
and modified from Robertson, R., New York Shell Club Notes, 329, always cemented by the partially to completely flattened left
12–18, 1993a. valve. Within the chamids and rudists, however, either valve
is used, depending on the species. So-called torsion in a few
bivalves (Arcidae, Mytilidae, the extinct Bakevelliidae, and
when there is a change in coiling direction during growth, the hiatellid Cyrtodaria) involves twisting of the valves around
as is obvious in the protoconchs versus the teleoconchs of the anteroposterior axis, the best known example being the
some heterobranch gastropods (Figure 3.11). arcid Trisidos (McGhee 1978; Morton 1983b; Savazzi 1984)
As noted above, most modern gastropods are dextrally (Figure 3.12).
coiled but the shells of members of a few gastropod fami- In the Silurian and Devonian, five or six lineages of
lies, namely, Triphoridae,2 Planorbidae, Physidae, as well shelled cephalopods (nautiloids and ammonoids) had conispi-
as most atlantid heteropods and thecosome pteropods, and ral coiled shells with sinistral and dextral taxa about equal
some genera and species of stylommatophoran land snails in number (Vermeij 1975). Some of these changes in coiling
are sinistrally coiled. In addition, some species or genera in may have been pathological variations resulting from sclero-
other families scattered through the gastropods are also sinis- biont3 infestation during the life of the ammonites (Stilkerich
tral (Vermeij 1975; Gould 1985; Robertson 1993a, 1993b). et al. 2017). Further changes in coiling parameters in ammo-
In sinistral taxa, the animal within the shell is also sinistral. noids also occurred in the Mesozoic with the appearance of
Freak coiling reversals (to sinistral) occur in many gastro- the uncoiled heteromorph ammonites (see Chapter 17).
pods, but are rare (e.g., Schilthuizen & Davison 2005). Such
sinistral sports, or occasional taxa that normally have sinistral
shells, usually have a dextral animal. 3.2.3 Shell Shape and Habit
The distribution of sinistrality in gastropods indicates The morphology of a shell is often thought to be correlated
that change in chirality has occurred repeatedly in the class, with habits and habitat. While many such examples seem to
particularly in non-marine taxa. Studies on land snails have justify this general observation (e.g., gastropods with large
shown that in some stylommatophorans a single gene may apertures clinging to wave-swept platforms, oysters cemented
be responsible for chirality and occasionally promotes spe- to rocks, burrowing snails with streamlined shells, etc.), often
ciation (e.g., Gittenberger 1988; Asami 1993; Schilthuizen &
Davison 2005). In internally fertilising gastropods, mat-
ing becomes difficult between partners of opposite chirality
because their genitalia are on the wrong side of the body.
Thus, selection would normally act against a change in coil-
ing direction (e.g., Schilthuizen & Davison 2005), although
exceptions occur, as for example, in the stylommatophoran
land snail Amphidromis where both left and right coiled snails
often occur in approximately equal numbers in interbreeding
populations (Schilthuizen et al. 2007, 2014).
Genetic factors are not the only influence affecting coil-
ing patterns in gastropods. Experiments in which near pla-
nispiral planorbid shells were weighted on one side, causing
the shells to lie at an angle instead of near vertically, resulted
in a change in the coiling pattern toward the weighted side
(Checa & Jiménez-Jiménez 1997).
Reversal of polarity of bivalve valves can be seen in some
asymmetrical bivalves like Chamidae (Odhner 1919) or,
uncommonly, in bilaterally symmetrical bivalves where the
hinge is transposed (Matsukuma 1996) so the hinge features FIGURE 3.12 The ‘twisted arc,’ Trisidos tortuosa, dorsal and lat-
normally seen on one valve appear on the other. eral views. Orginal
2 There are a few dextral triphorids. 3 Organisms living on hard substrates such as shells.
shell morphology is not readily correlated. For example, simi- substratum surface when the animal is crawling. This latter
lar shell morphologies frequently occur in different habitats, group often have elongate and/or siphonate apertures, while
thus frustrating attempts to correlate them. Limpets are found those with inclined apertures usually have simple rounded to
in a variety of habitats including wave-swept rock platforms oval openings (e.g., Vermeij 1993).
and in fast-flowing rivers, but also on various deep-sea bio-
genic substrata, at hot vents, and in quiet lakes and ponds.
3.2.4 Gastropod Shell Orientation in Life
Other limpet-like gastropods are parasites on bivalves or
starfish. Thus, limpet-shaped shells function well in many Linsley (1977) investigated shell orientation in gastropods
very different habitats and suggestions that strong currents in relation to the animal and substratum and proposed that
or wave action select for limpet-shaped shells are an over- coiled marine gastropods followed several ‘laws’. The first
simplification (Ponder & Lindberg 1997). There are many two and last two relate to the aperture, the other to the spire.
other examples of convergent shell morphology, including These ‘laws’ are (from Linsley 1977):
cockle-shaped shells of several groups of shallow-burrowing
bivalves and the whelk-like shells that have appeared in sev- Law 1: The Law of Radial Apertures4: Gastropods of
eral lineages of carnivorous caenogastropods. Similarly, elon- more than one volution with radial apertures do
gate tall-spired gastropod shells are often found in shallow not live with the plane of the aperture parallel to the
sand burrowers such as Terebridae, but other groups with very substratum. Most typically it is perpendicular to the
different shell morphology appear to be equally well adapted substratum.
to this mode of life (e.g., the globular Naticidae). Also, some Law 2: The Law of Tangential Apertures: Gastropods
tall-spired shells have very different lifestyles, the terrestrial of more than one volution with tangential apertures
Clausilliidae which live on rocks or tree trunks being one such live with the plane of the aperture parallel to the
example. substratum.
The orientation of gastropods in relation to the substratum Law 3: The Law of Shell Balance: If the shell of a gastro-
is also related to the nature of the aperture – whether it is pod is supported above the body, it will be positioned
radial or tangential (Linsley 1977). An aperture is ‘radial’ if so the centre of mass of the shell and its contents is
its plane passes through the axis of coiling, while the plane over the midline of the cephalopedal mass.
of a ‘tangential’ aperture is tangent to the last whorl of the Law 4: The Law of Apertural Re-entrants: Angulations
gastropod so the aperture and the ventral-most part of the last or re-entrants on the aperture indicate inhalant
whorl lie in the same plane (Figure 3.13). Radial apertures are or exhalant areas; inhalant areas will be directed
uncommon in living gastropods, being found in some living anteriorly.
vetigastropods (e.g., some trochoideans such as Liotiidae and Law 5: The Law of Apertural Elongation: Gastropods
Angariidae), in architectonicids, and in the tiny omalogyrids, having elongated apertures possess only a single gill
but they are common in older fossil gastropod taxa, including and develop a water flow through the mantle cav-
most bellerophontids, and in most coiled cephalopods. A gas- ity from anterior to posterior, along the long axis of
tropod with a tangential aperture can clamp to the substratum, the aperture; this axis is subparallel to the anterior-
which is impossible with a radial aperture. These apertural posterior axis of the foot.
types are further discussed below (see Section 3.2.4).
The lip of a gastropod shell aperture, when viewed from In gastropods, how the shell is carried on the body is cor-
the side, can range from a steep to moderate angle to the axis related with habits and habitat. If efficiency is achieved when
of coiling (prosocline), to parallel to it (orthocline), or at a the shell is ‘balanced’ on the foot as Linsley (1977) theorised,
negative angle (opisthocline). In conispiral gastropod shells with the centre of mass of the shell balanced over the midline
with a steeply inclined prosocline aperture, the snail crawls of the head-foot, such ‘balance’ can be achieved in two main
with the shell apex inclined obliquely. In those where it ways (Figure 3.14):
does not slope (orthocline), the shell lies horizontally on the
• Lowering the coiling axis
• Swinging the shell so the coiling axis is approximately
parallel with the longitudinal axis of the foot – a process
called ‘regulatory detorsion’ by Linsley (1978b).
Snails employ a combination of these two processes to achieve

a ‘balanced’ shell – by adopting a low centre of gravity and
Radial aperture
maintaining a tangential aperture (Vermeij 1971). Some have
Tangential aperture also argued that the lower angle of the shell to the foot has
plane of aperture
FIGURE 3.13 The two main types of aperture recognised

by Linsley (1977). Redrawn and modified from Linsley, R.M.,
Paleobiology, 3, 196–206, 1977.
4 See Section 3.2.3 and Figure 3.13.
shell coiling axis shell axis straightens relative to foot shell axis raised relative to foot
vertical shell axis

shell axis lowered relative to foot shell spire lengthened
horizontal shell axis
FIGURE 3.14 Some examples of changes in gastropod shell orientation relative to the head-foot. Taxa from left to right are:- top row:
Ampullariidae, Pleurotomariidae, Trochidae, second row, Helicidae, Littorinidae, Buccinidae, third row, Neritidae, Cerithiidae, Conidae,
bottom row, Patellidae, Terebridae, Olividae. The examples in this figure are not a phylogenetic series, but show trends in morphology.
Redrawn and modified from various sources including Hickman, C.S., Comparative morphology and ecology of free-living suspension-
feeding gastropods from Hong Kong, pp. 217–234, in B. Morton & Dudgeon, D., Proceedings of the Second International Workshop on the
Malacofauna of Hong Kong and of Southern China, Hong Kong, 6–24 April 1983, Vol. 1 and 2, Hong Kong University Press, Hong Kong,
China, 1985b.
the added benefit of drag reduction and consequently enables triphoroideans, tonnoideans, and neogastropods. Distinct
more rapid movement (Linsley 1978a, 1978b). Linsley (1977) exhalant canals are less common, being especially well-
noted that exceptions to his Law 3 included shells with the developed in many conoideans, some triphoroideans, and
aperture placed markedly on one side as in Conidae. High- Bursidae. Exhalant shell slits or holes occur in some vetigas-
spired forms such as many cerithioideans and terebrids also tropods with two ctenidia (Pleurotomariidae, Scissurelloidea,
do not conform well as the apertural plane is parallel to the Haliotidae). Apertural elongation is common in neogastro-
axis of coiling. A few groups employ different strategies, such pods, but uncommon in other caenogastropods, although
as some Strombidae and Xenophoridae, which use spines to seen in some such as many Strombidae, and all Ovulidae and
prop up their shells. Cypraeidae, where it is combined with considerable expan-
The fourth and fifth laws relate to the aperture of caeno- sion of the last whorl which effectively places the centre of
gastropods. Inhalant canals are found in some cerithioideans, gravity of the shell over the middle of the foot.
3.2.5 Larval Shells and Their Formation but in bivalves a groove is formed which develops into the
hinge line.
The larval shell is produced initially from the shell gland (see Although they noted these differences, Haas (1981) and co-
Chapter 8 for details). Larval shells (sometimes called embry- workers (Haas et al. 1979) concluded that shell formation in
onic shells) are called protoconchs in gastropods and prodis- both chitons and conchiferans is similar. They suggested that,
soconchs in bivalves. Chitons lack a larval shell and bivalves in chitons, specialised epithelial cells proximal to the shell
have paired cap-shaped prodissoconchs aligned in the lateral plates formed a ‘properiostracal groove’ that produces a thin
rather than in the anteroposterior plane. The fossil bivalved organic pellicle (properiostracum) which facilitates the depo-
group Rostroconchia differ from bivalves in having a larval sition of the shell (see below).
shell on one valve only and lacking a flexible hinge connect-
ing the valves. In monoplacophorans, scaphopods, and shelled

cephalopods the larval shell rests symmetrically on the tele- 3.2.6 Shell Formation/Secretion
oconch. In most of these taxa it is cap-shaped, although in The shell is secreted by the mantle (see Section 3.9) and typi-
scaphopods it is tubular; another interesting exception is the cally covers the viscera and the mantle cavity (see Chapter 4),
very unusual planispiral larval ‘ammonitella’ of the extinct thus protecting and supporting the soft body. The shell is a
ammonites. In gastropods, the larval shell is coiled or, in complex combination of organic material and different con-
patellogastropods, is caecum-like. figurations of calcium carbonate crystals that in combination
The protoconch is lost in adult scaphopods, but is often produce a mechanically strong structure. As an example,
retained in adult bivalves and gastropods and can provide an nacre, a crystalline form of aragonite, is over 1000 times
easily accessible marker to determine life history character- stronger than non-crystalline aragonite (Jackson et al. 1988).
istics. For example, in gastropod and bivalve larvae that feed For some time, it was generally assumed that crystals mak-
in the plankton (planktotrophic), two separate larval growth ing up the shell crystallised from a supersaturated solution
stages can be distinguished in the larval shells (protoconch or in the extrapallial space between the mantle edge and the
prodissoconch I and II), the former formed as the initial shell, periostracum, but recent studies have shown that the process
the latter growing during planktonic feeding. More detailed is much more complex than that. It involves an organic matrix
information on larvae and larval shells is given in Chapter 8 (see Section 3.2.6.2) which is elaborated within the extrapal-
and in the taxon chapters. Aspects of the evolution of gas- lial space using a wide variety of macromolecules, and it is in
tropod larval shells (protoconchs) through time are given in this matrix that the crystals form.
Chapter 13. Scheltema and Schander (2006) reviewed the strategies
There are significant differences in how chiton shells are involved in shell and spicule formation in different groups of
formed compared with those of the so-called conchiferan molluscs. Their conclusions are summarised below.
groups prompting Scheltema (1988a) to suggest that their
shells were independently derived, although this is rarely Polyplacophora: The mantle secretes a cuticle in which
accepted (see below). the shell plates and the aragonitic spicules of the gir-
The chiton larva develops first six and then seven dorsal dle and the eight dorsal shell plates are embedded.
transverse ridges made up of cells that secrete cuticle, while Spicules are produced in an invagination of either a
the depressions between the ridges (the plate fields) secrete single cell (the formative cell) or a group of cells (the
the shell plates. The plate fields have cells that develop an cell packet) (Figure 3.15), and the proximal region
enormous flat villus (stragulum) which seals each plate field of the spicule is covered with cuticle (Haas 1981;
from the external environment and creates a crystallisation Scheltema 1993). The shell valves are covered by a
chamber in which a rod-shaped shell plate anlage5 forms thin properiostracum secreted by epidermal cells in
(Figure 3.15). After formation of the rod, accretionary growth a groove at the mantle margin, and shell crystals are
is then initiated at the edges of the rod, producing the tegmen- deposited at the margins and on the ventral surfaces
tum layer of the plate, while the ventral hypostracum layer is of the shell plates.
subsequently added by cells in the central region of the plate Aplacophora: Also have a cuticle covered mantle
field, and the plate is then covered by the organic outer layer, secreted by the epidermis. As in chitons, the spic-
the properiostracum (Kniprath 1980). ules are aragonite, they are secreted extracellularly
Conchiferan larvae usually have the shell-secreting struc- in the invagination of a single cell (Haas 1981;
ture, the shell gland, formed early in development from invag- Okusu 2002) and each has a thin covering of cuticle
inated, thickened ectoderm which subsequently evaginates (Ivanov 1996).
when the larval shell is secreted. The periostracum is secreted Conchifera: Do not have spicules, and the mantle cuti-
at the distal edge of the shell gland and encloses a crystal- cle is secreted as periostracum in a groove on the
lisation chamber (the extrapallial chamber) closed off from mantle edge. Shell growth is by marginal accretion
external influences. The shell gland of gastropods is simple, and internal deposition.
Monoplacophora: Calcium carbonate is deposited
5 A primordium, or part of the embryo that develops into a particular under the periostracum at the shell edges with a one
structure. to one relationship between prisms and mantle cells.
microvilli shell plate stragulum mucoid mucoid

rudiment vesicles layer
microvilli
spine rudiment
microvilli
basal Ca CO3
secreting cell
After hatching
nucleus
cuticle condensed layer
Initial stage of spine formation
organic pellicle calcareous

of spine part of spine
vesicles filled
with organic
material
plate field intersegmental ridge
microvilli After 9 hours
basal Ca CO3
secreting cell cuticle shell plate
epithelial
cells
Growing spine
Development of a large spicule (spine)
on the girdle of Lepidochitona cinerea
(modified from Haas 1981) After 20 hours
Three stages in shell plate formation in Ischnochiton rissoa
(modified from Kniprath 1980)
FIGURE 3.15 Spicule and shell formation in polyplacophorans. The left-hand figures show the development of a spicule. Redrawn and
modified from Haas, W., Malacologia, 21, 403–418, 1981, and the right-hand figures show the formation of shell plates. Modified from
Kniprath, E., Roux. Arch. Dev. Biol., 189, 97–106, 1980.
Further inside, a nacreous layer (foliated aragonite) is fuse to the periostracum (Arnold 1992). Two forms
secreted by the mantle cells under the prismatic layer of crystals occur, proto-prisms and proto-platelets,
(Lemche & Wingstrand 1959; Checa et al. 2009b). which once assembled are incorporated into pris-
No extrapallial cavity has been found. matic and nacreous layers, respectively. TEM6 stud-
Nautilus: The shell is composed of aragonite structures ies by Westermann et al. (2005) on material from
that form within individual mantle cells just dorsal to juvenile and early adolescent individuals showed
the periostracal groove. Based on an SEM study made that the prisms were initially formed in intracellular
on Nautilus embryos, the crystals grow out of the
mantle edge epithelial cells, fuse together, and then 6 Transmission Electron Microscope.
vacuoles and moved through the cell surface to be it forms folds as it leaves the periostracal groove, and these
assembled extracellularly into their final form. To become conspicuous growth lines (Checa 2000). During long
our knowledge, this method of shell formation has inactive periods, layers of inner periostracum are occasionally
not been confirmed in adults. This finding has been added to the interior of the shell. When active shell secre-
largely ignored in the mainstream literature on shell tion occurs, both periostracum and shell are secreted (Checa
formation. 2000). In some marine species living in cold water, the thick
Other Conchifera: In most conchiferans, the shell is periostracum is also composed of layers. It can be structurally
formed in a fluid-filled extrapallial space between modified, with ridges, hairs, etc. and in some bivalves, and a
the epithelium of the mantle fold and the periostra- few gastropods, it is calcified. Chitons lack a true periostra-
cum (see Section 3.2.6.1). Crystals form extracellu- cum although a cuticular organic layer (the properiostracum)
larly in an organic matrix. is present (see Section 3.2.6).
In a departure from the situation in most conchiferans,
In the following sections, we deal firstly with the organic the unionid bivalve Amblema has outer and middle periostra-
components of the shell and then describe the formation and cum layers secreted by the periostracal groove and nucleation
microstructure of the calcium carbonate component. occurs within the middle layer of the periostracum (Checa
2000). This situation has not been reported in other bivalves,
3.2.6.1 Periostracum including other unionids, except for a somewhat similar vacu-
The periostracum is an organic cuticle-like layer on the out- olated middle periostracal layer in a mytilid (Harper 1997b,
side of the shell (the ‘ostracum’) that is usually yellow to dark figure 4a).
brown. It is composed of conchiolin consisting of highly
cross-linked quinone-tanned proteins. The periostracum 3.2.6.2 T he Role of Other Organic
forms a seal at the edges of the shell which isolates the extra- Compounds in Shell Formation
pallial space from the external environment, and in that space Despite the organic matrix comprising a minor (less than 5%)
calcification of the shell occurs, using an organic matrix as a part of the shell, it controls many processes involved in shell
framework (see next Section). formation. This organic material acts as a framework on which
The periostracum of conchiferans is secreted in the calcium carbonate7 is deposited, and some of the acidic pro-
periostracal groove in the mantle edge in the form of the teins are included within the crystal as it grows. This matrix is
soluble protein polymer periostracin which then quickly involved in the synthesis of amorphous minerals from which
becomes insoluble via a tanning process involving quinone the crystals form (Marin et al. 2012), and it acts as a point of
(Marin & Luquet 2004). It is usually composed entirely of nucleation of the crystals and determines their growth, posi-
protein, but, in a few taxa, it has calcium carbonate embed- tion, and form (e.g., Wilt et al. 2003; Marin & Luquet 2005;
ded in it. Jackson et al. 2010; Marin et al. 2012). This organic matrix
The periostracum may be smooth or rough and thick and includes the inner surface of the periostracum from where the
obvious, or it can be barely visible, very thin, and smooth and outer layer of calcium carbonate crystals is suspended.
often eroded away. Some species have regular sculpture or The shell matrix proteins increase the resistance of the
hairs that may be complex and are often species-specific in shell to fractures by several orders of magnitude (Marie
pattern. Periostracal hairs have often arisen in mollusc evo- et al. 2013). They play a crucial role in determining the type
lution and presumably provide adaptive advantages to taxa of CaCO3 polymorph, as well as crystal nucleation and their
that possess them (Pfenninger et al. 2005). In species with growth and form. The complex organisation of shell matrix
a heavy, opaque periostracum it obscures the shell beneath proteins is only reasonably well understood in simple shell
so any colour pattern is hidden, as in some species of Conus. structures – notably nacre.
While the periostracum may be flexible in life, once it has Organic compounds secreted into the extrapallial space by
dried out on an empty shell, it can become brittle and flake the mantle epithelium include proteins, chitin and other poly-
off. In species where a polished shell surface is secreted by saccharides, glycoproteins, and proteoglycans that make up
the mantle extending over the outer shell surface, as in cow- the organic shell matrix (e.g., Marin & Luquet 2004, 2005).
ries, the periostracum is absent. Of the many proteins expressed during shell formation, some
The periostracum can assist in slowing or preventing function as enzymes and others in cell signalling (Marin et al.
shell erosion, notably in fresh-water bivalves and gastropods 2012). Some are soluble and others insoluble, the latter appar-
and, in some bivalves at least, such as some marine mussels ently involved in the control of crystallisation (e.g., Belcher
(Mytilus), it has been shown to assist in reducing biofouling et al. 1996; Marin et al. 2012). The soluble proteins in the shell
(see Scardino et al. 2003). matrix inhibit crystallisation until they attach to a suitable
The periostracum usually consists of a single layer, but the
thick periostracum of fresh-water mussels (Unionidae) con-
sists of two layers. The outer layer is secreted in the periostra-
7 All mollusc shells are composed of calcium carbonate except for one
cal groove as in other bivalves, and the inner layer is secreted
questionable record of a phosphatic putative mollusc, the Silurian

by the outer mantle fold epithelium. When shell growth ceases Cobcrephora that was suggested to be a relative of chitons (e.g., Bischoff
or slows, the outer periostracum continues to be secreted so 1981; Cherns 2004) (see Chapter 13).
insoluble part of the matrix where they act as nucleation The most studied shell structure is nacre and, more specifi-
points in crystal formation (Marin & Luquet 2004). cally, the nacre formed in pteriomorphian bivalves. According
Interestingly, for shell crystals to form, the organic to Addadi et al. (2006), the first step involves the assembly of
matrix needs to be acidic. In contrast, the organic matrix the organic matrix in which a chitinous framework is filled
in the non-mineralised gladius of coleoid squid is basic with an organic ‘hydrophobic silk’ gel so it occupies the space
(Dauphin 1996). in which the nacre crystal will be formed. The orientation and
Until recently the control of the formation of shell crys- shape of the crystal are determined by the framework, and an
tals was thought to be through just two mechanisms, crys- amorphous colloidal calcium carbonate replaces the silk gel.
tal nucleation and growth inhibition, but the processes This is followed by nucleation on the organic matrix and the
involved are much more complex and under hormonal con- commencement of crystal growth utilising some of the acidic
trol. They include interactions between proteins and minerals, proteins included in the crystal.
protein-protein interactions and interactions with epithe- Three main groups of proteins have been identified in the
lial cells. Some proteins act as enzymes and others may be organic constituents of bivalve nacre (Addadi et al. 2006).
involved in cell signalling (Marin et al. 2012). In Lottia, for These are:
example, there are both highly conserved and unique proteins,
including enzymes such as peroxidases, carbonic anhydrases Chitin: Chitin is insoluble and is in the β-form which
and chitinases, acidic calcium-binding proteins, and protease has parallel chains that extend well beyond indi-
inhibitors (Marie et al. 2013), and this is probably similar in vidual mantle cells. These chitin fibres lie under
other molluscs. In the pearl oyster Pinctada fucata, there are individual nacre crystal tablets. The role of chitin
at least 30 kinds of shell matrix proteins, only three of which in the shell framework appears to vary considerably
are shared with gastropods (Miyamoto et al. 2013). In addi- as some molluscs have several genes involved in the
tion, the genes responsible for expressing the proteins are formation of the chitin matrix and others have only
differentially expressed in the larvae, juveniles, and adults, one (Jackson et al. 2010).
presumably in response to the different environments these Acidic proteins: Acidic proteins are highly diverse and
stages experience (Jackson et al. 2007). There are also dif- are involved in crystal nucleation. They are rich in
ferences in some shell proteins, even between closely related acidic amino acids like aspartic and glutamic acid
species. For example, in the pearl oysters (Pinctada spp.), the (e.g., Tong et al. 2004). Aspartic acid is most abun-
shematrin genes, which express proteins with silk/fibroin-like dant in both calcitic and aragonitic shell layers, while
domains, differ between species, suggesting that they may glutamic acid is usually associated with amorphous
evolve rather rapidly (Jackson et al. 2010; McDougall et al. calcium carbonate (Gotliv et al. 2005).
2013). Within these biomineralisation genes in abalone, only Silk-like proteins: These proteins are similar to
six were similar to those in the patellogastropod Lottia, and arthropod (especially spider) silk and have been
only one was shared between the pearl oyster and the aba- found in the nacre of pteriomorphian bivalves
lone (Jackson et al. 2010). The genes in common are probably such as Atrina (Addadi et al. 2006) and in oysters
ancient and may give clues to mineralisation processes in the (Takahashi et al. 2012). Addadi et al. (2006) pre-
first molluscan shells. The silk fibroin gel protein has only sumed that the silk was a hydrogel before mineral
been identified in nacre, with none known in the superficially formation, and that water is removed as the mineral
similar aragonitic or calcitic prismatic layers (Furuhashi et al. forms. The gel probably helps to keep the organic
2009a). sheets separated before crystallisation. Silk fibroin
As described above, the shell microstructural elements are gel protein has not been identified from aragonitic
formed in an organic matrix. Calcium carbonate precipitates or calcitic prismatic layers (Furuhashi et al. 2009b)
on a scaffold of insoluble chitin. In the model proposed by that are superficially similar to nacre and is absent
Suzuki and Nagasawa (2013), the chitin scaffold contains from the nacre of Haliotis (Jackson et al. 2010).
insoluble matrix proteins such as Pif, MSI60, or prisma- Mucin-like proteins: A report of a mucin-like protein in
lin-14, which have a hydrophobic region (enabling interaction the nacreous shell layer of Pinna nobilis was the first
between protein and chitin) and a hydrophilic-acidic region evidence that mucins have a probable role in calcifi-
enabling calcium carbonate-binding. Thus, these proteins cation (Marin et al. 2000).
provide the connection between the organic (scaffolds) and
inorganic (calcium carbonate crystals), form the intercrystal- 3.2.6.3 Shell Secretion at the Mantle Edge
line organic framework, and probably also regulate the nucle- Shell growth occurs at the edge of the shell when calcium
ation and orientation of the crystals. There are also soluble carbonate crystals form in a fluid-filled space between the
matrix proteins (e.g., nacrein, MSP-1, or Asp-rich), which, periostracum and the shell surface, the extrapallial chamber.
like the insoluble proteins, have a hydrophilic region for cal- The extrapallial fluid in the chamber is sealed from the exter-
cium carbonate-binding and are also involved in the regula- nal medium by the periostracum, and ions (mainly calcium)
tion, formation, and growth of the crystals, and some form the are accumulated by the work of epithelial ion pumps. The cal-
intracrystalline organic matrices. The extracellular organic cium is stored in tissues as granules, mobilised as required
matrix is secreted by mantle cells. and pumped (as ions) into the extrapallial space.
HAEMOLYMPH MANTLE EPITHELIUM EXTRAPALLIAL SHELL

metabolites
FLUID
CO2 passive diffusion
CO2
CO2
CA CA
A- or HCO3- A- or HCO3-
AT
CA
H+
HCO3-
ATP AT +
ADP Ca2 + HCO3-
CaCO3
+ via paracellular pathway +

Ca2 Ca2
A- Any exchanged anion ATP Adenosine triphosphate

ADP Adenosine diphosphate CA Plasma membrane-bonded
AT Active transport in plasma membrane of mantle cells carbonic anhydrase
FIGURE 3.16 A postulated metabolism of inorganic shell formation. Redrawn and modified from Wheeler, A.P., Mechanisms of mollus-
can shell formation, pp. 179–216, in E. Bonucci, Calcification in Biological Systems, CRC Press, Boca Raton, FL, 1992.
Crystallisation is possible because the pH of the extrapal- taxa. Regarding sites of calcium ion uptake, the respective
lial fluid is raised by ammonium ions, providing the con- roles of the mantle and gills are not known. Calcium ions are
ditions for calcium carbonate to be deposited, as in other transported from the haemolymph to the extrapallial cavity,
biomineralisation processes involving carbonates (Loest presumably involving active transport (Weiner & Addadi
1979b). Even so, the process is complex, with one possible 2011).
scenario illustrated in Figure 3.16. Different possible path- Shell formation requires complex genetic machinery involv-
ways of the movement of ions via epithelial cells to the ing a number of genes and transcription factors, and there is
extrapallial fluid have been proposed and four are illustrated also evidence for expansion of gene families being related to
below (Figure 3.17). mechanisms of shell formation (Takeuchi et al. 2016). On the
The mineral in mollusc shells is most often aragonite, whole, the transcription factors and signalling genes are con-
although layers of aragonite and calcite, and sometimes cal- served, but the expressed proteins are derived and can evolve
cite alone, can be formed, but the factors involved in the pro- rapidly (Jackson et al. 2007). The function of some genes is
duction of types of crystalline calcium carbonate in different known. Examples are Hox1 and Hox4 which control the onset
layers of the shell are still not well known. of shell mineralisation in gastropods, engrailed which defines
Uptake of calcium is essential for shell formation. In sea- the edge of the shell field, and Dpp and nodal which control
water, there is no diffusion gradient against calcium uptake shell shape (Hinman et al. 2003; Iijima et al. 2008; Grande &
because the concentration of Ca2+ in seawater and in the hae- Patel 2009; Samadi & Steiner 2009).
molymph of a marine mollusc is about 10 mM8 (Deaton 2008).
In contrast, in the haemolymph of fresh-water molluscs the 3.2.6.4 Addition of Shell to the Interior of
concentrations of calcium range from 3.2 to 8.5 mM, much the Shell by the Dorsal Mantle
higher than in the fresh-water medium (0.1–1.0 mM) (Deaton
Most of the studies on shell formation have focused on
2008). Thus, calcium must be actively transported from the
the processes occurring at the mantle edge, but the addition
water against this large concentration gradient in fresh-water
of material to the inner layers of the shell by the dorsal mantle
is less investigated, except in relation to pearl formation (see
8 millimoles. Section 3.2.6.6) and shell repair (see Section 3.2.6.5). Detailed
H+
extrapallial fluid
Ca2 /Na+
exchange
Ca2 /H+
+ exosomes
pump
+
+
CaCO3
deposit
H+
paracellular route
endoplasmic
reticulum
Calcium binding
H2CO3- HCO3-
HCO3-
septate junction vesicle with

amorphous haemolymph calcium ions
CaCO3
Electrophysiology Vesicular route Facilitated diffusion Calcium cell
FIGURE 3.17 Four possible systems involving the movement of ions at sites of shell formation. Electrophysiology option involves an
increase in acidity that facilitates movement of calcium ions from the haemolymph to the extrapallial fluid. Redrawn and modified from
Simkiss, K., Developing perspectives on molluscan shells, Part 2: Cellular aspects, in Saleuddin, S. and Mukai, S., Physiology of Molluscs,
Vol.1, Apple Academic Press and CRC Press, Palm Bay, FL, pp. 43–76, 2017.
comparative investigations of the mechanisms involved would snail Cornu aspersum. Fernandez et al. (2016) made holes in
be of interest because the shell-secreting dorsal mantle differs the last whorl of the shell of C. aspersum and these wounds
histologically from the cells on the shell-secreting mantle edge. were treated three ways: left uncovered, covered with an inert
material, and covered with chicken eggshell membrane with
3.2.6.5 Shell Repair its foreign organic matrix. The initial shell repairs in the
Repair of cracked or broken shells is accomplished by deposi- presence of the eggshell membrane were calcitic as found in
tion of new shell material in the damaged area. The nature of eggshells, but after 24 hours the snail mantle cells were pro-
the repair and how quickly it is carried out differs depending ducing their own organic matrix, and the shell repair mate-
on the taxon and the location of the damaged part of the shell, rial was aragonitic. While the repaired shell layers may be
although it is generally carried out more quickly in terrestrial the same as in the original shell, in many taxa the shell struc-
taxa. Much of the information below is from the comprehen- ture of the repair differs markedly, these differences probably
sive review of Watabe (1983). resulting from trauma to the organic matrix (see Watabe 1983
Repairs to the shell edge are usually composed of mate- for details). Of special interest are vaterite crystals, along with
rial similar in structure to the rest of the shell, although in calcite and/or aragonite, in the repaired shell. This form of
some, like the fresh-water planorbid snail Helisoma, the outer calcium carbonate is only very rarely present in normal shells.
surface of the repaired area lacks periostracum (Wong & The mineral composition of the repaired parts of the shell can
Saleuddin 1972). Such repairs involve little or no change in also be influenced by temperature (Watabe 1983).
the mantle, and the repairs have the same structural strength Increases in the number of amoebocytes are usually asso-
as those of normal shell (e.g., Blundon & Vermeij 1983). ciated with damage, and calcium is removed from storage for
When repairs occur away from the edge of the shell (i.e., the shell repair, mainly from calcium cells in connective tis-
away from the mantle edge), the shell structure and compo- sue and the mantle. Such changes and responses to damage
sition of the organic matrix is often markedly different and are mediated by hormones, including neurohormones (see
also involves changes to the mantle epithelium (Watabe 1983). Watabe 1983 and Chapter 2).
Shell repairs commence with the formation of organic mem- Shell repairs are usually readily observed as scars on
branes followed by calcification. The relationship between the shell surface. Such scars on recent and fossil shells have
changes in the organic matrix and resultant shell structure has often been used as an indicator of predation frequency and
been experimentally demonstrated in shell repair in the land failure (e.g., Vermeij et al. 1981; Skovsted et al. 2007), and
mantle cavity
pearl sac
mantle pearl
foreign extrapallial
fluid
body
nacre
layer
shell
outer shell
layer
periostracum
Structure of natural pearl Structure of cultured pearl
FIGURE 3.18 Diagram showing pearl formation in a bivalve and the comparison of the internal structure of a natural and a cultured pearl.
Modified from various sources.
Snegin et al. (2016) have used shell repair frequencies of land ‘seeds’ used that form the core of the pearl (see Chapter 10).
snails to estimate changes in ungulate (hoofed mammals) See Landman et al. (2001) for further discussion of the natural
populations on Holocene steppe ecosystems. history of pearls.
3.2.6.6 Pearl Formation

3.2.7 Shell Microstructure
A natural pearl is formed as a response to a foreign object,
often a parasite, lodged between the mantle and the shell. Shell material is laid down as crystals of calcium carbonate.
This may also occasionally be an inorganic irritant (e.g., a It can be either in the form of calcite or aragonite or, very
sand grain), but usually pearl formation is stimulated by an rarely, vaterite9 (Spann et al. 2010). The other three poly-
organic object. The mantle secretes numerous layers of thin morphs of calcium carbonate (protodolomite, monohydro-
shell to cover the invasive object. More broadly, this can calcite, and ikaite) are unknown in molluscs (Marin et al.
be viewed as part of the immune response of the mollusc 2012).
(see Chapter 2). There have been many investigations on the crystallo-
Natural pearls can be formed not only in a wide variety graphic features of the shell layers and their physical and
of bivalves, but also in gastropods, notably abalone. They are chemical properties. Such data on shell microstructure are
covered with the same shell material that forms the inner side obtained by a variety of methods, including scanning electron
of the shell, whether it is nacre or not. In some pearls, the microscopy, and analytical methods including microanalysis,
inner layers may differ from the outer layers, depending on X-ray diffraction, electron diffraction, and infrared spectros-
the maturity of the mantle tissue. In pearl oysters, juvenile copy (Paula & Silveira 2009).
mantle tissue secretes columnar aragonite while the mature There may be several different crystalline structures in
mantle tissue secretes nacre. The pearl is formed in a pearl sac a shell. In addition, the shell structure at the point of muscle
budded off from the mantle (Figure 3.18). Many natural pearls attachments differs from the remainder of the shell and is called
are uneven in shape, with spherical pearls from nacreous
bivalves, notably pteriids, being the most prized. Some form 9
Vaterite is also often found in repaired parts of the shell (see
‘blisters’ on the inner shell surface. Cultured pearls are pro- Section 3.2.6.5) and in egg capsules of ampullariids and some nudibranch
duced by much the same process as natural ones with various spicules (Watabe 1983).
periostracum
outer prismatic layer
nacre
myostracum
adductor
muscle scar
inner prismatic layer

Mytilus - an example of
a pteriomorphian bivalve
nacre
pallial line
prismatic layer
fibrillar layer
foliated layer
ligament
myostracum
crossed-lamellar
layer
shell
muscle scar
A generalised
patellogastropod
FIGURE 3.19 Shell structure of a mytilid bivalve. Redrawn and modified from Lowenstam, H.A. & Weiner, S., Mollusca, pp. 88–110, in
H. A. Lowenstam & Weiner, S., On Biomineralization, Oxford University Press, New York, 1989, Weymouth, F.W., State of California Fish
and Game Commission Fish Bulletin, 1–114, 1921, and a patellogastropod redrawn and modified from Lindberg, D.R., Heterochrony in gas-
tropods, a neontological view, pp. 197–216, in M. L. McKinney, Stehli, F. G. & Jones, D. S., Heterochrony in Evolution: A Multidisciplinary
Approach. Topics in Geobiology, Plenum Publishing Corporation, New York, 1988a.
the myostracum. As the shell grows the muscle attachment structure are recognised. These shell structural types can be
areas advance while the retreating portion of the myostracum subdivided into subtypes resulting in a complex terminology
is covered by the inner shell layer(s), so is retained as a distinct (see Watabe 1988, table 3.1). The formation of these different
layer within the shell (Figure 3.19). The myostracum is ara- shell microstructures is under tight biological control.
gonitic and prismatic. CaCO3 spherulites have been reported The main types of molluscan shell microstructure are
from the myostracal layer of Patella vulgata (Wu et al. 2017). illustrated in Figure 3.20 as follows10:
Diverse shell structures are seen in many bivalves (Taylor
et al. 1969; Taylor 1973; Carter & Clark 1985; Watabe 1988; Prismatic: Uniformly orientated columnar prisms of cal-
Carter 1990a) and lower gastropods (e.g., MacClintock 1967; cite or aragonite encased in an organic sheath, widely
Carter & Clark 1985; Carter 1990a; Hedegaard 1990, 1997; distributed in the Bivalvia, Gastropoda, Scaphopoda,
Bandel & Geldmacher 1996). The reader is referred to these and Polyplacophora. Simple prismatic structures have
reviews and to more general reviews by Paula and Silveira ‘mutually parallel, adjacent structural units (first order
(2009) for more detailed information to supplement the gen-
eral summary below. 10 he shell structure terminology used here generally follows that of Taylor
T
The calcium carbonate crystals making up the shell vary et al. (1969) and Carter and Clark (1985). Alternative molluscan shell struc-
in shape, orientation, and size and several types of crystalline ture taxonomies include Bandel (1990) and Vendrasco and Checa (2015).
FIGURE 3.20 SEM illustrations of types of shell structure. From left to right: Top row - homogeneous, aragonitic; simple prismatic,
calcitic; foliated, calcitic. Bottom row - crossed lamellar, aragonitic; sheet nacre, aragontic; columnar nacre, aragonitic. (Courtesy of J.
Carter.)
prisms) that do not strongly interdigitate along their Nacre: Thin, horizontal aragonitic plates (tablets) or
mutual boundaries’ (Carter & Clark 1985, p. 52). sheets each separated by a thin organic layer and laid
It resembles a layer of closely packed rods which parallel to the shell surface are the characteristic fea-
have their long axes perpendicular to the shell surface. tures of nacre microstructure. It is present in some
The layer may be thin with almost equidimensional Bivalvia, Gastropoda and Cephalopoda. The plates
prisms or thicker with elongated prisms, as found in may be overlapping (sheet nacre) or stacked (colum-
some neritimorph gastropods (Hedegaard 1996). nar nacre). Checa et al. (2009a) distinguished sheet
Several subtypes of prismatic microstructure are nacre from columnar nacre and proposed the term
recognised (Carter & Clark 1985). Waller (1990) foliated aragonite for sheet nacre. Sheet nacre occurs
suggested that this shell structure may not be derived in both monoplacophorans and some bivalves;
from a prismato-nacreous ancestor as often thought, columnar nacre in some bivalves, Vetigastropoda,
but could have originated as a repair mechanism along Cephalopoda, and rarely in monoplacophorans.
the shell margins and may have evolved more than Nacres in different molluscan classes were
once. thought to be homologous as they shared similarity in
This shell microstructure in Pteriomorphia is composition (aragonite), position (inner shell layers),
calcitic, while in heteroconch bivalves it is arago- and appearance (iridescence), as well as their occur-
nitic (Waller 1990). The plesiomorphic state for the rence in putative ‘primitive’ taxa, but these proper-
molluscan outer shell layer appears to be an arago- ties are also shared with some other shell structures.
nitic, prismatic structure (Runnegar & Pojeta 1985). Most shell structures are composed of aragonite;
This shell structure overlies inner nacre, crossed cone complex crossed lamellar structure is also
lamellar, and foliated structures across the Mollusca restricted to the interior of shells, and calcitic foli-
(see Taylor 1973). ated structures are also iridescent. The distribution
Hyolitha cephalopods, but present in some pteriomorphian

bivalves such as oysters and scallops, and in some
patellogastropods and the Paleozoic Platyceratidae.
Brachiopoda Composed of calcite tile-like crystals arranged par-
allel to one another, the crystal structure resembles
the tiles on a roof. There is less organic matrix than
Polyplacophora in nacre. Waller (1976) suggested that foliated micro-
structure was derived from the calcitic prismatic
layer, based on the observations that both layers
share the same mineralogy and that the foliated layer

Aplacophora
always developed below a prismatic layer (although
in many groups the prismatic layer appears to have
been secondarily lost). Carter (1990b) accepted the
Monoplacophora hypothesis of Waller, but cautioned that, depend-
ing on the group, foliated microstructure could have
developed either directly or indirectly through inter-
Bivalvia mediate fibrous prismatic, spherulitic prismatic, or
homogeneous shell microstructures.
Crossed lamellar: This is the most common shell
structure found in polyplacophorans and conchif-
Gastropoda erans other than cephalopods. The earliest mol-
crossed luscan shell structures are all crossed lamellar
lamellar
derivatives. This shell structure is nearly always
prismatic
aragonitic, although rare calcitic examples have
foliate Scaphopoda been recognised. Two main types are present:
simple and complex. Both types are similar, with
nacreous elongate crystals running in layers at angles to
Types of shell each other. This shell structure has a little organic
structure Cephalopoda material (Dauphin & Denis 2000), including more
chitin than in other shell structures (Furuhashi
FIGURE 3.21 A diagrammatic representation of the distribu- et al. 2009a). Crossed lamellar structures may
tion of the main types of shell microstructure in molluscan classes. have preceded the divergence of the extinct
The occurrences of nacre are probably homoplastic. The tree Hyolitha (see Chapter 13) and Mollusca (assuming
includes the Hyolitha and Brachiopoda as outgroups. Original.
Hyolitha are monophyletic and not molluscs) in
the late Precambrian or early Cambrian (570 mya).
of gastropod, cephalopod, monoplacophoran, and Crossed lamellar shell structure is resistant to
bivalve nacres on the tree in Figure 3.21 suggests breakage (e.g., Hou et al. 2004) as ‘crack energy’
that they are probably separately derived, and thus is absorbed because fractures are forced to take a
non-homologous. convoluted pathway through the criss-cross micro-
Nacre properties are presented in Table 3.3, and structure (Currey & Kohn 1976).
although they differ between the major molluscan Aragonitic commarginal crossed lamellar
subclades, there appears to be little variation within structure occurs in many gastropods and bivalves
these groups in the taxa examined. While none of (Bøggild 1930; Taylor et al. 1969, 1973). It is almost
the individual properties differentiates between ubiquitous in Patellogastropoda and Fissurellidae
subclade nacres, unique combinations of these (Bøggild 1930; MacClintock 1967; Hedegaard
characters clearly distinguish bivalve, cephalopod, 1990). Aragonitic radial crossed lamellar structure
and gastropod nacre and the nacre-like structure in is less common than commarginal. It is common in
monoplacophorans. These findings are supported by Lottiidae (Patellogastropoda) (MacClintock 1967;
Jackson et al. (2010, p. 605) who noted that the nacre- Hedegaard 1990), rare in neritimorphs, but absent in
like shell structure of bivalves and gastropods differs Fissurellidae (Hedegaard 1990).
in its crystallographic properties, indicating that the Wilmot et al. (1992) demonstrated that crystals
‘molecular mechanisms that guide the deposition of in aragonitic crossed lamellar structures with dif-
the variants of nacre and its derivatives across the ferent orientation relative to the shell are elongated
Mollusca are fundamentally different’. in different crystallographic directions. Based on
Foliate: Foliate structures are sheet-like crystals simi- only three observations, they concluded that crossed
lar to nacre, but are calcitic. This microstructure lamellar structures have been derived several times.
is absent in polyplacophorans, scaphopods, and While elongation in different directions may be an
TABLE 3.3
A Summary of the Properties of the Different Nacres in Four Molluscan Classes
Character Sources Monoplacophora Bivalvia Gastropoda Cephalopoda
Crystal axis toward the 1 C-axis C-axis C-axis C-axis
interior of shell
Axes in tablet plane 1 Aligned Aligned Unaligned Aligned
Twinning 1 Weak/absent Absent – Prominent
No. of crystals in tablet 1,5,6 1 1 1–20 3
‘Pores’ 2,3 Absent Sparse Abundant Abundant

‘Pore’ shape 2,3 – Small, round Small, round Large, oval
Radial membranes 2,3 Present Absent Present Present
Central accumulation 2,3 – Absent Present Present
Chitin 3,7 Absent Absent or present Present Present
Main AA 8 – Gly, Asx, Ala, Arg, Glx Gly, Asx, Ala, Ser Gly, Asx, Ala, Glx
CA activity 8 – Yes No No
Nucleation site 1,5 Edge of lower tablet Edge of lower tablet Centre of lower tablet Centre of lower tablet
Growth zone 1,5 Entire surface Entire surface Margin Margin
Texture 1,2,3 Fibre Double twin Fiber Double twin
Texture strength 1,2,3 – 49–>9999 (10) 88–90 (2) 51–333 (2)
% twinning 1,2,3 – 12–67 (11) – 50–92 (2)
Angle between a-axis and 1,2,3 – 90–95 (9) – 75–100 (2)
growth direction
Sources of Information: 1 – Hedegaard, C. and Wenk, H.R., J. Molluscan Stud., 64, 133–136, 1998; Chateigner, D. et al., J. Struct. Geol., 22, 1723–1735,
2000; Chateigner, D. et al., Mater. Sci. Eng., 528, 37–51, 2010, 2 – Grégoire, C. et al., Annales de l’Institut océanographique, 31, 1–36, 1955; Iwata,
K., J. Fac. Sci., 17, 173–229, 1975, 3 – Meenakshi, V.R. et al., Ultrastructure, histochemistry and amino acid composition of the shell of Neopilina:
Scientific results of the Southeast Pacific Expedition. II, pp. 1–12, in E. Chin, Scientific Research of the Southeast Pacific Expedition (A. Bruun
Report), Vol. 2, Texas A & M University, Galveston, TX, 1970, 4 – Mutvei, H., Zool. Scr., 7, 287–296, 1978, 5 – Mutvei, H., The nacreous layer in
molluscan shells, pp. 49–56, in M. Ōmori & Watabe, N., The Mechanisms of Biomineralization in Animals and Plants. Proceedings of the 3rd
International Biomineralization Symposium Ago-chō, Japan 1977, Tokai University Press, Tokyo, Japan, 1980, 6 – Kulicki, C. and Doguzhaeva, L.A.,
Acta Palaeontol. Pol., 39, 17–44, 1994, 7 – Machado, J. et al., J. Comp. Physiol. B, 161, 413–418, 1991, 8 – Marie, B. et al., ChemBioChem, 10,
1495–1506, 2009; Data compiled by C. Hedegaard and DRL.
Note: AA = Amino acid; CA = Carbonic Anhydrase activity. Number of taxa observed are given in paraentheses for the last three characters.
inherent property of crossed lamellar structures, it fissurellids (Hedegaard 1990). It is also found in some
is not necessarily an indication of independent ori- autobranch bivalves.
gins. Chateigner et al. (2000, 2010) described dif- Irregular complex crossed lamellar: This type of
ferent textures (crystallographic orientations) in crossed lamellar structure has the first order lamel-
crossed lamellar structures from numerous taxa, and lae comprised of ‘irregularly shaped, interpenetrat-
even from within a single taxon. Belda et al. (1993) ing aggregations of parallel second order structural
reported some deterioration of crossed lamellar shell units’ (Carter & Clark 1985, p. 62). It is found in some
structures in Tridacna related to the availability patellogastropods, the lepetelloidean Osteopeltidae,
of increased nutrients. These findings suggest the in most neritimorphs (Hedegaard 1990), and in arcid
morphology of crystallites in crossed lamellar shell bivalves (Carter & Clark 1985).
structures can be heterogeneous and may be subject Helical: First reported by Bé et al. (1972) in the shell
to some environmental modification. of the pteropod Cuvierina columnella, this micro-
Cone complex crossed lamellar: Prismatic first order structure was found in other pteropods including
lamellae are composed of second order lamellae which the Miocene Vaginella, and living Diacria and
resemble closely spaced, regular stacks of cones, Cavolinia (Bandel 1990). Bandel (1977) suggested
all with their apices pointing toward the exterior of that helical structures were derived from crossed
the shell (MacClintock 1967; Carter & Clark 1985; acicular structures, which are similar to crossed
Lindberg & Hedegaard 1996). In the traditional sense lamellar structure, and reported dendritic to heli-
of Carter and Clark (1985) and in the expanded sense cal structure transitions in secondary shell deposi-
of Lindberg and Hedegaard (1996), this shell struc- tion associated with repair in the shells of species
ture occurs in the patellogastropods (MacClintock of the pteropod Cavolinia. The properties of heli-
1967), cocculinids, most neritimorphs, and in cal shell microstructure enable the construction of
a thin, light shell with resilience to impact (Daraio repeated by Waller (1998), noted that cone crossed lamellar
et al. 2006; Zhang et al. 2011), ideal for organisms and nacre structures were both present in these earliest puta-
that live in the water column. Bandel (1990) found tive molluscs, and thus it was not possible to determine which
helical structures among crossed lamellar layers one was closer to the ancestral state. This view was also sup-
in the varices of the neogastropod Murex. These ported by Kouchinsky (2000), who considered it likely that
varices strengthen the shell, giving it greater resis- nacre and crossed lamellar shell structures evolved indepen-
tance to crushing forces (Vermeij 1978, 1979; Paul dently from the plesiomorphic aragonitic lamellar structure in
1981). different molluscan taxa, see also Vendrasco et al. (2011) for
Homogeneous: An aragonitic or calcitic structure a similar conclusion.
that shows a homogeneous structural pattern. Such The idea that nacre is plesiomorphic is not supported by
shell structures are seen in various gastropods and the distribution of nacre within molluscs (see Figure 3.21),
bivalves. The term ‘homogeneous’ shell structure is notably with crossed lamellar structures being present
unfortunate, as it implies that there is no discernible in Polyplacophora, and in the extinct, shelled outgroup
substructure, although it still retains an arrangement Hyolitha, and others. Crossed lamellar layers are also pres-
of the crystallographic axes. The term is used for ent in all conchiferan taxa except for Monoplacophora and
‘aggregations of more or less equidimensional, irreg- Cephalopoda. Nacreous structures are present primarily
ularly shaped crystallites lacking clear first order in non-heterodont bivalves (Protobranchia, Pteriomorphia,
structural arrangement except for possible accre- Unionida), whereas heterodonts primarily have crossed
tion banding’ (Carter & Clark 1985, p. 63). Thus, lamellar shells except for some Anomalodesmata (see
when a shell structure has no identifiable elements Chapter 15, Figure 15.4). In gastropods, nacre is absent in
other than minute granules, it is called homoge- patellogastropods and is only present in some vetigastropod
neous although homogeneous layers may show some taxa (see Chapter 18, Figure 18.6).
organisation, as with the accretion banding of Carter Regrettably the reports of nacre in older fossils are sparse,
and Clark (1985). It may also enclose sections of a but there are no demonstrated differences between Paleozoic,
more distinct structure, where the granules of the Mesozoic, and Recent nacres (Bøggild 1930; Grégoire 1966;
homogeneous structure are arranged into the pattern Mutvei 1967; Erben et al. 1969; Taylor et al. 1969, 1973; Batten
of a well-defined structure. The term ‘relics of…’ 1972; Mutvei 1983; Dullo & Bandel 1988; Carter 1990a).
has been used by Lindberg & Hedegaard (1996) to In general, the strength of a shell is determined by the
describe the structure of those sections embedded in mechanical properties of the shell structure and its shape and
the homogeneous layer. thickness. Currey (1990) provided an excellent summary of
the mechanical properties of shell microstructures so we need
Only bivalve and gastropod shell microstructures are particu- not dwell on the details here. Shells built with nacre are stron-
larly diverse and well-studied. The shell structures in some ger than those having other shell structures (Currey 1988,
groups of gastropods and bivalves have been extensively used 1990), with foliated and homogeneous structure being the
as systematic characters. The high diversity of shell structures weakest. Crossed lamellar structure is also strong and has the
in early gastropods and pteriomorphian bivalves strongly con- advantage that cracks are restricted due to the criss-crossing
trasts with the more derived taxa, where it is predominantly lattice of crystals.
aragonitic crossed lamellar, sometimes covered by a thin, Flexibility is increased by incorporating more organic
outer calcitic homogeneous layer (Carter 1990a). material, as in the shells of the protobranch Solemya, the pteri-
Polyplacophoran shell structure consists of aragonitic pris- omorphian pinnids, and some stylommatophoran land snails.
matic, homogeneous, and crossed lamellar layers (Carter & Shells are more easily broken by tension (pulling apart)
Hall 1990), while in monoplacophorans, the shell consists of than compression. Nacre is generally the strongest shell
an outer calcitic prismatic layer and an inner aragonitic nacre- structure under tension, compression, or when bent, although
ous layer. because of its high organic composition, nacre is energetically
From a historical perspective, inner plesiomorphic crossed expensive to produce, which is another trade-off.
lamellar structures have been replaced by several shell struc-
tures including fibrillar, foliated, and some others which were
3.2.8 Shell Colour, Patterns, and Pigments
all called ‘nacre.’ All these ‘replacement’ shell structures
are most likely derived from the outer spherulitic prismatic Colours and patterns are notable features of many molluscan
structures and seldom co-occur with one another except in shells. Even fossil shells can reveal colour patterns (not the
the Bivalvia. colour) under ultraviolet light (e.g., Krueger 1974) and traces
There is a general belief that nacre is plesiomorphic in mol- of patterns in early Paleozoic fossils show that such patterns
luscs and no alternative hypothesis has seriously challenged were developed early in molluscan evolution (Kobluk &
this traditional view. After examining Cambrian steinkerns Mapes 1989). Shell colours are formed either by pigments
for shell structure impressions Runnegar and Pojeta (1985), or by shell structure, thus falling into two main groups,
schemochromes (structural colours) and biochromes (true In most molluscan shells, the pigmentation is imparted by
pigments) (Fox 1966). Schemochromes include iridescent the mantle edge and is usually found in the outer shell layer,
colours resulting from the interplay of light through very thin although pigments can also occur in the inner layers. Some
layers of calcium carbonate such as in the nacre of shells and shell pigments and their patterns are genetically determined
pearls (Fox 1953, 1983). Some shells have patches of bright (see below), while others are the by-products of metabolism
iridescent colouration caused by interference or diffraction or derived from food, with the latter changing as diet changes.
from modified surface microstructure. Such structural colou- For example, variable striped colour patterns in the intertidal
ration is relatively rare and differs from that of a normal shell trochid Austrocochlea porcata are mainly composed of the
colouration caused by pigments, and it also differs from the pigment uroporphyrin I, the concentration and abundance
iridescent (pearly) appearance of nacre. Examples of such of which is related to available algal food and indirectly to
structural colours are seen in some gastropods including the wave exposure (Creese & Underwood 1976; Underwood &
patellogastropod limpets Patella pellucida (Figure 3.22) and Creese 1976). Such phenotypic changes have also been dem-
Helcion pruinosus which have bright blue streaks or spots. onstrated in several patellogastropods (Lindberg & Pearse
The structural blue colouration (schemochromes) in these two 1990; Sorensen & Lindberg 1991), predatory caenogastropods
patellogastropods appears to have developed convergently. (e.g., Gibbs 1993; Manríquez et al. 2009), and a few other veti-
In H. pruinosus, it is caused by interference or diffraction gastropods. Whether or not these food-derived patterns are
from highly regular microstructure of crystalline aragonite simply a function of metabolic waste disposal (e.g., Comfort
embedded in the transparent outer shell layer (Brink et al. 1951a), such phenotypic changes can also impart a selective
2002). In P. pellucida, the microstructure of calcite lamellae advantage to some individuals by making them more cryp-
underlies a thin, transparent, irregular, lamellar layer. These tic (e.g., Sorensen & Lindberg 1991; Manríquez et al. 2009).
lamellae are underlain by an array of colloidal particles that Crypsis and other mechanisms such as polymorphism, result-
absorb light and thus provide contrast for the vivid blue colour ing in apostatic selection (see below) by reducing visual pre-
(Li et al. 2015b). The blue stripes of P. pellucida are read- dation, may explain the pigmentation colour and/or patterns
ily visible through the water at several meters distance, and in some species, although in many other molluscs the utility,
Li et al. (2015b) speculated that the colouration may indicate if any, of the shell colours and/or patterns, remains unknown.
Batesian mimicry because two species of noxious nudibranchs Bauchau (2001) observed that pigment colours and their pat-
with bright blue warning colours also inhabit the Laminaria terns on shells appear to have no apparent function in many
fronds on which P. pellucida lives. Interestingly, the spectral molluscs, but this is difficult to accept given their complex-
range of the blue colour is within the band of minimal light ity and the assumed metabolic cost of their production. Thus,
absorption in seawater. while the selective advantage of cryptic and polymorphic
Pigments (biochromes) show as the colour of the reflected shell colouration is readily understood, the reasons (if any) for
wavelengths of light they cannot absorb. They may be laid the great diversity of colours and patterns that exist in many
down in the shell, and/or in the periostracum and the organic molluscs remain unknown.
matrix. They may exist as a uniform or graded colour, or of The possible functional or selective utility of colours and
regular or irregular patterns made up of contrasting tones or their patterns is even more enigmatic because many species
colours. possessing them live buried in sediment or their shell colou-
ration is hidden by an opaque periostracum or fouling organ-
isms. Nevertheless, selection for cryptic colour may be
occurring even in burrowing organisms. For example, Savazzi
(1994) noted that the shell colour of some species of Oliva was
correlated with the sediment colour. For these same reasons,
interspecific recognition is an unlikely reason for shell colou-
ration or patterning because of the limited, or lack of, visual
capacity of most molluscs.
Although their reason for existence is often mysterious,
some theories have been proposed to account for the for-
mation of pigmentation patterns. Waddington and Cowe
(1969) proposed a computer model for simulating pigmen-
tation patterns, but did not suggest a definitive physiologi-
cal mechanism to account for the process. A subsequent
computer model by Meinhardt and Klingler (1987) was pro-
posed in the light of a physiological model of Ermentrout
et al. (1986), which involved the control of pigment secret-
FIGURE 3.22 Patella pellucida – East Cornwall, England, on ing cells by neural activity. This was later developed fur-
Laminaria in the intertidal. (Courtesy of Malcolm Storey.) ther by Boettiger et al. (2009). Gong et al. (2012) used this
neural network model to explain the remarkable diversity of 1987), mudflat batillariids Batillaria (Miura et al. 2007)
colour patterns in species of Conus. The evidence for such and Velacumantus (Ewers & Rose 1966), the neritid Clithon
neural networks and neuroendocrine control is not strong, oualaniensis (Grüneberg & Nugaliyadde 1976), some rocky
being based mainly on work done on the planorbid Helisoma shore species of Littorina (e.g., Reimchen 1979; Atkinson &
(Saleuddin & Dillaman 1976; Saleuddin & Kunigelis 1984). Warwick 1983) and Nerita (e.g., Safriel 1969), and a few chi-
In cowries (Cypraeidae), colour patterns are found in most tons (e.g., Rodrigues & Absalão 2005). Some species of fresh-
species. While these appear to be two-dimensional (as in water neritids also exhibit pattern and colour polymorphism
other molluscs), they are actually three-dimensional in struc- (e.g., Clarke 1978; Bunje 2007).
ture due to the shell having been secreted by the overlapping Studies investigating colour polymorphism in shelled
mantle, and visible patterns are often the result of different molluscs have involved a range of approaches including
thicknesses of shell. While the shell patterns are not cryptic inheritance, genetic drift, frequency-dependent and direc-
(Savazzi 1998), the colour and form of the mantle that often tional selection, and biochemistry (e.g., Goodhart 1987a;
covers the shell may be. When this is withdrawn, it exposes Luttikhuizen & Drent 2008) with several concepts invoked
the markedly contrasting, brightly coloured, often patterned to explain the findings including non-adaptive and adaptive
shell which Savazzi (1998) suggested may cause predators effects. Among the latter are crypsis, visual, disruptive and
to confuse them with nudibranchs or other brightly coloured apostatic selection, climatic effects, assortative mating, genetic
noxious animals. drift, area effects, coadaptation, and pseudo-polymorphism
The models that explain how pigment patterns might be (see Goodhart 1987a for review). The latter term was intro-
generated do not explain why they exist. Bauchau (2001) produced by Grüneberg (1980) to cover examples where there
posed that the pigmentation patterns created a heterogeneous were many, often intergrading, colour forms unlikely to have
shell edge which assisted the mantle edge neural network to primarily evolved through visual predation.
regulate the growth of the shell. He proposed that uniformly Colour polymorphism is thought to have a selective
coloured or non-pigmented shells used ‘other substances’ to advantage with visual predators because the predators can-
mark the shell surface. To our knowledge, this hypothesis not develop a search image for all the morphs. While some
remains untested. studies have demonstrated selection related to visual preda-
The colour of many molluscs is probably largely geneti- tion, the colours of some polymorphs are hidden from preda-
cally determined although this has only been demonstrated tors, for example, in some bivalves they are only visible in
in relatively few taxa, examples being some land snails (e.g., the interior of the shell (e.g., Cain 1988a; Luttikhuizen &
Cain & Sheppard 1950; Cook & King 1966; Owen 1969; Drent 2008), and in the past, colour patterns evolved before
Murray & Clarke 1976; Roth & Bogan 1984; Chiba 1999; eyes were sufficiently well-developed to see them (e.g.,
Hayashi & Chiba 2004), some marine snails (e.g., Palmer Kobluk & Mapes 1989). Similarly, some complex and
1984, 1985b; Ekendahl & Johannesson 1997), and some colourful shell patterns are hidden beneath a thick perio-
bivalves (e.g., Adamkewicz & Castagna 1988; Winkler stracum, as noted above. In the tellinid bivalve Macoma
et al. 2001; Evans et al. 2009; Zheng et al. 2013). Where balthica, there are four, apparently genetically determined,
known, colour is usually determined by one to only a few colour morphs that are expressed only in the interior of the
genes (e.g., see Zheng et al. 2013). Change, or lack of it, opaque shell, although in small floating juveniles this can be
in the frequencies of particular colour morphs over time, visible through the shell (Luttikhuizen & Drent 2008).
has been demonstrated in some long-term studies on helicid Several workers have suggested that colour polymorphism
snails (Cowie 1992a; Cowie & Jones 1998; Cook et al. 1999; in rocky shore molluscs, such as patellogastropod limpets, is
Cameron et al. 2013a). Different immune responses in dif- a form of camouflage against predators (Giesel 1970; Hockey
ferent colour morphs have also been demonstrated (Scheil et al. 1987; Byers 1989). Crypsis is particularly important.
et al. 2013). Sorensen and Lindberg (1991) showed that individuals that
Some molluscs exhibit distinct colour polymorphism, but did not match their background were more likely to be taken,
the nature of this phenomenon has been investigated in only suggesting that selective visual predation can maintain dif-
a few species, the most famous being the European land snail ferences in spatial distributions of colour morphs. For some
Cepaea nemoralis (e.g., Jones et al. 1977), but there are also individuals such enhanced crypsis is an obvious selective
numerous other land snail examples (e.g., Comfort 1951b; advantage of colour polymorphisms in heterogeneous envi-
Parkin 1972; Goodhart 1987a), although no comprehensive ronments (e.g., Cain & Sheppard 1950, 1952, 1954; Smith
overviews are available to date. Besides land snails, there are 1975; Jones et al. 1977; Heller 1979; Palmer 1984; Hughes &
many examples with numerous colour morphs among both Mather 1986; Reid 1987; Cain 1988b; Whiteley et al. 1997;
marine and fresh-water molluscs (Clarke 1978). Examples Cook 1998; Johannesson & Ekendahl 2002; Rodrigues &
include the sandy beach bivalves Donax variabilis (Moment Absalão 2005).
1962) and Donacilla cornea (Whiteley et al. 1997), sublit- Usually the nature of the selection on shell colour morphs
toral bivalves such as many pectinids, sandy beach gastro- is a matter of speculation and may not only be a result of visual
pods such as the trochoideans Umbonium (Grüneberg 1980) predation. Non-biological factors may also be important in
and Bankivia (Clarke 1978; Ermentrout et al. 1986), some maintaining polymorphism, including those determined by
of the mangrove-saltmarsh species of Littoraria (e.g., Reid colour. For example, the effect of temperature in some snails
(e.g., Heath 1975; Jones et al. 1977; Etter 1988b; Stine 1989; Polyenes12 include carotenoids. Hedegaard et al. (2006) used
Sokolova & Berger 2000), where dark-shelled morphs heat Resonance Raman microspectrometry to identify polyenes as
more rapidly and thus may have an advantage in cold areas, shell pigments in 13 gastropods, one cephalopod, and four bivalve
while light-coloured shells may be of advantage in warmer taxa, but found there was no clear relationship between colour,
locations (Jones 1973; Stine 1989; Miura et al. 2007) or in pigment, and taxon with, for example, the same colour being due
alpine grasslands (Burla & Gosteli 1993). Similar effects have to a different pigment in different taxa. Although carotenoids
been observed in dark-shelled morphs of Mytilus (Mitton are not uncommon in molluscan tissues (e.g., Goodwin 1972;
1977) and darker shells may offer more protection from UV Vershinin 1996; Matsuno 2001), Comfort (1951a) did not find
radiation (e.g., Heller 1979). Parasites or parasitoids may also these compounds in shells, although they have since been identi-
favor particular morphs, invoking a form of selection (e.g., fied as shell pigments in some taxa. Carotenoids are responsible
Ewers & Rose 1966; McKillup et al. 2000). for the yellow colouration in a species of cowry (Cypraeidae)
Interactions between two sympatric species may result (Hedegaard et al. 2006) and were identified in Strombus shells
in colour divergence through frequency-dependent selection (Dele-Dubois & Merlin 1981). Carotenoids may also be respon-
from visual predation (e.g., Clarke 1962; Allen 1988; Chiba sible for the yellow colour of some pearls (Hedegaard et al.
1999). Sometimes, different sympatric colour forms regarded 2006; Li et al. 2014b) and have been found in shells of pectinids
as morphs of the same species appear to be different taxa and some neogastropods by Barnard and Waal (2006) using
(e.g., Joseph et al. 2014), while allopatric colour forms may Raman spectra, suggesting these pigments may be widespread.
be interpreted as representing genetically and/or morphologi- The striking blue-violet colouration of the pelagic ‘violet snail’
cally distinct forms of the same species (e.g., Nakano et al. Janthina is like that of its prey, the siphonophores Physalia and
2010; Mariottini et al. 2013). Velella. Analysis of the pigment in Velella and Janthina showed
The chemical composition of shell pigments is rather poorly that the carotenoids responsible for the colour differed in some
known with an early study (Comfort 1950, 1951a) showing that respects, suggesting that the gastropod may be chemically alter-
porphyrins11 were present. In lower bivalves, patellogastro- ing the chemical structure (Barnard & Waal 2006). Blue pig-
pods, vetigastropods, and ‘opisthobranchs’, the shell pigments ments are also found in a few other gastropod shells, but these
are acid-soluble, but in many caenogastropods and ‘pulmo- have not been investigated.
nates’ they are not (Comfort 1951a), and the composition of Indoles have a bicyclic structure and are found as pigments
these latter pigments remains elusive. Recent research using in molluscs in two forms, melanins and indigoids. Melanins
Resonance Raman microspectrometry have shown that poly- come in two forms – eumelanin and pheomelanin (Williams
enes, including carotenoids, are common (Barnard & Waal 2017). Melanins have been reported from the shells of
2006; Hedegaard et al. 2006). The summary below largely Lymnaea and Mytilus, but are presumably more widespread;
follows a recent review by Williams (2017). eumelanin is an important component of cephalopod ink
The main shell pigments known are carotenoids, melanin, (Derby 2014) and has also been detected in fossil ink sacs
and tetrapyrroles, including porphyrins and bile pigments. (Glass et al. 2012). Melanins are probably responsible for some
Tetrapyrroles are the main acid-soluble pigments in mol- yellow, red, brown, and black colours. Indigoids are thought
luscan shells. They occur in two main forms – cyclic struc- to be present in some shells, such as Haliotis cracherodii
tures (porphyrins) or linear structures (bilins) and produce (Comfort 1949), but Comfort (1951a) later suggested these
red, orange, green, blue, violet, yellow, or brown colouration supposed indigoids may be pyrroles, and there do not appear
(Fox 1976). Porphyrins are the most common shell pigments. to have been subsequent reports of indigoids in shells.
In these, the pyrrole rings form a ring, with the most common The shells (and often the animals) of many molluscs adopt
being uroporphyrin I and conchoporphyrin. They are prob- the same or similar colouration as their food and/or their
ably derived from chlorophyll obtained via food and can vary substrata, rendering them cryptic. Most of these cases have
depending on the available chlorophyll (e.g., Underwood & not been investigated as to whether the pigments are being
Creese 1976). These compounds produce red, brown, or purple sequestered from the food or whether the colours have a
shell colouration (Williams 2017) and have also been identified genetic basis and are derived de novo. Some are clearly derived
as responsible for the colour of some pearls and pearl-producing from pigments in the food (e.g., Comfort 1951a). For example,
bivalves (see Hedegaard et al. 2006 for references). Haliotis fed on different algal foods change colour, some-
Bilins, where the pyrrole rings form a chain, are much less times dramatically (e.g., Leighton 1961; Tajima et al. 1980).
common than porphyrins and are responsible for blue, green, The shell of Nucella lapillus may be white or grey with a diet
brown, or red colouration (e.g., the green colour in some hali- of barnacles and brown to purple when Mytilus is the main
otids, trochids, and turbinids (Jones & Silver 1979). food, with an abrupt change in colour if the diet is changed
Quinones may be responsible for the non-acid-soluble pig- (Moore 1936). Subsequent work, however, has shown that the
ments in some shells (Comfort 1951a). situation is more complex as the ground colour of the shell in
Nucella (Spight 1976a; Castle & Emery 1981; Palmer 1984)
11 eterocyclic or macrocyclic organic compounds comprised of four pyr-
H
role subunits connected via their carbon atom and methine (+CH–). A group of polyunsaturated conjugated organic compounds that are often
12
This group of compounds includes pigments, one of which is heme–the colored due to their low energy state resulting from multiple carbon to
red in haemoglobin. carbon double and single bonds.
and Haliotis (Liu et al. 2009) has a genetic basis, and this can elements and with an amazing and, sometimes, bizarre
be modified by pigments derived from the food. array of sculpture in ammonoids.
In coiled molluscs that develop elaborate projecting sculp-
ture (many gastropods and ammonoids), as the shell grows
3.2.9 Shell Pores
over the sculptured part of the preceding whorl the pro-
Chiton plates, monoplacophoran shells, and some bivalve truding sculpture is dissolved by the mantle (e.g., Carriker
and gastropod shells are penetrated by minute pores, and the 1972; Signor 1982b), enabling recycling of the calcium.
cellular extensions that enter them are called caeca. Similar Vetigastropods tend to cover any sculpture with a thick glaze
structures occur in some brachiopods, bryozoans, ostra- or have reduced whorl overlap (Vermeij 1973b, 1977b).
cods, and barnacles. They have a patchy distribution within It is usually assumed that shell sculpture is functional.
both gastropods [some fissurellids, some neomphaloideans Some sculpture roughens the surface, increasing the ability
(Sasaki et al. 2010b), neritoideans, a few glacidorbids], and for sediment and fouling biota to lodge and thus facilitat-
some bivalves [some pteriomorphians (all arcoids and limop- ing crypsis. Ribs and spines on shells should logically aid
soids), cyrenoideans, and Chamidae], but most taxa lack them. in deterring predators, but there have been relatively few
In bivalves, the pores are formed by projections from the man- attempts to test this. Experiments with epifaunal bivalves
tle penetrating the formed shell layers (Waller 1980; Reindl & tested the effectiveness of spines against predation by muri-
Haszprunar 1994, 1996a). In most bivalves, they are sparse cids and starfish. Spines deterred predation by muricids, but
and do not penetrate right through the shell or are restricted were not effective against predation by starfish (Stone 1998).
to the juvenile shell (as in Cyrenoidea) (Waller 1998). In the While evidence suggests that spines on bivalves may dis-
Arcoidea, however, they are dense on the inner side of the pal- courage borers (Beatty & Rollins 2002), experiments using
lial line (e.g., Waller 1980). artificial spines on Mytilus found that predation by Nucella
The function of many of the different caeca is uncertain – was not reduced (Willman 2007). Palmer (1977) experimen-
the shell limits the exchange of materials and sensory infor- tally demonstrated the role of the shell varices in the muricid
mation between the organism and its environment, and the Ceratostoma foliatum in providing hydrodynamic destabi-
caeca may assist in such exchange. In chitons, the caeca are lisation and increasing the probability that it lands aperture
called aesthetes and have sensory functions including imag- down if detached from the substratum. In follow-up work,
ing (see Chapter 14), but the cellular extensions that enter Palmer (1979) concluded that shell-crushing fish have been
the pores in gastropods are less modified. The detailed struc- important selective agents in the evolution of molluscan shell
ture of the caeca inside the pores in arcoid (and some other sculpture, especially in the tropics. In addition to antipreda-
Pteriomorphia) bivalves, vetigastropods, chitons, and bra- tion defenses, it has also been suggested that spines have other
chiopods are all very different (Reindl & Haszprunar 1996b), adaptive roles such as providing camouflage or for stabilisa-
and it is unclear as to whether or not they share a common tion on soft substrata. Other adaptive functions for certain
ancestry. sculptural elements include assisting with burrowing, nota-
bly the so-called ratchet sculpture (Signor 1982a) in some
gastropods and bivalves (e.g., Stanley 1981; Signor 1982a,
3.2.10 Shell Ornament and Its Function
1993; Seilacher 1985; Savazzi 1989) and the file-like sculp-
Shells can bear a wide range of ornament ranging from ture seen in the anterior part of the shell in bivalves which
enhanced growth lines to long spines or heavy knobs. While bore using mechanical means (e.g., pholadids and teredinids)
sculpture is usually arranged collabrally,13 which implies (e.g., Seilacher 1985; Savazzi 2005).
some discontinuity in growth, there are also often radial ele- The ‘ratchet sculpture’ is common in shallow-water
ments. In some taxa, the sculptural elements can be mark- bivalve burrowers that live in sand. It has ridges with a
edly divergent, as for example, in the divaricating sculpture of rounded edge toward the direction of burrowing that slip
some bivalves (Seilacher 1972). Sculpture can be continuous through the sediment while a steep face on the opposite side
as in lines, ridges, frills, or discontinuous as in granules, nod- resists backward movement, thus assisting by reducing slip-
ules, or spines. page when the foot is extruded. This type of sculpture is
In extant molluscs with shells, the most elaborate sculp- found in several bivalve families (Vermeij 1993) and some
ture is seen in bivalves and gastropods, while polyplacoph- have a modified version – divaricating sculpture, as seen for
orans either lack sculpture or it is subdued, with ridges and/ example, in the lucinid Divaricella and the tellinid Strigilla.
or granules developed in some taxa. Scaphopods are gener- This consists of oblique ridges with steep dorsal edges; the
ally smooth or have radial sculpture. All extant monopla- anterior ridges are at right angles to the posterior ones, so
cophoran and cephalopod shells lack sculpture. A different they grip the sediment as the shell rotates when burrowing.
picture presents itself with fossil cephalopods, with some Such oblique ridges not only enable efficient burrowing, they
nautiloids and belemnites having developed sculptural also strengthen the valves (Checa & Jiménez-Jiménez 2003).
Some burrowing gastropods also develop spirally arranged
Collabral – shell ornament or growth lines that conform to the growing
13
ratchet sculpture which has the steep side toward the apex,
edge of the shell (the outer lip of the aperture of a gastropod or the shell while in others, the shell is smooth, but there is a protruding
margin in a bivalve). suture (Vermeij 1993).
Sculpture in gastropods is not confined to the outer part of calcareous siphonal pallets in Teredinidae are secreted by the
the shell. The aperture may contain elaborate developments siphonal tissue, but the details are, again, not known.
of teeth, ridges, and other structures (Paul 1991) that are often
thought to serve as barriers to predators or to strengthen the
3.2.13 Agglutination
shell. In the ellobiid Pedipes, it has been suggested these teeth
prevent the foot of the snail from blocking the pneumostome In many shelled molluscs, epizootic organisms growing on
(Örstan 2010). Such internal sculptural elements are absent in the shell provide camouflage and hence protection against
chitons, scaphopods, and extant cephalopods, as well as most predation. In a few bivalve and gastropod taxa, sand grains
bivalves other than some scallops and cockles. and sometimes other objects are agglutinated on the shells.
The most famous examples are some members of the

Xenophoridae which attach dead shells, stones etc. to the
3.2.11 Shell Windows
outer surface of their shells. Other examples are the cerithioi-
Many species of small coiled gastropods have transparent dean gastropod Scaliola (Scaliolidae) and the venerid bivalve
or semitransparent shells, but some of those with an opaque Granicorum which attach sand grains to the exterior of their
shell have a transparent patch in the last part of the last whorl shells. Some land snails attach dirt, leaf fragments, lichens
of the shell behind the aperture. The eyes can be seen through etc. to their shells (e.g., Allgaier 2007).
this part of the shell. We are not aware of any experimen- Objects are typically cemented largely through periostracal
tal studies on coiled gastropods, but a similar situation in a and shell formation at the mantle edge. In some watering pot
patellogastropod limpet was investigated, and it was demon- shells (Clavagellidae), the adventitious shell produced by siph-
strated that it responded to light through translucent patches onal glands has agglutinated sand grains (e.g., Morton 1984).
on the anterior part of the shell which lack further modifica- Multicellular arenophilic glands are found on the mantle mar-
tion (Lindberg et al. 1975; Lindberg & Kellogg 1982). More gins of several other anomalodesmatan bivalves. These secrete
apomorphic ‘shell windows’ are found in a few bivalves with mucoid substances which enable the attachment of sand grains
symbiotic zooxanthellae where the shell structure is modi- and other particles to the periostracum (Sartori et al. 2006).
fied to direct light onto the tissues containing the photosyn-
thesising symbionts. The best known example is the cardiid
3.2.14 Other Shell Structures
Corculum cardissa which has anterior and posterior patches
of the shell forming the ‘shell windows’ that funnel light Special taxon-specific shell structures (e.g., bivalve hinges
through the shell in a way analogous to fibre optics (Watson & and ligament; cephalopod shell chambers) are discussed in
Signor 1986; Seilacher 1990). These ‘windows’ are formed the chapters in Volume 2 dealing with groups possessing
mainly from the outer prismatic shell layer, and their shape these features.
may help to focus light on the zooxanthellae bearing tissues
(Carter & Schneider 1997). Similar, but less developed, win-
3.2.15 Shell Reduction and Loss
dows are also found in some other members of the cardiid
subfamily Fraginae. Adult shell loss in conchiferans occurs only in gastropods
and cephalopods, and although extreme shell reduction has
occurred in a few bivalves (a few galeommatoideans and
3.2.12 Secondary Shell Structures
Teredinidae), complete shell loss in bivalves is unknown.
Adventitious tubes formed by watering pot shells (Clavagel- Examples of adult shell loss are scattered through the gastro-
loidea), ship worms (Teredinidae), and Gastrochaenidae, are pods, and in most groups it is rare. Vetigastropod examples
secreted by glands on the siphon (e.g., Savazzi 1982; Morton include some trochids (e.g., Gena), and some fissurellids. Shell
1984, 2006c; Morton et al. 2011; see Chapter 15 for more loss has occurred in neritimorphs (the slug-like Titiscania) and,
detail). The shell material comprising these tubes is simpler in in caenogastropods, the parasites Entocolax, Entoconcha, and
structure than true shell secreted by the mantle edge. Enteroxenos (Eulimidae) (Lützen 1968). A group of slug-like
In gastropods, Magilus (Muricidae, Coralliophilinae) and caenogastropods, the Velutinidae, have thin internal shells.
vermetids form long tubes secreted by the mantle edge, and No shell loss is known in patellogastropods.
the sole of the foot of hipponicids secretes a basal calcareous In heterobranch gastropods, shell reduction and loss is
plate attached to the substratum (e.g., Knudsen 1991, 1993). typical of many groups (Morton 1963; Gosliner & Ghiselin
In bivalved sacoglossans (the ‘bivalved gastropods’), the mantle 1984; Gosliner 1985, 1991; Tillier 1989) (see Chapter 20).
divides at settlement to produce right and left shell ‘valves’ with For example, there are no extant ‘nudibranch’ taxa with a
the larval shell remaining attached to the left valve (Kawaguti shelled adult, although their sister group, the pleurobranchs,
1959; Grahame 1969). Subdivision of the mantle presumably retain the larval shell and often have a reduced internal shell.
also occurs in the formation of the accessory shell plates in Developmental studies on the shelled pleurobranch Berthella
pholadid bivalves. A plate, the callum, covers the pedal gape show that the mantle fold extends back over the outside of
in mature individuals of the wood-boring pholadid Martesia the larval shell during development, enclosing it (LaForge &
and is presumably secreted by the mantle, although the details Page 2007). In developing nudibranchs, the mantle fold is also
of this process have not been investigated. Similarly, the reflexed and spreads dorsally after metamorphosis, but it does
not enclose the larval shell (see Chapter 20, Figure 20.67), organs of the visceral mass descending into the body cavity.
which is discarded (Thompson 1976). Discarding the larval Experiments with semi-slugs and slugs by Hausdorf (2001)
shell also occurs in onchidiids (Fretter 1943) and vaginulids showed that slugs were more mobile and flexible, better able
(G. Barker, pers. comm. Nov. 2014). to find shelter (by squeezing into tiny crevices) and could
Shell reduction and shell loss are also predominant in the grow more quickly because they lacked a shell. These and
coleoid cephalopods. While there appears to have been no other advantages have led to about ten independent origins of
shell reduction or loss in nautiloids, the external shell has been terrestrial slugs (Pearce & Örstan 2006). In coleoid cephalo-
reduced and internalised in coleoids (belemnoids, cuttlefish, pods, shell reduction and loss are thought to be related to the
octopods, and squid) or completely lost in some octopods, development of rapid jet locomotion using a contractile mus-
although a rudimentary shell may be present in some taxa. cular mantle wall (see Section 3.12.3.8.2), an innovation that
In both gastropods and coleoids, the adult shell is lost, not the would be impossible with an external shell (see Chapter 17).
larval shell, which is still produced in early development and Despite theoretically increasing vulnerability to predation,
then shed at metamorphosis (gastropods) or subsumed by the losing the shell can open opportunities. Besides streamlin-
adult mantle (octopus). ing, which may facilitate both burrowing and swimming, the
In most cases of shell reduction, the shell is first surrounded much-increased area of skin can provide additional respira-
by tissue and then reduced. These internal shells may be much tory surface and is often accompanied by reduction or loss of
reduced and even disappear, but in squid and a few hetero- the mantle cavity. Some shell-less slugs (some nudibranchs
branch gastropods, they are chitinous (Furuhashi et al. 2009a), and acochlidians) have secondarily produced spicules in their
having minimal or no calcareous material. In some taxa, the mantle (notum) (see Chapter 20). Shell loss has led to, or is
shell remains external, but is much reduced in size relative to correlated with, chemical defence in many nudibranchs and
the rest of the animal – as in teredinid and clavagellid bivalves other ‘opisthobranchs’ where it is often associated with warn-
(see Chapter 15), some ‘opisthobranchs’ (see Chapter 20), ter- ing colours (Cimino & Ghiselin 1998, 1999) or by the pro-
restrial ‘semi-slugs’, and Testacella (see Chapter 20). In some duction of defensive mucus as in some terrestrial slugs (see
gastropods, the shell is covered and eventually enclosed and Chapter 20). In a few nudibranch taxa, shell reduction or loss
partly or completely absorbed by either lateral folds of the foot has led to the sequestration of photosynthetic zooxanthellae,
(e.g., naticids or Akera) or the mantle encloses the shell as in or, in many sacoglossans, of plastids (see Chapter 20). Apart
some fissurellids (e.g., Scutus), Cypraeidae and Velutinidae from predation-related disadvantages of shell loss, for terres-
(e.g., Lamellaria), and various shelled ‘opisthobranchs’ trial and intertidal taxa it also results in markedly increased
(e.g., Philine, Pleurobranchus). A similar enclosure of the susceptibility to desiccation.
shell valves by the mantle occurs in some galeommatoidean
bivalves such as Phlyctaenachlamys and Devonia and a few
3.2.16 Growth
chitons such as Cryptochiton. Whether the shell enclosing
tissue is pedal or pallial, the shell becomes reduced and may Most studies on molluscan growth have focused on the shell
eventually be lost in the adult, but the derivation of the new as it is difficult to obtain accurate measurements of body
dorsal integument differs, being either pedal in origin or pallial. size for soft-bodied organisms such as molluscs. One notable
exception is the many growth studies on commercial species
3.2.15.1 Consequences and Opportunities of coleoid cephalopods (squid, cuttlefish, octopus) which has
The advantages of shell reduction or loss include a reduc- also been facilitated by the adoption of standardised measure-
tion in weight and musculature and hence energy savings, ments for the fishery.
and enhancing manoeuvrability and the ability to squeeze
into small spaces. The shell comprises much of the weight 3.2.16.1 Shell Growth and Its Record
of the mollusc, and moving it contributes significantly to Molluscs grow incrementally by adding shell material to the
their energy needs (e.g., Hausdorf 2001). A small increase in edge of their shell, and the shell also thickens as it grows
shell size can markedly increase shell weight. For example, by way of material added to its inner surface. In some taxa,
doubling the size of Nucella lamellosa required three times growth continues through their entire life, this being termed
the energy to carry the shell (Palmer 1992). Shell formation indeterminate growth, while others stop growing at a particu-
also expends considerable energy (Palmer 1992). Shelled lar stage in their life cycle. This determinate growth is obvi-
terrestrial gastropods must contend with greater energy ous in many gastropods where the aperture is thickened or
requirements for shell construction and the low calcium lev- otherwise modified at maturity, in marked contrast to those
els in many soils. Adopting a slug-like body allows the vis- with indeterminate growth with a thin-edged, undifferentiated
ceral mass to be lengthened and flattened and the foot to be aperture throughout their life (Vermeij & Signor 1992).
extended. This process, called ‘limacisation’,14 involves the The elaborations of the last whorl and apertural margin
became possible with determinate growth, characteristics
T his term, derived from the slug genus Limax, is the process of becoming
14 that have evolved from indeterminate growth ancestors in
slug-like. many gastropod lineages. Varix formation has appeared
more than 40 times during gastropod evolution (Webster & (e.g., Ekaratne & Crisp 1984). Resorption of the shell
Vermeij 2017), with varices, or at least a terminal varix-like may complicate growth rate studies using growth lines, as
structure in the adult, occurring in many higher caenogas- found in some unionoideans (e.g., Anthony et al. 2001) (see
tropods (notably tonnoideans, cerithioideans, stromboide- Section 3.2.19).
ans, and neogastropods) as well as some ellobioideans and Shell growth is under hormonal control as discussed
stylommatophorans. Many of the near basal caenogastropod in Chapter 2 and is modified by environmental conditions
cerithioideans, and certain ‘asiphonate’ caenogastropods (temperature, food availability, etc.) and the age of the
(e.g., many Rissoinidae and Rissoidae, some Epitoniidae, a individual. Growth is usually more rapid when young and
few Eulimidae, etc.), also possess apertural varices, indicat- slower later in life, and ceases in those taxa with determi-
ing this feature has evolved independently in several lineages. nate growth. Warm conditions also lead to increasing cal-
The varices are usually thickened externally, but are mainly cification (Graus 1974), and elaborate shell ornamentation
internal in some families (e.g., Potamididae, Strombidae, tends to increase with increasing temperature (Vermeij
Cancellariidae). 1993). Thus, cold water species typically grow in sum-
As the shell grows, many bivalves and gastropods produce mer and little or not in winter. Food supply may influence
sculptural elements at regular intervals which reflect changes not only growth rate, but also shell shape. For example, in
at the mantle margin. Growth lines and some sculpture can the littorinid Littorina littorea, individuals supplied with
be parallel to the growing margin (collabral), producing ample food grew faster and developed low-spired shells
concentric (bivalves) or axial (gastropods) sculpture, or per- with a large aperture, while those with limited food grew
pendicular to it, producing spiral elements. These sculptures more slowly and had higher-spired shells with a smaller
can be continuous (e.g., ribs) or discontinuous (e.g., granules, aperture (Kemp & Bertness 1984), although this result was
spines). reversed (relating to shell shape) in a study on Littorina
Growth proceeds in bursts (known as episodic growth) saxatilis (Saura et al. 2012).
in gastropods with intermittent varices, being very rapid Other ways of studying the environmental record in the
between varices. The periostracum and thin shell are quickly shell involve the analysis of oxygen and carbon isotopes and
formed in the growth spurt and subsequently thickened other elements as outlined below (see Section 3.2.18).
while the apertural varix is being formed. Varices in most
taxa are formed at about the same interval around a whorl,
3.2.17 Internal Septa
and because the gap between each pair of varices regularly
increases, the growth spurts also increase. Episodic growth Internal calcareous partitions that close off the interior of the
also occurs in Siliquaria (Siliquariidae), which is unique shell, termed septa, are also seen in some fossil enigmatic
among gastropods because it periodically increases the width gastropods (see Chapters 13 and 19) and a few modern gas-
of the shell slit and the cross-sectional area of the whorl by tropods including the tube-like vermetids, caecids, the cor-
breaking the sides of the shell into pieces, moving them out- alliophiline Magilus, some turritellids (Andrews 1974), and
ward, and reassembling them (Savazzi 1996). some architectonicids (Bieler 2009). Gastropod and cephalo-
Even on a daily time scale, shell growth is not continu- pod septa are analogues, with those in cephalopods differ-
ous, resulting in ‘growth lines’. This periodic growth not only ing in being more regular and the chambers between them
occurs in very short time scales (e.g., tidally, diurnally), but connected by a siphuncle (see Chapter 17). A similar process
also seasonally. Daily growth is recorded in the shell as to septa formation commonly occurs in many conchiferans
microscopic growth lines and seasonal growth as macroscopic where the shell is sealed as the protoconch is lost or the older
growth lines (e.g., Lutz 1976; Jones 1980). Such records in parts of the shell are removed by wear.
the shell have been extensively studied in some bivalves and The worm-like shells of most vermetids are cemented to
to a lesser extent in gastropods (e.g., Lutz 1976; Richardson hard substrata and can extend the shell aperture high above
et al. 1980; Jones 1985). For example, Butler et al. (2010) the substratum. The production of internal septa in the shell
reported a 489 year marine climate chronology in the Irish allows it to become much longer than the body. A similar, but
Sea using data derived from growth increments in the shell of unrelated group of gastropods, the siliquariids, are mostly
the bivalve Arctica islandica, individuals of which can live for not cemented, and those that live in sponges have a long shell
over 400 years and show no growth senescence (Ridgway & slit and do not produce septa.
Richardson 2011). Septa-like formations are found in the fresh-water pla-
Microscopic growth lines (microgrowth bands) that norbid limpet Gundlachia (Basch 1959a) and in a few
form with each tidal cycle have been used mainly in stud- Melongenidae (Vermeij & Raven 2009). In some land snails,
ies of intertidal bivalves (see references above) and some septa are formed because of parasitic fly infection (Knutson
gastropods (e.g., Ekaratne & Crisp 1984). This technique et al. 1967). Septa-like formations are also formed in some
is a more accurate and detailed measure of growth rate bivalve shells as foliated layers separated by water-filled
than other methods. Some studies show that the variation spaces, as for example, in some oysters and Spondylus (Healy
in growth rates between individuals can be considerable et al. 2001).
3.2.18 Stable Isotopes and Trace Elements in Shells Chemosynthetic molluscan communities and taxa have also
been studied using isotopes and, besides the shells, tissue of
Many isotopic studies feature molluscan taxa. The accre- living taxa provides isotopic evidence (13C and 15N) of dietary
tionary formation of the calcium carbonate shell provides a preferences and chemosynthetic nutrition (e.g., Windoffer &
historical ‘time and date stamp’ providing data on tempera- Giere 1997; Naraoka et al. 2008; Soto 2009; Becker et al.
ture, habitats, and biological processes (Butler et al. 2010; 2010; Demopoulos et al. 2010). In terrestrial habitats isotopes
Stott et al. 2010; Ridgway & Richardson 2011). Traditionally are important in determining physical conditions (mainly
growth increments have often been useful in determining temperature and rainfall) and food preferences and thereby
growth rate (see Chapter 3), but the chemical properties of serve as important palaeovegetation proxies (Yanes et al.
the shell itself can also provide data about the environmental
2013). For example, Colonese et al. (2013) have analysed

conditions that existed when the shell material was laid down shell carbon isotopes (13C) from Pleistocene and living Helix
by using carbon or oxygen isotopes (see Chapters 3 and 9) figulina from Greece and were able to identify C3 vegetation
(McConnaughey & Gillikin 2008; Ivany 2012; Gillikin & as the main source of carbon for both late glacial and early
Dehairs 2013). The ratios of the stable isotopes of carbon Holocene snails. Although C3 plants are typically associated
(13C/12C) and oxygen (18O/16O), found in the calcium carbon- with habitats with moderate sunlight and temperature, plen-
ate of the shell, are useful in estimating palaeosalinity and tiful water and high CO2 concentrations (200 ppm), the 13C
palaeotemperature. For example, an increase in temperature values from the shells were similar to snails living in extant
results in lower 18O/16O ratios and salinity tends to increase Mediterranean woody shrub communities adapted to drought.
18O relative to 16O, while the 13C/12C relationship provides
Many archaeology studies have combined shell chemis-
estimates of productivity, organic carbon burial, and vegeta- try with the study of growth increments (e.g., Jones 1983a;
tion type. Isotopes of nitrogen, hydrogen, and sulphur are also Hallmann et al. 2009). In the Aleutian Islands, Alaska, growth
commonly used. line studies coupled with stable isotope analyses (18O and 13C)
Various trace elements are also incorporated in shells by have shown that the cockle Clinocardium nuttallii grew faster,
assimilation into the crystal lattice where they replace cal- larger, and were older in the past (170–400 years BP) than the
cium, absorption on the crystal surface, or between lattice cockles found there today (Koike et al. 2012). The study was
planes, by their incorporation into the organic matrix, or by also able to determine that the cockles were collected from
accidental inclusions (Jones 1985). The relative abundance the early spring through early autumn and did not correspond
of calcium and various trace elements can be used to obtain to the seasons with the lowest tides. On a more recent time
information from fossils about the conditions of deposition scale, Schöne et al. (2003) used growth increment analysis
and environmental factors such as temperature (see below), combined with isotopic studies to document how diversion
although many factors need to be considered, including the and management of the waters of the Colorado River in North
affinities of different taxa to different elements. America have changed growth rates of two species of venerid
Each isotopic comparison requires a calibrated standard bivalves in the Colorado River estuary. This study is of partic-
to which sample results are compared. The standard used to ular interest because it demonstrated how the impact of water
calibrate C13 was a mollusc – the Pee Dee Belemnite (PDB), a management policies could be assessed in drainage systems
Cretaceous cephalopod fossil, Belemnitella americana, from where no pre-impact studies were conducted.
the Pee Dee Formation, South Carolina, USA. Samples of Shells of living and fossil Tridacna gigas have the poten-
the standard were depleted during calibration studies which tial to yield reliable records of past changes in seasonality and
required a new reference sample to be calibrated against the ENSO (El Niño Southern Oscillation) variability, and mean
original specimen. Since the laboratory that performed the climate conditions (Welsh et al. 2011). Since the shells are
recalibration was in Vienna, Austria, the standard is called generally more resistant to diagenesis than coral skeletons,
the V-PDB (Vienna PDB). Other isotopes have other stan- they may provide robust estimates of past tropical climate for
dards (or secondary standards now because of depletions). periods and locations where only altered coral skeletons are
For example, the oxygen and hydrogen standard is Vienna available. Molluscan isotopic and sclerochronological time
Standard Mean Ocean Water (or V-SMOW), while for nitro- series data have been useful for palaeoclimatic reconstruction
gen the standard is atmospheric air and for sulphur, it is the (Chauvaud et al. 2005; Schöne & Fiebig 2009; Gilbert et al.
Canyon Diablo meteorite (CD). 2017), reconstructing life history traits in taxa used in aquacul-
Studies of molluscan shell isotopes have led to numer- ture (Radermacher et al. 2009), and in reconstructing ENSO
ous papers estimating palaeotemperatures and salinities events (Carré et al. 2005a, 2005b; Lazareth et al. 2006; Black
and events such as changes in productivity and hydrography 2009). They are somewhat limited in their application as they
(e.g., Jones 1985). These data, often derived from fossil mol- yield relatively short time series (e.g., Carré et al. 2005b). These
luscs, have become important sources of palaeoenvironmen- factors complicate their use for assessing variation in strength
tal data in this time of unprecedented global climate change. and frequency of El Niño events under different conditions, as
Putative ‘molluscan’ shell isotopes (13C) have also been well as studies of the Western Pacific Warm Pool.
used to document the sequence of biomineralisation events Dense monospecific populations of bivalves in cold
during the ‘Cambrian explosion’ (Kouchinsky et al. 2012) seep communities (e.g., the giant white clam Calyptogena
and to reconstruct the carbonate content of Cambrian seas. and Bathymodiolus mussels) are of significance because
their accretionary mode of growth preserves a detailed organs. The epidermis can heal after damage (see Chapter 2)
record of environmental fluctuations in these unique habi- and can also uptake dissolved organic matter (DOM) by way
tats (Rhoads & Lutz 1980). This record includes chemi- of pinocytosis (see Chapter 5).
cal and isotopic fingerprints (Rio et al. 1992), while The histology of the epidermis has attracted much interest.
post-mortem accumulations of shells may contain additional Epidermal cells are typically columnar in shape and can be
taphonomic signatures of fluid venting (Callender & Powell ciliated, non-ciliated, or glandular. Their external surface is
1992; Callender et al. 1992). composed of a microvillous layer which assists in retaining
mucoid secretions in place and is sometimes wrongly referred
to as a cuticle (see Rieger & Rieger 1976; Rieger 1984).
3.2.19 Shell Resorption
However, a true cuticular layer is found in the mouth region of

Probably all shelled molluscs are capable of resorbing at least gastropods and cephalopods.
some internal shell material after it has been laid down. Most Microvilli are usually well-developed in the exposed gen-
coiled gastropods remove some shell material from the exte- eral epidermal regions of the body, but smaller on the outer
rior surface adjacent to the inner side of the aperture as the mantle epithelium.
shell grows. This is particularly necessary in highly sculptured The epidermis may perform its protective function by the
taxa such as those with spines or knobs, as resorption is neces- secretion of a shell and, in many gastropods, an operculum.
sary to remove these sculptural elements when the inner lip of Various chemicals and secretions are also produced by epi-
the aperture spreads across the parietal wall as it grows (see dermal gland cells, the most important of which is mucus (see
Section 3.2.10). In some fresh-water mussels resorption of the Section 3.3.2). Mucus often plays a role in protecting the epi-
shell occurs at a similar rate to shell growth with shell reduc- dermis in locomotion, and in terrestrial gastropods it assists in
tion recorded in some (Downing & Downing 1993; Anthony protecting against desiccation. With mucus, ciliated epithelial
et al. 2001). cells help cleanse the body surface and assist with locomotion.
Resorption of the internal parts of the shell is a charac- The epidermis may become folded into the connective tis-
teristic of only a few marine gastropods, notably most neri- sue to form complex glands that may secrete quinone-tanned
timorphs, and other examples include a few neogastropods proteins to produce byssus threads, an operculum, or radula.
such as Bullia, Conus, Conorbis, and Olivella, and in the In contrast, the jaws of many gastropods and the beaks of
heterobranchs the cephalaspidean Mnestia and ellobiids, cephalopods are derived from a simple epithelium.
with all these possessing elongate apertures (Vermeij 1977b). In addition to epidermal sense organs such as mechanore-
Species of Conus can remove up to around a quarter of the ceptors, chemoreceptors and light receptors (see Chapter 7),
internal shell material. Some terrestrial taxa also resorb inter- specialised epidermal cells are also involved with anti-
nal whorls (Solem 1983); the neritimorph taxa Helicinidae, predator defence, notably repugnatorial glands found in the
Ceresidae, and Proserpinidae all have complete resorption of mantle of some shell-less ‘opisthobranchs’, and specialised
their internal whorls, while ellobiids have partial resorption epidermal pigment cells (chromatophores) which enable ceph-
(e.g., Morton 1955a). Stylommatophorans never completely alopods to rapidly change colour for camouflage and displays
resorb the internal shell whorls. (see Chapter 17).
In some terrestrial slugs, the epidermal cells produce small
buds from their surface during apocrine secretion (Wondrak
3.3 THE BODY
1968; Yamaguchi et al. 2000). Non-glandular pigment cells
The body of a mollusc consists of the head, foot, and viscera – are also found in the epidermis of some slugs (Wondrak 1969,
collectively, and rather quaintly, called the ‘soft parts’ by 2012). Ciliated cells are abundant in areas such as the mantle
some authors. Some primitive molluscs are elongate, with an cavity of aquatic snails and the pneumostome of ‘pulmonate’
anterior end and a posterior anus. In others, the dorsoventral gastropods, the mouth, gills, and foot of most molluscs, and the
axis is extended, and the gut bent into a U-shape (ano-pedal labial palps of bivalves where they assist in maintaining water
flexure) enabling life in blind tubes and the development of a flow, particle sorting and rejection, and locomotion. Although
more compact body shape (see Chapters 1, 5, and 8). sparser on the general body surface and outer mantle, they are
also important in dispersing mucus over the body surface.
3.3.1 The Epidermis 3.3.1.1 Cilia
The epidermis (or skin or integument) protects the animal and Epidermal cells often bear cilia that may be immobile and sensory,
interfaces and interacts with the external world. It covers the or motile and involved in moving water, mucus, or in locomotion.
entire body and performs many functions including protec- Internally each cilium has a ring of microtubules, the axoneme,
tion, respiration, sensory input, and osmoregulation, while the which passes into the cell as the ‘root’ which is anchored in the
epidermis of the foot sole facilitates locomotion and tenacity. cell by a ‘foot’ or basal body. The root may be a single or a double
The epidermis is a single layer of external cells (Figure 3.23) structure in molluscs. If double, it consists of a long and short
on a basement membrane overlying connective tissue perme- ciliary rootlet. This short rootlet is probably plesiomorphic as it
ated by muscle fibres. It is supplied with nerves and contains is present in the Polyplacophora, Solenogastres, Caudofoveata,
sensory cells which, sometimes, have evolved into sense and Scaphopoda, but is absent in Monoplacophora, Gastropoda,
cilia
cilial
microvilli root
lysosome
desmosome
septate pigment
junction granule
secretory
Golgi vacuole
apparatus
nucleus
mitochondrion
smooth
endoplasmic
reticulum intercellular
space
rough
endoplasmic basal lamina
reticulum
mucous cell
epidermal cell ciliated cell
FIGURE 3.23 Three basic types of epithelial cells (epidermal, ciliated, and mucous) found in molluscan epidermis. Sensory cells are
not shown. Redrawn and modified from Simkiss, K., Molluscan skin (excluding cephalopods), pp. 11–35, in E. R. Trueman & Clarke, M. R.,
Form and Function. The Mollusca, Vol. 11, Academic Press, New York, 1988 and Voltzow, J., Gastropoda: Prosobranchia, pp. 111–252, in
F. W. Harrison & Kohn, A. J., Microscopic Anatomy of Invertebrates. Mollusca 1, Vol. 5, Wiley-Liss, New York, 1994.
Bivalvia, and Cephalopoda. There are, however, twin rootlets in salts comprise about 3% of the wet weight of Patella pedal
autobranch bivalves and cephalopods, but these probably rep- mucus (Grenon & Walker 1980). Two groups of protein-
resent a split vertical rootlet (Lundin & Schander 1999, 2001a, polysaccharide complexes have usually been recognised – the
2001b, 2001c; Lundin et al. 2009). glycosaminoglycans (GAGs; often called mucopolysaccha-
Flattened ‘paddle cilia’ have been reported from many adult rides or proteoglycans) and glycoproteins (Reid & Clamp
and larval molluscs on structures such as the gills and osphra- 1978; Di et al. 2012).
dia. Haszprunar (1985a) reviewed the occurrence of paddle While the mucoid gels are all called ‘mucus’, they are
cilia in molluscs and other taxa. They have been variously generally secretions containing polymers that make large
interpreted as locomotory for either moving water or moving entangled complexes to form slippery gels (Smith 2010).
through it, and even for applying byssus threads. They have The structure and composition of the polymers differ mark-
also been considered as chemoreceptive structures and their edly in different molluscs and in other phyla.
presence to be a proof of this function (e.g., Matera & Davis The wide range of secretions is reflected in the diversity of
1982; Haszprunar 1985a, 1987b), but they are now thought to gland cells that produce them in molluscs (see Section 3.3.3).
be fixation artefacts (Ehlers & Ehlers 1978; Matera & Davis While different kinds of mucus produced, notably by the foot,
1982; Beninger et al. 1995b). are presumably derived from different gland cells being acti-
vated, secretions from several different types of gland cell may
combine to produce a specific type of mucus (Shirbhate &
3.3.2 Mucus
Cook 1987).
The molluscan epithelium typically contains mucus-secreting The variety and complexity of molluscan mucus, and in
gland cells which cover the outer surfaces with mucoid secre- particular the legendary slime of terrestrial slugs, is rarely
tions. Mucus is a viscous colloidal solution of mostly water appreciated. The range of different functions (see below)
plus a protein-polysaccharide complex of high molecular often necessitates different physical and biochemical proper-
weight and inorganic salts. It may comprise less than 1% to ties of the mucus which in turn must be produced by a variety
up to over 20% of the wet weight of a mollusc. The inorganic of gland cells (Denny 1983; Davies & Hawkins 1998; Smith
2010) (see Section 3.3.3). Despite attention being paid to the It consists mainly of mucoprotein and some calcium (e.g.,
biochemical structure of some adhesive gels, largely because Campion 1961) and is sufficiently porous to allow some res-
of their potential practical applications (e.g., Smith 2006, piration (Barnhart 1983). About half the organic material
2010) (see also Chapter 10), much of the work on molluscan making up the epiphragm comprises three proteins which,
mucus is still in its infancy. when extracted, have also been shown to cause stiffening in
Mucus is dynamic and versatile, functioning as a slippery littorinid gel (Pawlicki et al. 2004). Some high intertidal lim-
lubricant, an adhesive, or even a rope. This adhesive sub- pets also secrete an epiphragm-like barrier to avoid desicca-
stance is a viscoelastic solid which, when stress increases, tion (Wolcott 1973).
becomes a liquid, but returns to an effectively solid state The mechanisms in marine molluscs are not well under-
when the stress is released. This property enables its use stood, but in terrestrial slugs and a few marine molluscs,
in locomotion (see Section 3.3.2.1). The many functions the mucus is released from secretory cells in packages sur-
of mucus in marine molluscs were summarised in a review rounded by a thin membrane, which immediately absorb
by Davies and Hawkins (1998), and its many roles in ter- water and increase dramatically in volume. Usually a mucous
restrial molluscs are overviewed by Denny (1983). Mucus secretion is formed from a mixture of mucin-like secretions
is vital in feeding (see Chapter 5), reproduction, and loco- from different kinds of gland cells (see Davies & Hawkins
motion and adhesion. It also insulates the mollusc from the 1998; Smith 2010 for reviews). This is particularly the case
surrounding environment, acting as a barrier to diffusion in the pedal epithelia of gastropods (see Section 3.3.2.1)
(Grimm-Jørgensen et al. 1986) and possibly facilitating including terrestrial slugs, the latter being well known for
ionic regulation (Hillman 1969). Some molluscan mucus has their slime.
antimicrobial properties (e.g., Otsuka-Fuchino et al. 1992) Vertebrate mucins are formed from large protein-
and can also protect against predators by the addition of polysaccharide complexes that tangle together. In molluscs,
distasteful or toxic compounds (see Chapters 9 and 20), the although structurally and biochemically diverse, mucus is
production of copious gelatinous secretions, or by making also composed of different protein-polysaccharide complexes
the surface too slippery to grasp. Mucus has also been shown (Denny 1983). These polysaccharides are usually called
to protect from pollutants, and even extreme cold (Davies & mucopolysaccharides and can be neutral or acidic. Acidic
Hawkins 1998). In those taxa associated with cnidarians, mucopolysaccharides (AMPS) often form sticky adhesive
mucus can inhibit the discharge of nematocysts as in some gels, but only after adding specific proteins and/or metal ions
nudibranchs (Chapter 20), the coral living scallop Pedum sourced from other gland cells. The AMPS are an important
spondyloideum (Yonge 1967), and the coral-boring mytilid component of the mucus and are good lubricants because
Lithophaginae (Morton & Scott 1980). In patellogastropods, they are not readily hydrated or separated from the epithe-
foot secretions also trap and stimulate the growth of algae lium (Faillard & Schauer 1972). The negative charge facili-
and diatoms on the substratum (Connor & Quinn 1984; tates cross-linkage (Smith 2002) and affinity to certain metals
Connor 1986). (see Section 3.3.2.1). Sulphated AMPS have been found in
Mucus plays a vital role in the molluscan gut (see bivalves and gastropods, and two types were found in a chiton
Chapter 5) and is of critical importance in suspension-feeders. (Höglund & Rahemtulla 1977). This latter report is one of the
In autobranch bivalves, mucus is crucial for the transportation very few concerned with chiton mucus, despite its production
of food from the gills via the labial palps to the mouth and, being a large part of their energy budget (Horn 1986). Lectins
in some gastropods, sheets or strings of mucus trap food par- (see Chapter 2) have also been reported from the mucus of
ticles. It is also critical in moving (aided by cilia) and binding some stylommatophorans and a loliginid squid (see Davies &
waste to clean the mantle cavities of most molluscs, where it Hawkins 1998 for references).
is secreted by the general epithelial layers and, often in large Prezant (1990) discussed the evolution of the many and
quantities, by the hypobranchial gland(s). varied roles carried out by mucus in bivalves with most stud-
Once secreted, subsequent dehydration of the mucus can ies concerned with the mucus produced by the gills and its
markedly increase its strength and stiffness, as seen in some role in feeding (see Chapter 5).
upper shore and terrestrial taxa. For example, intertidal Few details are known regarding the mucus secreted by
snails such as littorinids and land snails can use mucus to the foot and mantle in scaphopods. Of particular interest is
attach to vertical or overhanging rocks to reduce desiccation. the adhesive mucus produced by the club-shaped heads of the
The secretion of a thick layer of mucus that separates the feeding filaments (captaculae) which are employed in food
foot from the substratum can also help reduce heat stress, capture (see Chapter 16).
as has been shown in some intertidal snails and limpets (see There are few details available about mucus in cepha-
Davies & Hawkins 1998 for review). Some stylommatopho- lopods. Their skin is supplied with gland cells that secrete
ran snails secrete an epiphragm, a layer of mucus that either mucus consisting of a protein-polysaccharide complex
seals the aperture to a hard surface or forms an operculum- (Packard 1988). Coleoid ink (see Chapter 17) is used to deter
like sheet across the whole aperture. The epiphragm hard- predators and is bound in mucus to slow dispersion (Denny
ens when dry and prevents moisture loss during aestivation. 1989).
Nautilus tentacles lack suckers or hooks and instead have of minutes. This markedly contrasts with the slippery and
adhesive papillae that produce a mucoid glue composed viscous mucus these slugs use in locomotion (Deyrup-Olsen
mainly of neutral mucopolysaccharides. Gland cells in the et al. 1983) (see Section 3.3.2.1). Both the mucous secretions
non-adhesive epithelium of Nautilus produce acidic muco- produced by the foot sole and the dorsal part of the foot
polysaccharides (Byern et al. 2012). contain glycoprotein complexes and smaller proteins, but
Some of the biochemical diversity in gastropod mucus pre- the glue contains additional short proteins that trigger gel
sumably reflects phylogeny, but so few taxa have been inves- stiffening (Pawlicki et al. 2004). The defensive sticky mucus
tigated in detail that generalisations are premature. The three produced by some terrestrial slugs is rich in metals (calcium,
main taxa investigated are described briefly below, based manganese, zinc, iron, magnesium, and copper) (Werneke
mainly on a review by Smith (2010). They reflect a very lim- et al. 2007; Smith 2013).
ited selection of gastropod diversity with only three of the five Mucus production, and particularly that involved in locomo-
major groups of gastropods being investigated in detail and tion, involves a considerable cost to the animal, utilising up to
those only from intertidal and terrestrial habitats. 70% of all consumed energy (Davies & Hawkins 1998). While
Patellogastropod limpets adhere strongly to the substra- much of the mucus generated in the gut is reutilised, some that
tum using an adhesive gel, but can alternate between suction binds faecal material is lost. Mucus plays an important role in
and glue, suggesting that the pedal gel properties can change suspension-feeding molluscs, with much of the mucus utilised
(Smith 1992; Worms et al. 1993). Those investigated include being assimilated during feeding, although the mucus binding
both lottiids and patellids. In Lottia, the pedal mucus con- the pseudofaeces in bivalves is lost to the animal.
tains relatively short proteins that cross-link into large aggre- The contribution of molluscan mucus to POM15 and its
gates by way of non-covalent bonds to form an adhesive gel role in shallow marine ecosystems is virtually unknown, but
that contains relatively little carbohydrate (Smith et al. 1999). could be significant (Davies & Hawkins 1998). In a recent
This glue-gel contains a protein absent from the mucus used study of sedimentary organic matter remineralisation, gastro-
in locomotion and in clamping using suction. These last two pod mucus in the sediment was found to accelerate the rate of
gels differ from those of other molluscs in that the non-water remineralisation of nitrogen by 29% (Hannides & Aller 2016).
component is mainly composed of protein molecules instead Although readily degraded by bacteria, slime trails persist
of the very large complexes of protein and carbohydrate for some time on surfaces where gastropods or chitons have
(Grenon & Walker 1980; Smith et al. 1999; Smith & Morin been crawling and may affect microbial film composition and
2002). This gel stiffening protein may cross-link the gel mol- settlement of various marine organisms (e.g., Connor 1986;
ecules (Pawlicki et al. 2004). Holmes et al. 2002).
The caenogastropod ‘marsh periwinkle’ Littoraria irro-
rata (Littorinidae) (as Littorina in much of the literature) 3.3.2.1 The Role of Pedal Mucus in Locomotion
produces both locomotory and adhesive gels (Smith & Morin and Adhesion in Gastropods
2002). Like many upper shore littorinids, when not subjected As noted above, mucus is used for many purposes in mol-
to wetting, they glue the shell aperture to the substratum. luscs, but here we examine the role of mucus in locomotion.
This is done by foot movements that transfer gel from the The remarkable properties of pedal mucus enable gastro-
sole of the foot to the edges of the aperture (Bingham 1972b). pods to adhere to many surfaces by coating them with a
The adhesive mucus contains protein and carbohydrate in thin (10–20 µm) layer of mucus (Denny 1980a, 1980b, 1981;
approximately equal amounts, while that used for locomotion Shirtcliffe et al. 2012). This layer of mucus between the foot
has about the same amount of carbohydrate, but much less and the substratum has several roles. It provides the liquid
protein. The carbohydrates are large, complex polysaccha- in which the propulsive cilia beat, and it can also act as an
rides, and the glue has short proteins not found in the locomo- anchor and/or adhesive. As the animal moves, it leaves a trail
tory gel which are implicated in gel stiffening, presumably of mucus which can often be followed by conspecifics or
by cross-linking the carbohydrates (Smith & Morin 2002; sometimes by predators (see Chapter 9).
Pawlicki et al. 2004). Pedal mucus is extremely important in both cilial and
The mucus of two stylommatophorans, the snail Cornu muscular locomotion. In addition, in creeping molluscs, the
aspersum (as Helix aspersa in most literature), and the slug foot enables the animal to effectively clamp to the substratum
Arion subfuscus (Pawlicki et al. 2004) has non-water com- or climb or clamp on steep surfaces. The adhesive power of
ponents mainly consisting of small proteins, and it also the foot is a combination of the area of attachment and the
contains substantial metal ions involved in cross-linkages properties of the pedal mucus. Increased tenacity is associated
(Werneke et al. 2007). Some stylommatophoran slug mucus with low mucous secretion. The adhesive properties of the
is renowned for its quantity and stickiness. In Ariolimax and mucus can be very efficient, with the force required to remove
Arion, the mucus is extruded from both the dorsal surface patellid limpets ranging from 1.03 to 5.18 kg/cm2 (Branch &
and the foot, is probably mainly defensive (e.g., Mair & Marsh 1978; Grenon & Walker 1981). Little is known about
Port 2002), and the total secretion can be over 5% of the the chemical composition of the pedal mucus of chitons and
body weight of the slug (Martin & Deyrup-Olsen 1986).
The dorsal mucus is initially secreted as a viscous slime,
but becomes very sticky after several seconds to a couple Particulate organic material.
15
nothing about that of monoplacophorans, but there is some that can change its viscoelastic properties (Denny & Gosline
good information about gastropods (e.g., Trueman 1983). 1981), although, in stylommatophoran snails and slugs more
As a muscular pedal wave (see below) moves across the generally, the proteins necessary to form the glue-like mucus
sole of a gastropod foot, the mucus changes in fluidity. It is appear to be added from the ‘protein glands’ on the anterior
much more fluid (and thus not adhesive) beneath the moving margin of the foot (Wondrak 2012).
wave than beneath the stationary parts of the sole where it is When crawling, gastropods have about a third of the tenac-
thick and adhesive (see Figure 3.31). The generation of the ity they have when stationary (Miller 1974a). This is because,
pedal wave (see Section 3.10.3) results in reduced pressure in in limpets at least, glue-like adhesion is used when immobile
that area causing the mucus to become fluid. The mucus then for a period of time, and suction is used when they are active
transforms back to its more solid gel phase at the trailing edge (Smith 1991, 1992).
of the wave. This transition from fluid to gel states is very AMPS (and carbonic anhydrase) from the foot and mantle
rapid and results in mucus acting as a ratchet-like material edges of patellogastropod limpets can produce scars on the
facilitating moving in the desired direction (Denny 1980a). rock surfaces on which they rest (e.g., Lindberg & Dwyer
That part of the sole that is the wave can move with respect to 1983). These home depressions can be deepened by the limpet
the rest of the foot due to this fluid mucus. scraping the rock with its radula (see Chapter 9).
Pedal mucus is a dilute gel made up of a complex mixture
of polysaccharides and proteins (Pawlicki et al. 2004), and
3.3.3 Epithelial and Subepithelial Gland Cells
yet it can produce strong adhesion to wet surfaces, despite
being more than 95% water. Trail mucus is mainly composed Gland cells associated with the epithelium can be lodged in the
of large molecules rich in carbohydrates and some relatively epithelium (intraepithelial) or sunk beneath it with a duct that
small proteins, and the adhesive form of the gel contains extends through the epithelial cells to reach the surface. These
2%–3% more protein than the dilute gel (Smith et al. 1999; subepithelial (or extraepithelial) cells may be unicellular or in
Smith & Morin 2002). These proteins are thus an essential clusters, and in the latter case, may have a common duct as in,
component of the glue and probably cross-link polymers in for example, the pedal epithelium of the gastropods Littorina,
the gel to stiffen it (Pawlicki et al. 2004). Also important Veronicella, and Siphonaria (Smith 2010). The epithelial gland
are transition metals including zinc, iron, and copper which cells are usually unicellular, but multicellular epithelial glands
are necessary for the proteins to act on the gel to form glue. do occur. The gland cells that secrete substances onto the exte-
The polymers in the gel are cross-linked with the involvement rior of the body are called exocrine glands (as opposed to endo-
of metals (Smith 2002, 2006), apparently by catalysing the crine glands whose secretions are supplied to the interior of
cross-linking (Werneke et al. 2007). the body). Gland cells can also be categorised as holocrine and
While the formation and composition of mucous secretions merocrine depending on their method of secretion. Holocrine
of few species have been examined in detail, there may be sig- secretions are formed in the cell cytoplasm and released by the
nificant differences in gastropods from different major groups. cell membrane rupturing, destroying the cell. Merocrine secre-
For example, in the patellogastropod Lottia, there is about tions are released from the cell from small cytoplasmic vacu-
six times more protein than carbohydrate in both the trail oles by way of exocytosis, and the cell continues to function.
and adhesive gels, while in the caenogastropod Littorina the The diversity of types of mucoid secretions is related to the
adhesive form has approximately the same amounts of protein diversity of gland cells that produce them. Most molluscan epi-
and carbohydrate, with two of the proteins being absent from thelia contain various kinds of secretory glands that produce
Lottia. In a stylommatophoran slug and snail investigated by different materials, but details about the products secreted by
Pawlicki et al. (2004) the optimal protein component was specific gland cells are limited to a small number of species.
between 6% and 27%. These differences, together with struc- Studies are difficult because several types of glandular cells
tural modifications, have been in part derived from variations contribute to mucus production and most gels are the prod-
in the habits and habitats of these taxa, but there is presumably ucts of more than one type of gland cell mixed together (Smith
also a significant evolutionary component, given their long 2010). Most detailed studies have focused on gastropods, with
separate histories. It will be of interest to test a wider range of those on bivalves being mainly concerned with the muco-
taxa so the taxon-specific components can be separated from cytes associated with the gills. Consequently, the text below is
those resulting from adjustments to differences in habits. mainly based on information from gastropod studies.
Davies and Hawkins (1998) noted that the number of types The diversity of pedal glands in some gastropods was
of mucocyte differed in different taxa of marine gastropods. reviewed by Smith (2010). Of the nine kinds of gland cells found
Nine types of mucocyte have been reported from the patel- in the foot of the European limpet Patella vulgata, six are found
logastropod Patella vulgata and six from Lottia testudinalis in the sole, and some of those are subepithelial (Grenon & Walker
(Grenon & Walker 1978), but only five in the caenogastropod 1978) (Figure 3.24). Several different gland cells produce either
Littorina littorea (Shirbhate & Cook 1987). Multiple types acidic or neutral mucopolysaccharides (see Section 3.3.2.1),
of mucins may usually be required to produce mucus with proteins, and sulphated and non-sulphated sugars with some
the necessary viscoelastic properties required for locomo- magnesium and calcium produced in the secretions (Grenon &
tion. However, a single kind of mucocyte on the foot sole of Walker 1978, 1980). The subepithelial glands of the sole are the
the terrestrial slug Ariolimax columbianus produced mucus probable source of the adhesive gel (Smith 2010).
Mucus-secreting cells are also present in the epithelia of

dorsoventral the mantle edge and foot of bivalves. Three types of secretory
muscle fibres cells were found in the foot of the arcid Tegillarca granosa,
which are all unicellular and merocrine, being typical of most
secretory cells reported in other bivalves (Lee et al. 2012).
subepidermal A study of the venerid Mercenaria (Eble 2001) reported pedal
gland cell gland cells containing acid glycosaminoglycans rich in sul-
phate and carboxylate groups. In another venerid, Gomphina,
the pedal mucous cells contained mainly AMPS with carbox-
ylate groups abundant in the acidic material (Park et al. 2012).

basement Specialised mantle glands are found in the pedal apertures of
membrane
some burrowing and boring bivalves (see Chapter 15).
Specialised defensive glands on the mantle are found in
columnar
ciliated some gastropods including a few caenogastropods, notably
epithelial the slug-like velutinids (see Chapters 9 and 19) and hetero-
cell branchs including several nudibranchs and marine ‘pulmo-
nates’, notably siphonariids and trimusculids (see Chapter 20).
epithelial
mucocyte
cilia sole 3.3.4 Modifications for Terrestrial Life

Terrestrial snails and slugs suffer osmotic stress less than
FIGURE 3.24 Epithelial and subepithelial gland cells in a marine fresh-water snails, but their main challenge is preventing
gastropod foot sole. Redrawn and modified from Voltzow, J., water loss. This occurs through evaporation via the skin,
Gastropoda: Prosobranchia, pp. 111–252, in F. W. Harrison & Kohn,
locomotion (mucus), and also when discharging waste prod-
A. J., Microscopic Anatomy of Invertebrates. Mollusca 1, Vol. 5,
Wiley-Liss, New York, 1994. ucts (urine and faeces) (see Chapter 6). Terrestrial eupulmo-
nates have developed mechanisms to prevent water loss via
the body including various physiological, behavioural, and
Shirbhate and Cook (1987) examined the histochemistry structural adaptations.
of the pedal and opercular gland cells of three caenogastro- The composition of the slime of terrestrial slugs ranges
pod snails from markedly different habitats. The foot of the from dense mucus produced by vesicular mucous cells to
intertidal Littorina littorea has five types of mucus-secreting clear watery fluid containing little mucus. It also contains
cells, all subepithelial (Shirbhate & Cook 1987). Two types high molecular weight proteins too large to diffuse through
comprise much of the anterior pedal gland that opens into a the skin. Thus the secretions of the skin of stylommatopho-
groove on the anterior edge of the foot. Each type secretes a ran snails and slugs are a combination of mucous secretion
different neutral mucoprotein, and one also has neutral muco- from gland cells, large protein molecules, and watery prod-
polysaccharides. The three types of subepithelial gland cells ucts derived directly by way of ultrafiltration from the blood
on the sole of the foot produce sulphated and carboxylated (Burton 1965; Deyrup-Olsen & Martin 1982). This water and
mucopolysaccharide and a mucoprotein. Glands on the dorsal the large molecules are released via large (~0.5 mm long)
surface of the foot secrete a sulphated mucopolysaccharide and specialised channel cells that penetrate the skin in terrestrial
a mucoprotein. stylommatophoran slugs and snails where they open to the
Three gland cell types make up the anterior pedal gland exterior (Luchtel et al. 1984), thus differing from pore cells
of the terrestrial littorinoidean Pomatias elegans and produce (see Chapter 6). These cells have a central channel and assist
mucoprotein, protein, and sulphated mucopolysaccharide. in regulating the body fluid by allowing water, large particles,
In this terrestrial species, the sole of the foot lacks gland cells and macromolecules to be passed directly to the environment
except in a median furrow where two cell types produce a (see Figure 3.25). They achieve this by having cell membranes
neutral and a sulphated mucopolysaccharide. The dorsal sur- with permeability greater than normal cells – a function facili-
face of the foot has five cell types producing secretions that tated by large pores that allow the big molecules, includ-
aid in reducing desiccation. ing haemocyanin, to pass through the cell walls (Simkiss &
In the fresh-water truncatelloidean caenogastropod Wilbur 1977; Deyrup-Olsen & Martin 1982). The channel
Bithynia tentaculata, the single cell type of the anterior cells assist in restoring the volume of body fluid to normal
pedal gland produces neutral and weakly acidic mucopro- levels following hyperhydration and, possibly, providing fluid
tein, while the foot sole has two types of gland cell that for mucus secretion and body cleansing. The activity of chan-
secrete AMPS and protein. There is also another cell type nel cells depends on neural and/or endocrine16 control of both
that produces carboxylated mucopolysaccharide that is
restricted to a transverse band halfway down the sole of
T he neurohormone arginine vasotocin stimulates the movement of both
16
the foot. Dorsally, three types of gland cell produce various fluid and particles through the channel cell, and this is inhibited by nor-
mucosubstances. epinephrine (Luchtel et al. 1994).
Meghimatium (= Incilaria) fruhstorferi (Yamaguchi et al.

microvillous epithelial cells 2000) and the limacid Lehmannia valentiana (as L. poiri-
eri) (Arcadi 1967). In contrast, Cook and Shirbhate (1983)
found in the dorsal epithelium of the body surface of another
limacid, Limacus ecarinatus (as Limax pseudoflavus), two
kinds of secretory glands (other than channel cells) out of
central 13, one of which secreted AMPS and an unusual type that
passage of haemolymph
vacuole secreted protein. All these gland cells are subepithelial, with
ultrafiltrate into and
through the vacuole their narrow necks extending between the epithelial cells
(Smith 2010). In stylommatophorans, the peripodial groove

tubule surrounds the foot and is richly supplied with glands which,
in the slug Limacus ecarinatus at least, consist of three types
ion exchange & transport
processes that modify the of gland cells (Cook & Shirbhate 1983). In addition, there are
composition of the fluid three distinct groups of secretory cells on the anterior edge of
in the vacuole the foot, one on the dorsal anterior edge where the suprapedal
gland duct opens, one a median gland, and the other an infe-
rior gland. The suprapedal gland is a greatly enlarged anterior
basement mucous gland found in all stylommatophorans. It extends pos-
membrane teriorly along the dorsal side of the foot as a tubular suprapedal
gland. The whole gland comprises identical mucus-secreting
cells (Wondrak 2012).
nucleus
The systellommatophoran Veronicella has 11 types of
gland cell in its skin and also, in response to irritation, pro-
FIGURE 3.25 Channel cell from the dorsal integument of the duces a very sticky mucus on its dorsal surface, where there
terrestrial slug Ariolimax. Redrawn and modified from Luchtel, are two types of gland cells (Cook 1987), but at other times
D.L. and Deyrup-Olsen, I., Body wall: Form and function, pp. 147– the surface appears to be dry. Unlike the stylommatophoran
178, in G. M. Barker, The Biology of Terrestrial Molluscs, CABI slugs mentioned above, the subepithelial gland cells secrete
Publishing, Wallingford, UK, 2001.
into a common duct that opens to the surface. The most abun-
dant type of gland cell secretes neutral and weakly acidic,
haemocoelic pressure and the permeability of the channel non-sulphated carboxylated mucopolysaccharides while the
cells (Martin & Deyrup-Olsen 1982; Luchtel et al. 1984). second cell type secretes protein. It is presumably the com-
Eight types of gland cell occur in different regions of the bination of these two secretions that results in the adhesive
skin of Cornu aspersum (Smith 2010). Of these, three types secretion released on the surface from the inflated common
on the collar (mantle edge) appear to secrete the epiphragm gland ducts when the slug is irritated (Davies & Hawkins
(Campion 1961) (see also Section 3.3.2). They are all sub- 1998; Smith 2010). The foot mucus, secreted by gland cells
epithelial and large, one of the most common being a mucous on transverse ridges on the sole, is, as usual, a mixture of
gland which secretes an acidic, probably sulphated, muco- mucopolysaccharides and protein. There is also a very small
polysaccharide and the gland contents appear to be reticu- suprapedal gland which produces a weakly acidic and a neu-
late. Another, less common, type of mucous cell which also tral mucopolysaccharide and a protein (Davies & Hawkins
secretes AMPS has granular contents and is like cells found 1998).
on the foot sole. Calcium glands are also common on the ven- In stylommatophorans, clusters of small gland cells are
tral part of the mantle collar and contain rod-shaped or spheri- also often associated with chemoreceptive epithelia on the
cal granules in a protein matrix (Campion 1961). Also present tentacles (e.g., Wondrak 1981) and Semper’s organ, associ-
on the collar are ‘protein glands’ whose watery contents con- ated with the mouth (see Chapter 7), has three types of gland
tain protein, and these may actually be channel cells (Luchtel cells (Lane 1964).
et al. 1984; Smith 2010).
The skin of slugs (Figure 3.26) has been better studied than
3.3.5 Acid-Secreting Tissues
other stylommatophorans. In Ariolimax columbianus there
are three main types of gland cells in the dorsal surface – Some molluscs can produce strong sulphuric acid secretions
mucous cells, calcium cells, and channel cells (Luchtel et al. such as seen in the skin glands of some ‘opisthobranchs’
1984), with the mucous and calcium cells secreting the adhe- (Edmunds 1968b) (see also Chapter 20), and cypraeoideans
sive mucus (Martin & Deyrup-Olsen 1986). (Thompson 1969), in the acid glands of Philine (Thompson
Less sticky watery mucus is found on the dorsal surface of 1986), and in the salivary glands of tonnoideans and pleu-
slugs which lack calcium cells, suggesting that calcium may robranchoideans (see Chapter 5). The secretory mechanism
be the catalyst for rendering the mucus adhesive (Smith 2010) appears to be the same in all these cases and similar to the
(see Section 3.3.2). Examples of slugs with only mucous secretion of hydrochloric acid by mammalian oxyntic cells
and channel cells (i.e., no calcium cells) are the philomycid (Andrews et al. 1999). The epithelium in contact with free
Dorsal surface septate junction

microvilli
basal lamina
muscle sensory cell
glycogen
haemocyanin muscle
pore cell
mucus
nucleus
-secreting
pore
extracellular cell
coat
mitochondrion
Golgi zone
cilia
Ventral surface
(Sole)
FIGURE 3.26 Diagrammatic sections through the dorsal and ventral (sole) epidermis of terrestrial slugs (based on Arion and Deroceras).
Redrawn and modified from Newell, P.F., Malacologia, 16, 183–195, 1977.
acid secretion is protected by various possibly molecular spaces. The dilation and contraction of parts of the body in
devices and a coating of mucus, or cirri, or cilia that prevent this way is typically a fairly slow process, although contrac-
the acid contacting the cell surface (Andrews et al. 1999). tion or withdrawal can be rapid if it involves retractor muscles.
In many molluscan structures there are retractors, but obvious
antagonists are often lacking (Russell-Hunter 1968). Thus,
3.4 MUSCULAR HYDROSTAT
blood flow is reliant on antagonists that are often at some
Most movements made by molluscs involve forces generated distance from the organ concerned and this feature, together
by antagonistic muscle elongation and contraction against a with a constant blood volume in the haemocoel, results in
hydraulic skeleton comprising the blood in the haemocoelic some unusual features and limitations (Russell-Hunter &
Russell-Hunter 1968). Examples include limits to the number skeleton can be three to four times the capacity of the shell
of structures that can be extended at any given time. For exam- (Russell-Hunter & Russell-Hunter 1968).
ple, a copulating stylommatophoran land snail displaces a
large proportion of its blood to expand the male genital struc- 3.5 ATTACHMENT OF THE BODY TO THE SHELL
tures, resulting in other parts of the body becoming flaccid.
The total volume of blood in most gastropods and bivalves The molluscan body is attached to the shell by muscles. These
is limited to that which can be contained in the animal when are mainly the foot or pedal muscles of chitons, bivalves, scaph-
withdrawn into the shell, but inefficiencies can be overcome, opods, monoplacophorans, Nautilus, and gastropods (columellar
at least in part, by dividing the haemocoel into compartments. muscles), and mantle muscles which attach to the shell (e.g., pal-
If the blood in a particular structure is isolated from the rest lial line in bivalves). Other muscles such as the buccal retractors,
of the haemocoel, the antagonistic muscles can be used more head and gill muscles, etc. are also typically attached to the shell
efficiently. Examples include the mantle wall of coleoid ceph- which provides a stable anchor point. Unusually, in the palaeo-
alopods where the radial muscles act against the main circu- heterodont bivalves (Unionida and Trigoniida), small patches of
lar muscle system in the mantle wall (see Section 3.12.3.8.2). the mantle also directly attach to the shell (Smith 1983).
Similar systems occur, for example, in some bivalve siphons It was thought that the muscles attached to the shell by
(e.g., Chapman 1995) and the proboscis introverts of higher way of an adhesive epithelium (Hubendick 1958), but when
caenogastropods (Golding et al. 2009b). closely examined using a transmission electron microscope, it
Mechanisms that sidestep these basic limitations are found was seen that there was no direct attachment of the muscle to
in some molluscs. Bivalves with very large siphons and fused the shell. In gastropods and bivalves, a collagenous intercel-
mantle edges use seawater contained in the temporarily sealed lular matrix and an epithelium (tendon cells) lie between the
cavities of the mantle and siphons as an accessory hydrostatic muscle and the shell. An extensive network of extracellular
skeleton. In these cases, the siphonal musculature is the antag- organic fibres extends from the microvilli of the epithelial ten-
onist of the shell adductor muscles (Russell-Hunter 1949; don cells to the inner surface of the shell (often called a brush
Chapman & Newell 1956; Russell-Hunter & Grant 1962). border in earlier literature) (Hubendick 1958; Mutvei 1964;
Another very different mechanism is the water-sinus system Nakahara & Bevelander 1970; Plesch 1976; Tompa & Watabe
in naticids (see Section 3.8.2), where the resulting hydraulic 1976; Watabe 1988) (Figure 3.27). More recently Song et al.
Shell
organic fibrils
tendon sheath
fibril
apical hemidesmosome
microvillus of tendon cell
macula adherens
septate desmosome
Epithelial tendon shell

cell
microfilament
epithelial
tendon cells
basal hemi-
desmosome
myotendon space
Columellar muscle
muscle hemidesmosome
FIGURE 3.27 Diagrammatic section through the attachment zone of the columellar muscle of a gastropod snail. Redrawn and modified
from Tompa, A.S. and Watabe, N., J. Morphol., 149, 339–352, 1976.
(2013) suggested that proteins might act as a glue binding the and muscular control are responsible for rapid colour changes
adductor muscle to the outer calcite layer of the muscle scar in coleoid cephalopods (see Chapter 17).
in the mussel Mytilus.
The mantle also adheres to the shell by tendon cells that 3.7 NON-CALCAREOUS STRUCTURAL
contain tonofilaments (Bubel 1984). In bivalves, the attach- ELEMENTS IN THE BODY
ment scar is indicated as the pallial line on the interior of
3.7.1 Chitin – A Structural Polysaccharide
the shell, although the attachment of muscles and mantle is
not always marked on the shell – as for example, on the colu- Chitin, a long-chain polymer of the monosaccharide
mella of neogastropods (Price 2003). N-acetylglucosamine, which is derived from glucose, is found
in the cell walls of fungi, the exoskeleton of arthropods, and in

various molluscan structures including the radulae and jaws,
3.6 PIGMENTS IN TISSUES and inside epithelial cells lining the body and parts of the gut
of aeolidioid nudibranchs (see Chapter 20).
In this section, we briefly outline the main pigments i dentified
in molluscan tissues. For some explanation of the pigment
types in shells, see Section 3.2.8 and Williams (2016). Useful 3.7.2 Cartilage – Structure and Homology
treatments of p igments in molluscan tissues include the earlier Cartilage tissue occurs in several invertebrate groups other
reviews of Fox (1966), Goodwin (1972), Fox (1983), and the than Mollusca, including the Chelicerata, Annelida, and
more recent overview of Bandaranayake (2006). Brachiopoda (Cole & Hall 2004; Schmidt-Rhaesa 2007).
The main pigment classes recognised by Bandaranayake In molluscs, cartilage occurs in the buccal or odontophoral
(2006) are carotenoids derived from plants and are cartilages in all classes other than bivalves, and it is also found
responsible for yellow to red colours. They are present encapsulating the brain of cephalopods. Although in general
in most m olluscs (e.g., Kantha 1989; Vershinin 1996). the cellular structure of cartilage is rather similar in all inver-
Carotenoproteins produce many colours, including blue, tebrates that possess it, there are some differences. For exam-
green, purple, and red and have been found in various tis- ple, there are differences in the size and number of vesicles in
sues including the ovary and eggs of some molluscs (e.g., the cells, and squid head cartilage cells have long cytoplasmic
Heras et al. 2007). extensions into the matrix (Philpott & Person 1970) that are
Tetrapyrroles include the haemoglobins, haematins, not found in odontophoral cartilages or in the cartilage seen
and porphyrins. They play a primary role in oxidation in other invertebrates (e.g., Kryvi 1977). Odontophoral carti-
and, secondarily, as pigments (Bandaranayake 2006), with lages are described in Chapter 5.
porphyrins also being important as shell pigments (see
Section 3.2.8). Bilichromes (or bilins) are metabolic prod-
ucts of porphyrins with colours varying between yellow,
3.8 HEAD-FOOT
green, red, and brown. Like most bilaterally symmetrical organisms, molluscs have
Other pigments include the pheomelanins and eumela- undergone cephalisation with a concentration of nervous tis-
nins, diverse melanins that range from red to yellow and sues and sensory organs at the anterior of the animal, along
brown, and brown to black, respectively, and melanopro- with the mouth, comprising the head region of the mollusc.
tein which comprises the ink of some coleoid cephalopods. The foot is immediately posterior to the head region and
Ommochromes are found in the chromatophores of cole- often shares dorsoventral muscles with the head (see also
oid cephalopods (Branden 1976), and indoles include the Chapter 12). In three groups – scaphopods, cephalopods,
famous Phoenician dye Tyrian purple, which was produced and gastropods – the head and foot are distinctly separate,
from the hypobranchial gland of Stramonita haemastoma but closely linked, structures – hence the term head-foot.
and other muricoidean taxa. Eumelanins are probably We introduce two new terms to recognise the different rela-
involved in the dark brown and black pigment patterns seen tionship of the head with the shell. The ligocephalic con-
on the sides of the foot, mantle edge, and head of many dition is where the head region is attached dorsally to the
gastropod taxa. shell, and buccal muscle scars are often present on the inte-
Pigments in the external body obtained from food can assist rior of the shell. This condition is seen in Monoplacophora,
with crypsis and perhaps aposematism, as with shell colou- Polyplacophora, and Bivalvia. The apocephalic condi-
ration (see Section 3.2.8). For example, the aforementioned tion is when the head region is not attached to the shell.
dark pigmentation of exposed body regions of gastropods Buccal muscle scars are absent except those integrated with
probably reduces the threat of visual predators. Pigments in shell muscle(s). This condition occurs in Cephalopoda,
the external body tissues are also considered important in apo- Scaphopoda, and Gastropoda.
sematism in some nudibranchs (Edmunds 1991; Haber et al. In shelled taxa (bivalves excepted), it is the head and foot,
2010) and in octopuses (Huffard et al. 2010; Mäthger et al. along with the mantle edge, that are in direct contact with the
2012). Pigment-containing chromatophores under nervous external environment.
3.8.1 The Head Region internally fertilising taxa other penial structures are usually
present. There are sometimes additional tentacles associated
Aplacophorans have a poorly differentiated, eyeless head region with the foot and mantle edge. The various types of tentacles
with a terminal or subterminal mouth. Solenogasters have a sen- found in gastropods are discussed in more detail in Chapters 7
sory vestibule located anterodorsally to the mouth and, when and 18–20. In some higher gastropods, the snout is inverted
moving, the head region is held above the substratum and is to form a retractile proboscis (introvert) (see Chapter 5).
motile. Caudofoveates have a sensory oral shield that may assist Cephalopods have a pair of large lateral eyes, and the
with food detection, but is also involved in burrowing. mouth is surrounded by a series of tentaculate ‘arms’ (up to
In both chitons and monoplacophorans, the head region is 90 in Nautilus or 8–10 in coleoids). In coleoids, these may
constrained by its attachments to the shell. It is small, eyeless,
bear suckers or hooks and, if there are ten, a pair are modi-
and situated anterior to the foot, from which it is little more fied as retractile tentacles. Nautilus ‘tentacles’ or cirri lack
than a protrusion to carry the ventral mouth. The head is gen- suckers. The derivation of the arms appears to be from the
erally simple in chitons. An oral disc surrounds the mouth and foot (Shigeno et al. 2008), as discussed in more detail in
may have extended lips or lappets (e.g., the carnivorous chiton Chapters 8 and 17. In male coleoid cephalopods, one arm (the
Placiphorella). In Lepidopleurus there is a dorso-lateral hood hectocotylus) is modified as a copulatory structure.
surrounding the oral disc similar to the ‘velum’ structure
found in monoplacophorans (Lemche & Wingstrand 1959).
3.8.2 The Foot
Monoplacophorans also have a posterior pair of tentaculate
post-oral appendages and a small preoral tentacle between the The aplacophoran Caudofoveata lack a foot while the
‘velum’ and the anterior mantle fold. Solenogastres have a very narrow foot (retracted within the
Bivalves are the only molluscan group which lacks a dis- ventral pedal groove in preserved specimens) which consists
tinct head region. The only remaining vestiges of the head of a non-muscular fold or folds and is ciliated and richly sup-
region are the mouth and its associated labial palps, with plied with mucous glands. Movement is by ciliary creeping on
ciliated tracts which assist in sorting food particles captured mucus produced by a ciliated, eversible pedal pit that lies at
either directly (protobranchs) or indirectly via the ctenidia the anterior end of the pedal groove. There is evidence that the
(autobranchs). Because of the lack of a head and associated foot reduction or loss in the aplacophoran groups is secondary
sensory structures with which to assess the external world, (Ivanov 1996; Scheltema 1996).
bivalves mainly utilise the mantle edge to gain sensory infor- In polyplacophorans and monoplacophorans the foot
mation. Many have sensory papillae or tentacles along the has a broad, creeping sole capable of clamping to hard
mantle edge and/or siphons, and in a few taxa (e.g., many scal- surfaces. In both groups it is surrounded by a mantle
lops) there are eyes, some of which have double retinas and groove containing the gills, and the groove is covered
guanine crystal mirrors (Palmer et al. 2017) (see Chapter 7). externally by a fleshy girdle in chitons and the shell in
Eyes are also developed on the ends of siphons in a few taxa. monoplacophorans.
For further details on the sensory equipment of bivalves see The foot in gastropods is particularly well-developed,
Chapters 7 and 15. mobile, usually flexible and, in orthogastropods, divided into
The remaining three taxa – Scaphopoda, Gastropoda, and an anterior propodium and a larger metapodium. Dorsally,
Cephalopoda – all have distinct, detached heads, those of gas- there is usually an opercular lobe which secretes the opercu-
tropods and cephalopods being especially well-developed. lum (see Section 3.8.3). A lateral fringe, the epipodial fringe,
The detachment of the head from a dorsal exoskeleton reori- is present in many vetigastropods and typically bears tentacles
ents head musculature, facilitates withdrawal into the shell, and epipodial sense organs (see Chapters 7 and 18). In caeno-
and appears correlated with the development of additional gastropods, other tentacles are associated with the foot, and an
cephalic sense organs. opercular lobe is sometimes also present. Lateral extensions
The scaphopod head consists of a large ‘snout’ (often called of the foot form the parapodia of several groups of euopistho-
a ‘proboscis’) that is not homologous with the snout seen in branchs such as Atyidae, Hydatinidae, Akeridae, Aplysiidae,
gastropods because it is formed anterior to the jaw. A series and Gastropteridae. The wings of the pelagic pteropods
of long, hair-like tentacles (captaculae) that emerge laterally are modified parapodia. The other completely pelagic gas-
from the head is unique to scaphopods (see Chapters 5 and 16). tropod group, the heteropods, have the foot modified as a
Steiner and Dreyer (2003) compared the captaculae to cepha- keel-like ‘fin’. The hydrothermal vent snail Chrysomallon
lopod arms, and Wanninger and Haszprunar (2002a) concluded squamiferum has developed iron-mineralised scales on the
that they also resemble the cephalic tentacles of gastropods. sides and top of the foot (see Chapters 9 and 11).
The gastropod head bears a short to elongate snout with The foot can, particularly in some burrowing caenogas-
the jaws just inside the distal mouth (a synapomorphy of gastropods, be markedly expanded. In naticids, this is achieved
tropods), a pair of tentacles (cephalic tentacles), and a pair of by taking up external seawater into an extensive pedal water-
laterally located small eyes. In a few groups of gastropods sinus system to expand the foot (Morris 1950; Bernard
one of the cephalic tentacles is modified as a penis, but, in 1968; Russell-Hunter & Apley 1968; Russell-Hunter &
Russell-Hunter 1968). The external pores of the water-sinus The anterior pedal gland is particularly well-developed
system are in the mesopodium so that during expansion, sea- in many gastropods and in some extends deep into the foot.
water must be pumped from the mesopodial water-sinuses to In stylommatophorans, it is developed as the suprapedal
those of the propodium. Thus, pedal expansion cannot occur in gland – a long tubular gland that runs between the viscera and
naticids on dry surfaces, and even in water expansion is slow, the muscular part of the foot.
taking several minutes, although retraction takes only a few While all gastropods have gland cells opening to the sole
seconds (Russell-Hunter & Russell-Hunter 1968). It is pos- of the metapodium, in some these are concentrated in a large
sible that this unique water-sinus system in the foot of naticids posterior pedal (or metapodial) gland that opens via an aper-
could be derived from epidermal invaginations such as seen in ture or slit in the sole.
the infolded pedal mucous glands of some other caenogastro- A modified posterior pedal gland, the byssal gland, is
pods (Russell-Hunter & Russell-Hunter 1968). The very large found in the foot of many adult autobranch bivalves and in all
foot of the surf beach nassariid Bullia is expanded largely due autobranch bivalve larvae (for more details see Section 3.11.1
to haemocoelic pressure, but some minor water uptake may and Chapter 15).
also occur (Brown 1964). Mangum et al. (1978) showed that The musculature of the foot is described below (see
the foot in Busycon carica is expanded by seawater uptake, Section 3.12.3.4).
and that blood and water mix freely in the foot, greatly dilut-
ing the blood. The blood is reconcentrated (presumably by
3.8.3 Operculum
the kidney) before returning to the gill and mantle. When the
foot is fully retracted into the shell, blood and water are both Opercula occur in Mollusca, Hyolitha, Bryozoa, and Annelida,
expelled to enable the body of the whelk to fit within the shell. and appear to represent multiple derivations of this protective
In scaphopods and many bivalves, the foot differs from structure, even within phyla (e.g., Brinkmann & Wanninger
the broad creeping surface typical of chitons, monoplacopho- 2009). In the Mollusca, opercula occur in Cephalopoda –
rans, and gastropods in being capable of digging in sediment nautiloids and ammonites – and in the Gastropoda, all appar-
using hydrostatic pressure generated through haemocoelic ently independently derived. In the cephalopods, ammonites
spaces by enlarged anterior and posterior pedal retractor had a pair of horny, and sometimes calcified, lower jaw plates
muscles. The bivalve foot is often large, typically laterally (the aptychi), which closed the aperture of the shell when
compressed (modified for digging), rarely expanded laterally the animal withdrew. In living Nautilus, two modified cirri
for crawling, or very reduced or even lost (in adults). In pro- form a leathery hood structure which closes the shell aper-
tobranch bivalves, the foot is divided ventrally to form two ture when the animal withdraws into the body chamber (also
ventral keels fringed with papillae in most species. The keels see Chapter 17). The gastropod operculum is generated on the
can be expanded laterally to act as an anchor in the sediment. dorsal surface of the foot and is composed of conchiolin and
In autobranch bivalves, the foot is often hatchet-shaped or sometimes calcified. Some early workers considered the gas-
rounded and sometimes a small sole-like flattening is present tropod operculum a second shell valve and equivalent with
ventrally, especially in the posterior part of the foot, while in the bivalve shell (see review in Fretter & Graham 1962, p. 76),
most cementing bivalve species the foot is reduced. but the production of the supposed second valve by the foot
In scaphopods, the foot lacks pedal glands and differs in epidermis, not the mantle, shows it is not a homologue.
the two main groups, Dentaliida and Gadilida. In the former, The gastropod operculum is a readily identified synapo-
the conical foot has well-developed smooth epipodial lobes morphy of the group. It usually first appears in the larval
laterally and ventrally that anchor the foot in the sediment. stage; it is absent in the larvae of pleurobranchs, but present in
In the Gadilida, the terminal disc of the foot is often fringed most nudibranch larvae, although it is lost at metamorphosis
with papillae. (Gibson 2003). An operculum is also absent in direct-devel-
In cephalopods, the foot is so highly modified it cannot oping embryos of some gastropods, including stylomma-
be recognised as such, although developmental studies have tophorans and vaginulids (G. Barker pers. comm. Nov. 2014).
shown that the arms are derived from the foot (Shigeno In adult gastropods, an operculum is present in most vetigas-
et al. 2008) (for further information see Chapters 8 and 17). tropods and caenogastropods, in lower heterobranchs, and
The muscular funnel directs a stream of water expelled from some basal euthyneurans. It is absent in adult patellogastro-
the muscular mantle cavity, notably during jet propulsion (see pod, cocculinoid and lepetelloid limpets, most euthyneurans,
Chapter 17 for details). and some taxa in a number of vetigastropod and caenogastro-
pod families. The operculum is also absent in some terrestrial
3.8.2.1 Pedal Glands neritimorphs (Proserpinidae and Ceresidae), while limpet-
Besides epithelial sole glands, glands near the anterior end like neritimorphs (e.g., Phenacolepas and Septaria) have a
of the foot in aplacophorans, chitons, monoplacophorans, and reduced operculum embedded in a fleshy pocket.
gastropods secrete mucus to lubricate the sole during locomo- Three basic types of gastropod opercula are usually rec-
tion (see Section 3.3.2.1). Anterior pedal glands are also found ognised: multispiral (polygyrous) with numerous spirals and
in a few bivalves, but these are probably not homologous with a central nucleus, paucispiral (oligogyrous) with few spirals,
those of other molluscs or even within bivalves (Waller 1998) and concentric. This latter type is not spiral, and its nucleus
(see Chapter 15). can be situated internally, marginally, or terminally. Spiral
opercula (whether multispiral or paucispiral) are secreted at In the only detailed investigation of the operculum in
the internal edge of the opercular disc (see below), and the recent years, Checa and Jiménez-Jiménez (1998) recog-
operculum rotates as it grows. Based on the outside spiral pat- nised two main kinds of spiral opercula – those that closely
tern, the rotation is always clockwise in dextral and counter match the aperture in shape (rigiclaudent) and those that
clockwise in sinistral taxa. Concentric opercula grow differ- do not (flexiclaudent), as in opercula of vetigastropods like
ently – new material is added along all or part of the periphery Pleurotomariidae and Trochidae where the operculum fits the
of the operculum, but these seemingly neat distinctions are aperture by the edges bending outward. These authors dis-
not as clear-cut as often thought. For example, some opercula tinguished three main types: (1) flexiclaudent spiral (mostly
change from an initially spiral pattern to become concentric, multispiral) operculum, the shape of which does not fit the
as in bithyniids. There is also considerable variation in the aperture, but fits by flexing into the aperture, (2) rigiclau-
number of spirals and how tightly they coil so there is not a dent spiral (fitting the aperture and may be multispiral or,
clear distinction between multispiral and paucispiral opercula. more usually, paucispiral), and the aperture is used as a tem-
Calcification of the operculum has occurred multiple times in plate when growing, and (3) rigiclaudent concentric, which
gastropod evolution. The earliest fossils sometimes interpreted also typically fits the aperture unless it is reduced in size.
as calcified opercula are the Early Ordovician fossils named The flexiclaudent spiral type is secreted when the foot is
Ceratopea (Yochelson & Bridge 1957), but these cap-shaped extended. The other two types which do not flex upon retrac-
shells are probably not opercula (Yochelson & Wise 1972). tion, except perhaps at their outermost margins, grow when
Typical multispiral calcified opercula are known as early as the operculum is held in the aperture, and this growth may
the Middle Ordovician, while Maclurites from the same period or may not be spiral (i.e., the operculum rotating as it grows).
have a paucispiral operculum (Yochelson & Linsley 1972). As already noted, there are many intermediate situations
The operculum is attached to a disc-like epithelium, on between the distinctions in form, structure, and formation
the dorsal surface of the foot, called the opercular disc. It is described above.
attached to only part of the operculum, not the whole under Opercular calcification can occur only in rigiclaudent
surface. Secretory cells in the opercular groove and disc gen- opercula, but is achieved in several ways. For example, in
erally secrete mucopolysaccharide and at least two differently turbinids a thick calcareous layer is added on the outer sur-
staining proteins (Shirbhate & Cook 1987). face of a corneous paucispiral operculum. This is achieved
The operculum is composed of conchiolin, mainly a homo- by a fold of epithelium that lies at the anterior (when the
geneous scleroprotein hardened by quinone tanning. All oper- foot is extended) edge of the opercular groove (Figure 3.28).
cula examined show a similar pattern of amino acids with a The precipitation of calcium occurs when this fold partially or
high glycine and aspartic acid content, although the varnish completely covers the operculum when the animal is crawl-
has higher levels of glycine than the other layers (Hunt 1976). ing, but it is retracted and the operculum exposed when the
The operculum consists of several layers (Figure 3.28), foot is retracted. Other types of calcified spiral opercula occur
which are typically – from outer to inner side – a thin outer in some neritoideans and naticids. In naticids with calcareous
hyaline layer, a thicker main layer, and the adventitious and opercula, the labial mantle margin, not the foot, deposits the
varnish (shiny) layers (Checa & Jiménez-Jiménez 1998). calcium (as aragonite) onto the otherwise corneous operculum
While the main and varnish layers are always present, a hya- (Checa & Jiménez-Jiménez 1998). Some concentric opercula
line layer is found in spiral and concentric opercula with the are calcareous (e.g., Bithyniidae, Pomatiidae), where organic
nucleus on the labral edge, and adventitious layers are only and calcareous layers are closely packed together.
found in concentric opercula. In some taxa, one or more cal- A flexiclaudent (mostly multispiral) and rigiclaudent spi-
careous (calcitic or aragonitic) layers are added. ral are generally the types present in vetigastropods, with
The different layers are produced in different ways. the former predominant. Neritimorphs have a rigiclaudent
The hyaline layer (when present) is secreted in a slit-like operculum, and this is also the usual type in lower caeno-
structure of the foot, the opercular groove. On the extended gastropods, although a few cerithioideans have flexiclaudent
foot, this structure lies at the anterior edge of the opercular spiral opercula. Higher caenogastropods mostly have con-
disc and runs across the main body axis, and the material it centric opercula, and this is the only kind found in neogas-
secretes bears similarities to the periostracum. When the foot tropods. Rigiclaudent spiral opercula are found in nearly all
is retracted, the opercular groove coincides with the inner lower heterobranchs and the few operculate euthyneurans
edge of the aperture. The main layer of the operculum lies (Checa & Jiménez-Jiménez 1998), with exceptions being con-
below the thin hyaline layer (when present) and is secreted centric opercula in Rissoellidae and Retusa.
by tall cells at the edge of the opercular disc. Varnish may be While the distribution of the different kinds of opercula
secreted by a second groove that lies immediately behind the in gastropods has a phylogenetic basis, this is modified by
opercular groove, as in some trochids, but in others (including changes imposed by shell morphologies. For example, the
concentric opercula), it is secreted by a flap on the posterior depression of the spire leading to planispiral or near planispi-
edge of the opercular disc. In concentric opercula, layers are ral shell morphology will often result in oval paucispiral oper-
added posteriorly from the surface of the opercular disc, each cula becoming circular with more spirals, while an elongated
added at the bottom of the operculum (see Checa & Jiménez- aperture with a canal will result in a concentric operculum
Jiménez 1998 for more details and references). (Checa & Jiménez-Jiménez 1998).
nucleus
varnish layer
multispiral flexiclaudent
nucleus conchiolin (main) layer

paucispiral rigiclaudent
nucleus
adventitious layer
concentric with terminal nucleus
nucleus
concentric with internal nucleus
Sections through opercula
opercular
groove
opercula
r disc
varnish
secreting multispiral flexiclaudent concentric with external nucleus
groove
direction of rotation of
epipodial extension which operculum as it grows
secretes calcium layer
calcium layer
foot
opercular
paucispiral rigiclaudent with paucispiral rigiclaudent lobe
external calcareous layer
FIGURE 3.28 The structure of various types of gastropod opercula, as seen in cross-section, and its relationship to the foot and opercular
disc. Uppermost section redrawn and modified from Checa, A.G. and Jiménez-Jiménez, A.P., Paleobiology, 24, 109–132, 1998; next three
and lower right redrawn and modified from Fretter, V. and Graham, A.L., British Prosobranch Molluscs: Their Functional Anatomy and
Ecology, Ray Society, London, UK, 1962; based on Houssay, F., Archives de zoologie expérimentale et générale, 2, 171–288, 1884 and
Kessel, E., Zeitschrift fur Morphologie und Okologie der Tiere, 38, 197–250, 1942; three of lower four redrawn and modified from Checa,
A.G. and Jiménez-Jiménez, A.P., Paleobiology, 24, 109–132, 1998.
Various theories have been proposed to account for the and can secrete shell material to thicken the overlying shell,
operculum on the surface of the foot, and how it obtained the or in some taxa, dissolve the shell. For example, in taxa such
ability to secrete the conchiolin which forms the operculum. as ellobiid and neritid gastropods, the inner chambers of the
This substance is chemically like the periostracum and Checa shell are dissolved, making the calcium available to the ani-
and Jiménez-Jiménez (1998) proposed a ‘periostracum shav- mal (see Section 3.2.19). In shell-less sea slugs, the dorsal
ing model’ to account for the origin of the operculum based on surface (plus the extending edges) is often referred to as the
the morphology of the flexiclaudent spiral operculum, which dorsum or notum (which, depending on its derivation, may be
appears to be the most primitive type. They argued that in the homologous with the dorsal mantle), and the ventral surface
parietal segment of the mantle the periostracal groove became beneath the protruding edges is called the hyponotum. In sys-
independent from the rest of the mantle and migrated on to the tellommatophoran slugs, the hyponotum, along with the foot,
foot providing the necessary organic material to form an early forms part of the ventral creeping surface. This is demarcated
form of the operculum. With the development of the opercu- from the notum by a sharp angulation (or sometimes a groove)
lar disc, the flexiclaudent spiral operculum could be formed called the perinotum. In some shell-less taxa the dorsal sur-
from the periostracal strip produced by the opercular (i.e., face is formed from a reflected mantle edge or parapodial
modified periostracal) groove. These opercula do not fit the flaps from the foot (see Section 3.2.15).
aperture shape, but this was rectified by the subsequent inde- Other modifications of the dorsal mantle include epider-
pendent evolution of the rigiclaudent type in several lineages. mal papillae in chitons and aplacophorans which are possi-
The evolution of rigiclaudent opercula also preceded their cal- bly plesiomorphic for Mollusca (see Scheltema 1993), while
cification. A greater range of apertural modifications (such as in some shell-less gastropods (slugs), it can be produced into
a siphonal canal) became possible and greatly increased with elaborate projections. The tubules from the dorsal mantle in
the evolution of the concentric operculum and its wide range some gastropod and bivalve taxa extend into the shell forming
of possible shapes (Checa & Jiménez-Jiménez 1998). shell pores (see Section 3.2.9), while in chitons, the aesthetes
that penetrate the shell are formed from nervous tissue (see
Chapter 14).
3.9 THE MANTLE
Along with the head and foot, the mantle edge has direct con-
3.9.2 Mantle Skirt
tact with the external environment and thus plays a significant
role in the interactions of the animal with that environment. This term is used for the parts of the mantle that extend beyond
The mantle, sometimes called the pallium, is one hallmark the visceral part of the body, particularly that cape-like part
of molluscs. It covers the dorsal body, including the mantle of the mantle that forms the external roof of the mantle cavity
cavity, and carries out several functions – the formation of the or, as in nudibranch slugs, the overhanging part of the dorsum.
shell and/or spicules, the reception of sensory information, The inner epithelial layer of the mantle skirt, which is often
and often a significant respiratory surface. It is also responsi- modified as structures such as hypobranchial glands and/
ble for regulating water currents entering or exiting the mantle or ciliated fields or ridges (see Chapter 4), is not part of the
cavity or mantle groove. mantle.
The mantle consists of two main parts: the part that typically
lies beneath the shell, or in those molluscs where the shell has
3.9.3 Mantle Edge
been reduced or lost, the part that lies over the surface of the
body. There is some confusion as to the terminology associ- The free edge of the mantle skirt and any protrusions com-
ated with the mantle, and its extent – for example, in gastropods prise the mantle edge. It usually has two or three lobes, one of
some (e.g., Hyman 1967) restrict the mantle to the last whorl which may bear tentacles, and, in some taxa, one lobe may be
of the shell, while many others (e.g., Fretter & Graham 1962) expanded to cover some or all of the shell. The mantle edge
also use the term for the dorsal epithelium covering the viscera. consists of two layers of epithelia separated by a space contain-
Here we treat the mantle as the epithelium that forms the entire ing some muscle, connective tissue, and blood spaces, and the
dorsal covering of a mollusc body (except for the head and foot) lower epithelial layer is in contact with the external medium.
together with, if they are present, the protruding edges. The peri- Parts of the mantle edge are responsible for the secretion of
ostracum and the growing edge of the shell are secreted by the the periostracum and the initial shell material deposited at the
mantle edge. The mantle underlying the shell secretes additional growing edge of the shell. The mantle edge is also respon-
material to thicken or repair the shell from the inside. We use the sible for the control of water currents entering and leaving
terminology outlined below for the parts of the mantle. the mantle cavity by way of controlling the size of apertures
with folds, flaps, or siphons. In some bivalves, the closure of
much of the mantle edge confines and directs the water flow
3.9.1 Dorsal Mantle
(see Chapter 15 for details). Because it is in contact with the
The thin epithelial layer (‘skin’) covering the visceral part of external environment, the mantle edge is an important sensory
the body. In shelled molluscs, it lies against the inner surface surface and provides a major part of the sensory equipment
of the shell. It is in contact with the extrapallial fluid between in many molluscs. Many elaborations, including tentacles and
the mantle and the shell (i.e., that part lying beneath the shell) eyes, enhance this function (see Chapter 7), particularly in
bivalves because they lack a head. It also has other secretory

functions including being a source of mucus secretion in many
molluscs and, in some, has developed repugnatorial secretory
structures that deter predators. For example, assumed dis-
tasteful secretions of the mantle edge in the limpet Cellana Polyplacophora
deter predators and competitors (Branch & Branch 1980) and
those from the repugnatorial glands of Trimusculus anesthe-
tise potential predators (Rice 1985). There are also examples
in other gastropods, and notably nudibranchs, where noxious
chemicals are sometimes concentrated on the mantle edge

(see Chapter 20). Aplacophora
The mantle edge has one or more folds which are elabo-
rated differently in the major groups of molluscs (Figure 3.29),
as outlined by Beedham and Trueman (1967) and Stasek and
McWilliams (1973).
In polyplacophorans, the mantle skirt and edge form a gir-
dle around the lateral edges of the eight valves. It is composed Monoplacophora
of three regions. A small fold on the proximal upper surface
secretes the shell and is separated from the main mantle rim
by the periostracal groove. The main mantle rim comprises the
girdle and secretes the spicules, hairs, or scales. The third com-
ponent is a low ridge on the underside of the mantle edge that Bivalvia
contains mucous glands. It has been suggested that the part of
the mantle edge in chitons between the proximal wall of the
properiostracal groove and the shell edge is homologous with
the conchiferan outer mantle fold (Haas 1972; Stasek 1972).
Aplacophorans are unlike other molluscs in having a
spicule-producing mantle surrounding a worm-like body with Gastropoda
no distinct mantle edges. Although this condition has been
considered primitive for molluscs (e.g., Salvini-Plawen 1980a;
Haas 1981), it is only one of several possible evolutionary sce-
narios (see Chapter 12).
The monoplacophoran mantle edge has a periostracal
Scaphopoda
groove situated ventrally some distance inside the mantle (and
hence shell) edge and an inner ventral fold, while the middle
fold is less distinct (Haszprunar & Schaefer 1997).
In all bivalves, the mantle edge is comprised of three folds
(Stasek & McWilliams 1973) (Figure 3.30). In some galeom-
matoideans, the middle lobe is expanded over the outer shell Cephalopoda
surface. In other bivalves these folds fuse in various combina-
tions to close the mantle and form siphons (see Chapter 15 for
more details).
An indication of the plesiomorphic state of the mantle edge
in cephalopods can be seen in Nautilus where it is trilobed, FIGURE 3.29 A diagrammatic comparison of the morphology
like the situation in bivalves, with the periostracal groove situ- of the mantle edge of a typical bivalve and a typical gastropod.
ated between the outer lobe (that secretes the shell) and a mid- Redrawn and modified from Stasek, C.R. and McWilliams, W.R.,
dle lobe or fold. There is also an inner fold (Westermann et al. Veliger, 16, 1–19, 1973. Monoplacophoran redrawn and modified
2005). In coleoids, the mantle has covered the body by an from Schaefer, K. and Haszprunar, G., Zool. Anz., 236, 13–23, 1997.
extension of the mantle rim. Thus, the exposed dorsal surface
of coleoid cephalopods is not derived from the dorsal mantle,
but from the mantle edge. a prominent inner fold or swelling, but the largest deviation
Despite the size and diversity of the group, gastropods from the normal gastropod pattern is seen in fissurellids, where
have, with a few exceptions, a relatively uniform arrangement the mantle edge is distinctly trilobed. In some species, a well-
of the mantle edge (Figure 3.30). In most, including patello- developed middle fold envelops part of the shell, and a larger
gastropods, the mantle edge forms a single lobe that secretes ventral fold forms a fleshy curtain below the shell. In other gas-
the shell, and the periostracal groove is situated adjacent to tropods with the mantle enveloping part or all of the shell, it is
the shell edge. In many limpet-like orthogastropods, there is the single mantle lobe that is extended (Figure 3.30).
periostracum
shell outer shell
fold
periostracal
groove
mantle
rim
middle
epithelium fold
inner
fold
Bivalve Gastropod
FIGURE 3.30 Mantle edge morphology in molluscs redrawn and modified from Stasek, C.R. and McWilliams, W.R., Veliger, 16,
1–19, 1973.
Scaphopods have a large, fleshy lobe-like extension to their 3.10.1 Ciliary and Muscular Locomotion
anterior mantle edge that assists in closing off the aperture. Using A Creeping Foot Sole
The periostracal groove lies adjacent to the shell edge.
An early study by Vlés (1907) provided a classification and
terminology for the different modes of locomotion in gas-
3.10 LOCOMOTION tropods which were subsequently modified by others (e.g.,
Olmsted 1917; Miller 1974b) (see Table 3.4). Much of the
Molluscs move by crawling, burrowing, or swimming.
review below is derived from the detailed studies of gastro-
In those that crawl or burrow, and in some that swim, the
pod locomotion conducted by Susanne Miller (Miller 1974a,
foot is the main organ of locomotion. As deftly expressed by
b), who investigated modes of locomotion, speed, tenacity,
Kappes and Haase (2012), ‘The Mollusca provide proverbial
and foot form of nearly 300 species in 52 families of marine
examples for “sluggishness” and time-consuming movements
gastropods (other than Heterobranchia). Her work showed
“at a snail’s pace”’. Chase (2002) argued that the famously
that the greatest diversity in locomotory modes occur within
slow movements of gastropods are largely due to the lack of
the caenogastropods, and that foot size and shape, and small
a hard, internal skeleton, thus limiting the amplification and
differences in locomotory mode, affect the speed of move-
antagonism of muscular action. While there is some truth in
ment and the strength of adhesion to the substratum.
this, faster movements do occur in some molluscs, such as
the leaping movements of strombid gastropods, the aggressive
territorial responses of some limpets, the swimming of some
shell-less heteropods and pteropods, the rapid jetting of many 3.10.2 Ciliary and Arrhythmic Locomotion,
cephalopods, and the energetic burrowing rates of some
Including Leaping
bivalves (e.g., Donax). Simple rate-based values of distance
travelled do not adequately describe the breadth of the roles Solenogasters have a long, narrow, reduced foot (see
of locomotion, all of which depend on a complex and flex- Section 3.8.2) and the animal moves by ciliary action along
ible system of behaviours. For example, the four basic drives a thick mucus strand, which has been likened to a monorail
(Four Fs) of Aplysia all include locomotion (Dickinson 1996; (Salvini-Plawen 1968b; Scheltema & Jebb 1994).
Moroz 2011). Locomotion in some gastropods can be entirely due to the
The broad, creeping foot of chitons, limpets (and presum- action of pedal cilia, which are highly coordinated and thought
ably monoplacophorans), provides for both adhesion and to be under nervous and/or neurosecretory control (e.g., Jékely
locomotion. Chitons, limpets, snails, and slugs creep slowly 2011), and they produce a smooth, uniform, and rapid gliding.
by cilia or waves of muscular activity (pedal waves) that This type of locomotion is seen in most tiny gastropods, but
move along the foot. The eight independent shell plates of also occurs in some large taxa, e.g., in some naticids, neogas-
chitons allow them to adhere and move over highly irregular tropods, land and fresh-water ‘pulmonates,’ and many ‘opistho-
surfaces that would be difficult for a single-shelled gastro- branchs’. Compared to muscular propulsion (see below), ciliary
pod. Backward locomotion is fastest in polyplacophorans locomotion is relatively ineffective, especially in larger species,
(e.g., Chiton, Ischnochiton, Cryptochiton) (Parker 1914; although the weight carried by the foot is reduced in aquatic
Boyle 1977; Kuroda et al. 2014). Miller (1974b) found back- habitats, enabling larger species to use this means of locomo-
ward locomotion in gastropods to be rare, and when present tion. In terrestrial habitats, gastropod locomotion using cilia
it was slow and of limited duration. Backward locomotion alone appears to be restricted to small species (Jones 1975).
has been reported in both patellogastropods and vetigastro- The speed of locomotion depends on the rate of ciliary
pods (e.g., Patella, Lottia, Fissurella, Monodonta) (Olmsted beating and on environmental factors (e.g., temperature, sub-
1917; Jones & Trueman 1970; Kuroda et al. 2014). strata). A longer cilium has a faster tip speed, so those with
Some species with ciliary locomotion, such as those in the

TABLE 3.4 caenogastropod Nassariidae, can thrash their foot effecting
Classification and Higher Taxon Occurrences of Ciliary a leaping movement (but in a different way from that seen
and Muscular Locomotory Modes in Polyplacophora in Stromboidea and Xenophoridae – see below) to avoid
and Gastropoda predators.
If the first molluscs were small (see Chapter 12), it is
I. Muscular
a. Rhythmic
likely that they first moved with cilial action alone. It is thus
i. Monotaxic
interesting that chitons and some primitive gastropods move
1. Retrograde Polyplacophora, Vetigastropoda, by pedal waves (see below). Many apogastropods17 move
Neritimorpha by cilial action, this perhaps being a consequence of their

Caenogastropoda, Heterobranchia assumed paedomorphic origin (Ponder & Lindberg 1997).
2. Direct Caenogastropoda, Heterobranchia The groups of apogastropods with various types of loco-
ii. Ditaxic motory methods alternative to cilial movement have presum-
1. Retrograde ably developed these independently. Some cilial movers may
a. Transverse Patellogastropoda (forward), show irregular, rather unpredictable muscular movements of
Vetigastropoda, Caenogastropoda the foot sole – a phenomenon called arrhythmic locomotion
b. Diagonal Caenogastropoda (Miller 1974a, b) which was divided into those with distinct
2. Direct terminating waves and those with indistinct waves. The latter
a. Transverse Patellogastropoda (backward), type was further subdivided into continuous or discontinu-
Vetigastropoda, Caenogastropoda ous type 1 and type 2 locomotion (Table 3.4). These indis-
b. Diagonal Caenogastropoda
tinct pattern-less movements differ greatly from the regular
iii. Composite Caenogastropoda
undulations that form pedal waves described below, and they
b. Arrhythmic
are grouped with cilial movement in Figure 3.35. These
i. Distinct Terminating Waves
arrhythmic waves can begin and terminate anywhere on the
l. Continuous Caenogastropoda
2. Discontinuous Type 2 Caenogastropoda
sole, these being areas where the sole epithelium elongates
ii. Indistinct
(as in retrograde waves – see below). One type of arrhythmic
1. Continuous Caenogastropoda locomotion (the ‘indistinct discontinuous type 2’ of Miller)
2. Discontinuous Type I Caenogastropoda is found only in the Stromboidea and Xenophoroidea and
3. Discontinuous Type 2 Caenogastropoda facilitates leaping behaviour. This type is distinguished in
c. Leaping Caenogastropoda Figure 3.35 and is discussed further below.
II. Ciliary Solenogastres, Caenogastropoda, Arrhythmic waves occur when the movement of the sole is
Heterobranchia discontinuous and can occur in species with indistinct move-
ment (see above) and in some with a distinctive pedal gait.
Sources: Miller, S.L., J. Molluscan Stud., 41, 233–261, 1974b; Salvini- There are two main types (Miller 1974a, b): in the first, the
Plawen, L. v. Sarsia, 31, 105–126, 1968a; Kuroda, S. et al., J.
foot is extended while the shell rests on the substratum and
Royal Soc. Interface, 11, 20140205, 2014.
the foot is then attached or anchored as the shell is pulled for-
ward by contraction of the columellar muscles. In the second,
the shell is thrust forward, and then the foot is brought for-
long pedal cilia (as in many aquatic taxa) will move faster ward and attached or anchored at a point in front for the next
than those with shorter cilia (Jones 1975). forward movement of the shell. Leaping is a specialised form
While ciliary locomotion is employed by many small- of this latter type of discontinuous locomotion and occurs in
sized molluscs (and other animals), it is also the main locomo- members of the caenogastropod families Strombidae (Berg
tory power in some large gastropods such as the nearly 30 cm 1972, 1974; Field 1977), Struthiolariidae (Crump 1968), and
long and heavy Cassis tuberosa (Cassididae) (Miller 1974b). Xenophoridae (Morton 1958c). The operculum is modified as
This species and other large gastropods employing ciliary a lever and when the foot twists, the operculum is thrust into
locomotion have a very large foot sole that spreads the weight the substratum to provide the leverage to vigorously thrust the
per unit foot area (Miller 1974b). For example, Copeland shell forward or even backward (Miller 1974a). Besides leap-
(1922) calculated that the pedal cilia of Polinices duplicata ing, arrhythmic pedal locomotion is usually less efficient than
could transport weights of 4 g/cm2, although this species, like rhythmic pedal waves (Miller 1974a). A similar, specialised
some neogastropods, uses muscular waves (see below) when mode of locomotion involves the use of the snout together
greater speed is necessary. with the foot, as described below.
Non-heterobranch gastropods that move by ciliary Species with either type of arrhythmic locomotion have
means differ from those that use muscular waves (see a wide range of foot sizes and shapes; they mainly have a
below) in having a broader, longer foot (longer than the short, broad foot although some can have a long, narrow foot
shell). For example, the Nassariidae have a much larger foot (mostly Conidae). Foot shape can vary considerably within
area than most buccinoideans with non-ciliary locomotion
(Miller 1974b). Caenogastropoda + Heterobranchia.
17
clades. For example, although all Conoidea examined have 1980b, 1981; Denny & Gosline 1981; Chan et al. 2005).
indistinct arrhythmic locomotion, species of Terebridae and This method of locomotion is very effective, but is also ener-
‘Turridae’ have a shorter, broader foot than do members of the getically expensive (Denny 1980b; Tyrakowski et al. 2012).
Conidae, and these differences are not entirely correlated with It is achieved by a succession of muscular waves moving
substratum preference (see also Section 3.10.6). In caenogas- along the foot which is connected to the substratum by a
tropods (where most variation is seen), the foot area relative thin layer of mucus. This mucus becomes more solid under
to size tends to be most diverse in those taxa with retrograde pressure and more fluid when that pressure is relaxed (see
ditaxic locomotion. Section 3.3.2.1). The biomechanical properties of mucus
Those species with type 1 discontinuous locomotion (most combined with the muscular waves produces a very effective
have indistinct arrhythmic pedal movement) have a compara- means of locomotion that can be mathematically modelled
tively short and broad foot. Miller (1974a) e xamined the perso- (e.g., Chan et al. 2005; Iwamoto et al. 2014).
nid Distorsio anus which had non-leaping type 2 discontinuous Chitons have a broad foot and move using muscular waves,
locomotion (arrhythmic terminating waves) and a broad, short but in gastropods there is a considerable variety of foot shape
foot, but had a broader shell than species with type 1. The leap- and the type of movement employed. While some creep on a
ing strombids have a foot smaller and narrower than the shell broad foot, in others the foot is narrow and more agile. In a few
than in other species (Miller 1974a). cases, the operculum is used to assist locomotory m ovements,
Some species with type 1 discontinuous locomotion (nota- the most famous being the leaping of strombids (see below).
bly Terebridae) are very effective burrowers (Miller 1974a). Pedal waves may be retrograde (moving in the opposite
Type 2 discontinuous locomotion, including leaping, is char- direction to the animal) or direct (moving in the same direction
acteristic of species with a large, broad shell and a small foot as the animal). The waves may be monotaxic (waves extend-
(e.g., Strombidae, Xenophoridae, Distorsio). The shell pro- ing horizontally across the foot) or ditaxic (in two series which
vides a wide, flat, stable base which reduces the possibility alternate on either side of the foot). These waves can be formed
of it tipping over. Animals without these shell modifications, either solely by differential contraction of muscles or a combi-
such as immature Strombus gigas, are unstable on sand, mak- nation of muscles acting in concert with blood spaces.
ing their movements much less efficient than in mature indi- Retrograde waves begin with the extension of the anterior
viduals (Miller 1974b). end of the foot, and the wave then moves backward along the
foot by the anterior muscles which form the wave contract-
ing and those behind stretching backward (see Figure 3.32).
3.10.3 Rhythmic Muscular Locomotion In direct waves, the opposite occurs, with the wave com-
mencing posteriorly and contraction at the anterior edge of
and Adhesion
the wave. For these reasons, retrograde waves are known as
Rhythmic muscular locomotion is broadly distributed ‘waves of elongation’ and direct waves are known as ‘waves of
among gastropods (Table 3.4). In many taxa, locomotory compression’ (Lissmann 1945; Miller 1974a; Trueman 1983).
waves on the creeping sole are used together with adhesion Thus with direct waves, movement is achieved by parts of the
(see Section 3.3.2.1), which also provides anchorage during sole being attached to the substratum at maximum extension,
the movement of other parts of the foot (see Figure 3.31). and forward movement occurs when the remainder of the foot
Chitons and gastropods use the special properties of their is shortened. With retrograde waves, the foot is anchored by
pedal mucus in conjunction with pedal waves – a locomo- regions at their shortest length, and forward movement occurs
tory method known as adhesive locomotion (Denny 1980a, with the sole maximally extended.
zone of dorso-ventral transverse zone of

contracting muscles pedal muscles pedal muscles relaxing muscles
viscous mucus fluid mucus substratum haemocoelic space
FIGURE 3.31 A diagrammatic representation of the employment of muscles in the formation of a retrograde wave in the patellogastropod
Patella. Note the compression of the haemocoelic spaces and the mucus changing from viscous to fluid state under the raised part of the
pedal wave. Redrawn and modified from Trueman, E.R., The Locomotion of Soft-Bodied Animals, Edward Arnold, London, UK 1975.
DIRECT WAVE RETROGRADE WAVE

Direction of movement
1 1
elongating
2 2
contracting elongating contracting elongating

3 3
wave wave
4 4
5 5
NORMAL SPEED - one wave occurs on one side of foot RAPID SPEED - one wave at a time - twice as fast
at one time
Method 1 Wave frequency doubles
Wave is one quarter length of foot
No change in wave-length
Wave forms in 2 sec 5mm - 1 sec

Wave travels length of foot in 10 sec Method 2 Wave-length doubles
No change in wave frequency
5mm - 2 sec
10mm - 2 sec
FIGURE 3.32 The upper figures show the two main pedal wave patterns in gastropods, direct waves (waves of compression), and ret-
rograde waves (waves of elongation). The lower figures show two methods of acceleration in vetigastropods. Redrawn and modified from
Miller, S.L., J. Molluscan Stud., 41, 233–261, 1974b.
Chitons and some gastropods have retrograde monotaxic generate waves smaller than those with retrograde waves and
waves while in a few other gastropods the waves are direct can thus achieve greater gripping power with a smaller foot
(Table 3.4). Retrograde ditaxic pedal waves are seen in patel- (Miller 1974a). Small direct waves are, for example, seen in
logastropods, some vetigastropods, and many caenogastro- many stylommatophorans and may be important when climb-
pods. In the caenogastropod land snail Pomatias, one side of ing as only a small part of the foot sole is released from the
the foot remains anchored while the other moves forward – substratum at any one time. Large waves do have advantages,
producing an almost bipedal gait. The retrograde ditaxic wave- despite reducing tenacity. Speed can be increased by increas-
form is associated with a large range of foot sizes and shapes, ing wave velocity or wavelength. In the first instance, the
and these waves are at least one third as long as the foot, while speed of contraction of the sole musculature must increase,
direct waves (and other waves of compression) are often much so the energetic cost is greater. If the wavelength is increased,
smaller and the range of foot shape is restricted, usually broad then it is unnecessary to increase the speed of contraction
(for high tenacity) or long and narrow. Compression waves (Miller 1974a).
can maintain high tenacity even when the animal is moving In species with retrograde ditaxic waves the size and shape
quickly because the waves can be very small and can travel of the foot is variable, but none have a foot longer than the
rapidly. Experiments by Miller (1974a) showed these small shell (Miller 1974a). Taxa with direct ditaxic waves have a
waves had greater adherence against shear forces than large large foot area, and some (e.g., some trochids) have a foot lon-
pedal waves. Those gastropods with direct waves appear to ger than the shell.
Direct monotaxic Direct ditaxic Retrograde monotaxic Retrograde ditaxic
Composite waves
FIGURE 3.33 The main kinds of pedal wave seen in the gastropod foot. Redrawn and modified from Trueman, E.R., Locomotion in mol-
lusks, pp. 155–198, in Salauddin, A.S.M. and Wilbur, K. M., Physiology, Part 1. The Mollusca, Vol. 4., Academic Press, New York, 1983,
the bottom row is redrawn and modified from Miller, S.L., J. Exp. Mar. Biol. Ecol., 14, 99–156, 1974a. See Figure 3.35 for their distribution
in gastropods. Composite waves are found only in cowries (Cypraeoidea). The small red arrows show the direction that the pedal waves are
moving, and the large red arrows show the direction of movement of the animal. In the figures in the top row, the animal is moving toward
the top of the page.
So-called composite waves are less common and seen in a forward movement, a single pattern of locomotion is usually
few gastropods such as cowries where the waves can move in employed, as is the number and size of muscular waves.
various directions. Modifications of these basic types can be Some burrowing gastropods, notably Naticidae and
recognised, and Miller in her study of ‘prosobranch’ locomo- Olividae, use monotaxic waves to burrow or increase speed
tion, recognised 14 kinds (Miller 1974a, b). Of all the mus- (Copeland 1919, 1922; Miller 1974a).
cular patterns observed in gastropods by Miller (1974a), she Polyplacophorans, patellogastropods, vetigastropods, and
considered the composite waves of cypraeoideans the most neritimorphs use only rhythmic pedal waves which move in
complex, enabling them to move quickly and turn easily with- regular parallel bands from one end of the foot to the other.
out reducing the amount of sole attached to the substratum. The amplitude of the rhythmic waves during normal for-
Taxa with composite wave patterns have similar foot sizes and ward locomotion is low, and all parts of the sole not within a
shapes when compared to species with direct ditaxic waves wave at any moment remain stationary and are usually firmly
(Figure 3.33). attached to the substratum (Miller 1974a).
If the main shell muscles in the foot cross, the locomotory Lower caenogastropods have a wide diversity of wave
wave is ditaxic, whereas if they remain separate the wave is types, but diagonal ditaxic waves are only found in some neo-
monotaxic (Figure 3.34). gastropods. Other neogastropods use a variety of wave types,
The type of locomotion reflects both phylogeny (see but many groups primarily use cilia.
Figure 3.35) and habits. In addition, a species may use one pat- Small-sized ‘pulmonates’ use either ciliary movement or
tern for forward movement, but, for an increase in speed, it can monotaxic waves and the larger basal ‘pulmonates’, onchi-
modify the normal pattern. Some species use a different pattern diids, and stylommatophorans all have direct monotaxic
of locomotion for escape, reversing, or climbing, but for normal waves.
Tenacity in gastropods is not just passive adhesion, but is

pedal an active process involving muscular action. Maximum adhe-
muscles sion is usually attained when an animal stops moving and
clamps its shell tightly against the substratum. Stationary
caenogastropods usually have the propodium retracted and,
although tenacity is greatly enhanced because of a change
Patellogastropod in the nature of the secreted mucus (see Sections 3.26 and
Ditaxic pedal waves 3.26.1), the total foot area in contact with the substratum is
less than when crawling.
Some patellogastropods, once dislodged, will not reattach

pedal
wave for several minutes. Once reattached, tenacity is poor at first,
but increases with the time that the limpet remains stationary.
The strength of pedal adhesion in patellogastropod limpets can
sole of exceed the strength of attachment of the muscles to the shell.
foot Fissurellid and siphonariid The highest stationary tenacity recorded by Miller (1974a) was
Monotaxic pedal waves 2.8 kg/cm2 for Lottia pelta, while Aubin (1892) found that a
Patella vulgata with a foot area of 2.9 cm2 resisted pulls of up
FIGURE 3.34 A diagrammatic representation of how shell muscle to 4.8 kg/cm2, but figures of as much as 5.2 kg/cm2 have been
interactions determine whether the pedal waves will be mono- recorded for other limpets (Branch & Marsh 1978). Smith (1992)
taxic or ditaxic. Figures on left show the pedal waves on the sole, found that lottiid limpets in the eastern Pacific switched between
those on the right are transverse sections through the foot s howing
suction and adhesion attachment depending on tidal height.
the musculature (blue). Redrawn and modified from Voltzow, J.,
Gastropod pedal architecture: Predicting function from structure
During high tide about three-quarters of the limpets used suction,
and structure from function, pp. 83–84, in C. Meier-Brook, while about the same percentage used adhesion during low tides,
Proceedings of the 10th International Malacological Congress, although mean tenacity was less at high tide than at low tide.
Tübingen, 27 August – 2 September 1989, University of Tübingen, Miller (1974a) experimentally investigated the factors
Tübingen, Germany, 1992. determining the tenacity of a snail or limpet. These include:
(1) direction of the dislodging force; (2) whether the animal is
moving or stationary; (3) whether the force is sudden or grad-
ual; (4) how long it is applied; and (5) the substratum type and
In detached caenogastropods, the propodium (with its texture. Differences between taxa include the size of the foot
associated anterior pedal gland) is used to initiate reattach- and the locomotory patterns. Those with continuous pedal
ment with the rest of the foot being applied subsequently. muscular locomotion have high tenacity, especially when sta-
In contrast, some vetigastropods (e.g., Haliotis, Trochus) and tionary, while those with ciliary action or discontinuous loco-
patellogastropods can readily attach any part of the sole when motion (including leaping) have very low tenacity. Similarly,
righting themselves (Miller 1974a). species with broad feet tend to have tenacity higher than those
Looping using the foot and snout is seen in species of with narrow feet. The optimal foot for high tenacity is broad
Truncatellidae, and in some Assimineidae and Pomatiopsidae. and slightly less than the length of the shell so the shell can be
In this mode of progression, the anterior end of the snout is clamped tightly against the substratum for maximum adhesion.
used along with the foot to practise a looping mode of pro- Other factors such as musculature and the nature and distribu-
gression (Figure 3.36) (Fretter & Graham 1962; Davis 1967). tion of pedal glands presumably also play an important role.
Some strombids also practise a similar mode of progression The requirements for speed and tenacity conflict, and max-
that may sometimes involve the snout (Berg 1974; Solem imum tenacity is usually achieved only when the animal is
1974) (Figure 3.36). stationary, but experiments with the trochoidean vetigastro-
pods Calliostoma and Tegula by Miller (1974a) imply that, at
least in those rather narrow-footed taxa, speed can increase
3.10.4 Adhesion and Tenacity
without affecting tenacity against shearing forces if wave pat-
Tenacity is important if chitons, snails, or limpets clamping tern or the method of movement do not change.
onto rocks are to withstand wave action and currents and The experiments of Miller showed that the optimal wave
to discourage predators. Two mechanisms are involved in pattern is a compromise between speed, energy efficiency,
tenacity – suction and adhesion (see also Sections 3.26 and and tenacity. Direct waves and other waves of compression
3.26.1). With suction, a space is formed under the foot to cre- have greater tenacity than retrograde ditaxic waves of elonga-
ate a negative pressure when pull is exerted. Adhesion is the tion because they are typically smaller and closer together.
force holding together two closely applied surfaces with a Thus, where both speed and tenacity are needed, rhythmic
thin layer of liquid between them. Adhesion is generally pos- pedal waves are optimal because the waves move quickly over
sible because the foot sole can closely conform to the shape of the sole while much of it remains firmly attached, enabling
most surfaces, and the thin layer of adhesive pedal gel greatly good adhesion. In contrast, long rhythmic waves (which move
increases its adhesive capabilities. a large proportion of foot area at once) probably require less
POLYPLACOPHORA
VETIGASTROPODA
PATELLOGASTROPODA
Trochoidea
Haliotoidea
Fissurelloidea CILIARY
CILIARY
NERITIMORPHA
Architaenioglosssa
Cerithioidea
Rissooidea
Eulimoidea
Epitonioidea
Triphoroidea
CAENOGASTROPODA
Littorinoidea
Naticoidea
Stromboidea
Xenophoroidea
Calyptraeoidea
Velutinoidea
Cypraeoidea
Tonnoidea
Buccinoidea
Muricoidea
Olivoidea
Pseudolivoidea
Conoidea
Cancellarioidea
Valvatoidea
Acteonoidea LEAPING
Nudipleura
HETEROBRANCHIA
Aplysiida
Cephalaspidea
Pyramidelloidea
Siphonarioidea
Sacoglossa
Hygrophila
Ellobiida
Stylommatophora
Systellommatophora
FIGURE 3.35 Pedal wave patterns in polyplacophorans and gastropods based mainly on data from Miller, S.L., J. Exp. Mar. Biol. Ecol.,
14, 99–156, 1974a. See Figure 3.33 for key to locomotor types. Note: Rissooidea = Rissooidea + Truncatelloidea.
energy than small, rapid waves achieving the same speed, but conducted by Miller (1974a) determined that the optimal foot
tenacity is much reduced. form for high tenacity were ratios of shell length/foot length
Because the modes of locomotion differ considerably in of about 1.5 and foot length/foot width of between 1.1 and 1.5.
the mechanism employed, they might be expected to differ This appeared to be due to two factors. Tenacity is approxi-
in mechanical power, but no one major type of locomotion is mately proportional to foot area, but if foot size is equal to or
restricted to species of small or large size. The experiments exceeds shell size, tenacity is much reduced. Limpets have
Truncatella
snout
foot operculum
Snout starting to extend Snout extended Snout contracted

and gripping substratum and foot brought
forward to its base

Strombus
operculum foot snout
Operculum embedded, shell and Posterior foot dragged forwards and Foot and snout make
head-foot thrust forwards operculum re-embedded. contact with substratum
Snout thrust forwards
FIGURE 3.36 Looping and utilisation of the snout in locomotion in the caenogastropods Truncatella and Strombus. Truncatella redrawn
and modified from Fretter, V. and Graham, A.L., British Prosobranch Molluscs: Their Functional Anatomy and Ecology, Ray Society,
London, UK, 1962; Strombus redrawn and modified from Solem, A.C., The Shell Makers. Introducing Mollusks, John Wiley & Sons,
New York, 1974.
by far the greatest strength of adhesion when stationary, and cemented to a hard substratum. Others need to move rather
Miller (1974a) suggested that tenacity may be increased by quickly for feeding, to reach shelter, to find mates, or to
the short shell muscles. If, as in snails, shell (i.e., columellar) avoid predators.
muscles must curve to reach the outer edges of the foot, much In gastropods with ciliary locomotion, speed is corre-
of the pull would be parallel to the substratum, not vertical lated with the rate of ciliary activity (Copeland 1919), but,
to it as in limpets. This may in part explain the adoption of a in taxa employing muscular locomotion, speed is a function
limpet-shape by many intertidal gastropods. The maximum of the size and frequency of the pedal muscular waves (see
pull by the shell (or columellar) muscles can only be exerted if above), or, in a few, the whole foot can be employed in a
the foot is smaller than the aperture, allowing the shell to be ‘step’ with discontinuous (including leaping) locomotion
pulled against the substratum. (Miller 1974a).
While optimal foot size and shape, and the type of locomo- Many species with rhythmic pedal waves merely increase
tion employed for high speed and high tenacity, are not com- the size of waves at greater speeds, while others can increase
pletely compatible, both attributes can be maximised to a high speed without altering the pattern. For example, the speed of
degree because the foot size and shape optimal for both are two trochoidean vetigastropods studied by Miller (1974a) dou-
similar. Thus, most species in exposed habitats studied by bled when they made contact with a starfish (from about 0.8 to
Miller (1974a) moved rapidly and clung tightly. Miller showed 1.4 mm/sec and 1.2 to 2.9 mm/sec, respectively). They did this
experimentally that the type of foot ideal for clamping is by increasing the number and frequency of waves and the size
less flexible and at a marked disadvantage on more complex of the steps. While the sizes of steps increased linearly with
topography compared with those with a long, flexible foot. speed in both species, Calliostoma with retrograde ditaxic
Miller (1974a) demonstrated that many gastropods, unlike waves, whose mean foot length was greater, took larger steps
most other animals, have no difficulty climbing Teflon coated than Tegula (with direct ditaxic waves) at any speed, while
vertical surfaces whether submerged or in air. Tegula had a greater wave frequency. An increase in wave-
length with an increase in speed is common in gastropods,
especially in those with retrograde waves. Wave frequency
3.10.5 Speed of Locomotion
probably increases mainly because of an increase in wave
Cephalopods are the fastest molluscs and are discussed under velocity, and not by a change in the spacing of the waves.
jet propulsion below (see Section 3.10.9.1). Similar changes occur in a terrestrial slug (Limax), which
In gastropods, the speed of movement with normal pedal has 11–19 direct monotaxic waves on the sole at any one time
locomotion (for alternatives see below) differs consider- (Crozier & Pilz 1924). Thus, this method of increasing speed
ably between taxa. Some have little need to move much may be typical of gastropods with rhythmic pedal waves
and some (vermetids and hipponicids) are permanently (Miller 1974a).
even between distantly related taxa – for example, both types

TABLE 3.5 occur in the Trochidae and Muricidae in species of similar
Heat Map of Maximum Gastropod Speeds Parsed by size, and those with direct waves moved significantly faster
Locomotory Mode and Shell Size. Median Values for than those with retrograde waves. Relatively high speeds were
Size and Mode also Given also regularly found in species with direct monotaxic waves
which employed waves of compression, so they had a com-
Locomotory Mode <15mm 15–40 mm 41–80 mm >80 mm Mode posite pattern.
Medians
Monotaxic
Several factors were identified by Miller (1974a) as impor-
tant in determining crawling speed. These were wavelength
Retrograde
and foot size and shape and its relationship with shell size,
Direct
both of which are discussed below.
Ditaxic
Wavelength – rapidly moving species with retrograde
Retrograde ditaxic waves usually had a wavelength equal to or greater
Direct than half the foot length, while in species with direct ditaxic,
Composite the wavelength did not increase more than the normal 1/5 to
Arrhythmic 1/3 foot length. In theory, if the speed of contraction + con-
Terminating waves
traction per unit sole area + the time between successive waves
are all equal, an animal with longer waves should move faster
Indistinct
as each wave would cause a larger forward step, but such fac-
Discontinuous
tors are usually not equal. Thus, among trochids and some
Type 1
muricids, Miller (1974a) found that species with direct waves
Type 2 moved faster even though many had shorter wavelengths.
Leaping Loping (sometimes called galloping) occurs intermittently
Ciliary in some stylommatophoran land snails and at least one species
Size medians of arionid slug (Pearce 1989). In this method of locomotion,
the head is lifted from the substratum and thrust forward.
It touches the substratum, but a low arch is formed behind and
Slow Fast
the rest of the body is then moved forward to this new point
Source of data: Miller, S.L., J. Molluscan Stud., 41, 233–261, 1974b. of contact (Figure 3.37). More than one arch may be pres-
ent at any one time. This method of progression is not mark-
edly faster than regular gliding. It thus differs from galloping
Miller (1974a) recorded speeds ranging from 0.1 to in the sea hare Aplysia which is a distinct type of retrograde
37.2 mm/sec (Strombus) within gastropods (Table 3.5). locomotion faster than crawling (Parker 1917; Pearce 1989).
Overall, leaping locomotion was by far the fastest. Leaping is Foot size and shape and its relationship with shell size –
dynamic because the power of the entire head-foot and colu- in medium to large species with continuous muscular pedal
mellar muscle complex (dorsal-ventral) are involved in each locomotion, those with a foot length equal to shell length had
step, and the distance travelled with a single contraction is the highest speeds. As the foot becomes shorter than the shell
potentially much greater than that with muscular pedal waves. or when foot length exceeds shell length, maximum speed is
In general, taxa with ditaxic waves are capable of fairly high reduced. Species with discontinuous locomotion (leaping) are
speeds, and their tenacity exceeds that of other taxa regardless different – in Strombus the narrow foot is 1/2 to 1/3 the shell
of the type of locomotion. Larger taxa with ditaxic waves may length, yet locomotion is rapid. In those that rely on ciliary
be slower than those that use leaping locomotion, and small- action, the foot in the most rapid movers is at least as long as
sized ditaxic movers (<15 mm) are also slower than those of the shell and is often (but not always) broad.
similar size with ciliary locomotion. There is relatively little data for the ‘minor’ classes on
Ciliary movement was performed consistently well over locomotory speed. Aplacophorans are very slow-moving and
all sizes. Rhythmic wave patterns, especially ditaxic, also either crawl on their cnidarian food or burrow in soft sediment
performed well at larger sizes, as did those with a composite (see Chapter 14). Chitons are generally slow crawlers, moving
pattern unless size exceeded 80 mm. In contrast, arrhythmic rather like a gastropod limpet. Some species of Ischnochiton
muscular locomotion (other than leaping), was slow, with that live on the undersides of rocks can move relatively rap-
arrhythmic terminating waves generally performing better idly away from light when the rock is overturned and move at
than indistinct arrhythmic locomotion and either type of dis- speeds around 10 cm/min (Boyle 1977).
continuous locomotion (Table 3.5). Scaphopods and many burrowing bivalves can quickly bur-
Direct and retrograde ditaxic patterns were close in row downward into the sediment, but cannot move efficiently
the maximum speeds attained for animals of similar size. laterally, and some shallow-burrowing bivalves can readily
Taxa with retrograde ditaxic waves exhibited a wide range move laterally by ploughing through the sediment. Some cock-
of speeds, and those with direct ditaxic waves more con- les (Cardiidae) use their long muscular foot to actively leap
sistently showed higher speeds (Miller 1974a). This is true away from predatory starfish (Morton 1964; Ansell 1967b;
Creeping gait Galloping gait
FIGURE 3.37 Different modes of locomotion in a terrestrial helicid snail. Redrawn and modified from Lissmann, H. W. J. Exp. Biol., 22,
37–50, 1945 (figures on left), and Gray, J., Animal Locomotion, Norton, New York, 1968 (figures on right) as reproduced in Kandel, E.R.,
Behavioral Biology of Aplysia: A Contribution to the Comparative Study of Opisthobranch Molluscs, W. H. Freeman & Co., San Francisco,
CA, 1979.
negative
stimulus
FIGURE 3.38 Leaping movement of the cardiid bivalve Laevicardium crassum. Redrawn and modified from Morton, J.E., Locomotion,
pp. 383–423, in Wilbur, K.M. and Yonge, C. M., Physiology of Mollusca, Vol. 1, Academic Press, New York, 1964.
Yonge & Thompson 1976) (Figure 3.38). Similar leaping locomotion. Hard and soft substrata provide very different
movements have been observed in several other bivalve taxa surfaces and topographical complexity can necessitate com-
(Ansell 1969), including Gari (Ansell 1967a), and are assumed plex movements such as climbing and turning.
to be possible in Neotrigonia (e.g., Ansell 1969) because of Experimental work carried out on marine gastropods by
similar foot morphology. The fastest-moving bivalves are the Miller (1974a) investigated how substratum and topography
swimming scallops (see Section 3.10.9 and Chapter 2). influenced their form and locomotion.
The responses of patellogastropod limpets to starfish and Differences in the substratum. The experiments that Miller
other predators have been well studied with some moving (1974a) conducted showed that taxa living on soft substrata
away (e.g., Phillips 1975), others twisting (e.g., Bullock 1953), tend to use ciliary locomotion or arrhythmic discontinuous
and some even attacking the predator (e.g., Branch 1979). waves and those on hard substrata use rhythmic pedal waves.
Those that live on both tend to use arrhythmic waves. Species
with ciliary, leaping, or discontinuous locomotion move effi-
3.10.6 The Effect of Substratum and Topography
ciently on soft substrata and on horizontal hard surfaces,
on the Locomotion of Gastropods
although with their leaping movement strombids are ineffi-
Substratum type and topography are often variable and cient on smooth hard surfaces, as are species with discontinu-
changes experienced by an animal can present problems for ous locomotion and poor tenacity (Miller 1974a). To climb
vertical, smooth, hard surfaces, species with discontinuous and contrasts with narrow-footed relatives living on hydroid
and leaping locomotion usually adopt an indistinct arrhyth- colonies (Robilliard 1970). The foot of several species of cili-
mic movement. In strombids, this is possible only on the ary movers that burrow (e.g., the caenogastropods Olividae,
adhesive anterior part of the foot, but large individuals are Naticidae, and several shelled ‘opisthobranchs’) envelops
typically unable to climb. While species employing ciliary some or all of the shell, and burrowing is assisted by pedal
movement can usually climb hard surfaces, smooth surfaces cilia moving sand dorsally over the shell (see also below).
can cause slippage. Taxa with high tenacity are found on hard substrata, and
Most species with muscular pedal waves generally move those with minimal tenacity usually on soft substrata, while
most effectively on hard surfaces. Miller (1974a) tested the taxa with intermediate tenacity are less restricted. All ciliary
speed on sand of several gastropod species which normally movers whose tenacity was measured by Miller (1974a) were
live only on hard substrata and found those with high locomo- sand-dwellers; taxa associated with hard substrata that pre-
tor tenacities (see below), such as patellogastropods and the sumably employ ciliary motion (e.g., Velutinidae, Triviidae)
neogastropod Nucella manage poorly on sand, whereas most were not tested.
of the others from hard substrata had no difficulty, irrespec- There are also some patterns of locomotory types with a
tive of locomotory wave pattern. Thus, various muscular wave preference for intertidal or subtidal environments and wave
patterns can be employed for movement on sand, except for exposure. Dislodgement by the forces generated by breaking
those that employ firm adhesion. waves is probably an important selective agent for intertidal
Topology. Species with a relatively long, narrow foot gen- snails (Denny 1985; Denny et al. 1985; Wright & Nybakken
erally proved to be the most capable of manipulating them- 2007). The risk of dislodgement can be reduced by a smaller
selves over complex surfaces. Species with a broad foot rarely or flatter shell, streamlining, and reduction of the projected
turn more than 90 degrees at once and to achieve even that surface so that lift is reduced, and increased adhesive strength
angle much of the foot area had to be detached. A large shell by way of a larger foot area or increased tenacity (see also
can be a hindrance on complex topography unless the foot is Denny 1988).
very flexible, and it is certainly a disadvantage on vertical or In the lower littoral or sublittoral, ciliary and discontinu-
overhanging surfaces due to the weight relative to the area of ous movers and closely related species with monotaxic pat-
adhesive foot surface. terns dominate, while on wave-exposed sandy beaches the
taxa present (often Olividae) are usually burrowers. Most taxa
on soft substrata are found in sheltered shores where reduced
3.10.7 Correlation with Habitat
wave action and inland drainages allow for the accumulation
Miller (1974a) showed that different locomotor types were of deep sediments. Those that leap and those with other dis-
strongly correlated with the environment in which they live, continuous locomotion were also consistently found low on
as summarised below. the shore or in the sublittoral.
In relation to the substratum, retrograde, direct ditaxic, and Species in the higher tidal zones of the more exposed
composite patterns are mainly found in species on hard sub- shores are relatively fast-moving and have rhythmic, ditaxic
strata, while those with ciliary and discontinuous locomotion pedal waves. Small pedal waves are found in only a few spe-
are mostly on soft substrata. Species with monotaxic waves cies in such situations with most taxa in the highest zones
present on soft substrata are members of families primarily (littorinids, planaxids, neritids, and several muricids) typi-
using ciliary locomotion (Naticidae and Olividae). Almost cally moving with a large pedal wave (≥1/3 foot length).
half the species with distinct arrhythmic terminating waves The marine panpulmonate limpet Siphonaria has initially
and indistinct arrhythmic locomotion occurred in sand or small waves, but the entire back of the foot then moves for-
mixed sand/rock habitats. ward at once. The patellogastropod lottiids and the vetigas-
Ciliary and discontinuous locomotion are primarily found tropod Tegula have a normal wavelength about l/3 of the
in vetigastropods and caenogastropods associated with soft foot length, but can increase this to increase speed. Various
substrata and both have low tenacity. Taxa with arrhythmic muricids living on exposed hard shores have short direct
terminating waves and continuous indistinct arrhythmic pedal waves, thus maintaining a large area of the foot stationary
movement tend to inhabit mixed substratum habitats or soft to increase adhesion. This same pattern is seen in abalone
sediments exclusively. Some of those with continuous indis- (Haliotis spp.) which also live in exposed lower littoral and
tinct arrhythmic pedal movement have a large foot, like that sublittoral habitats. Others with narrow waves include many
seen in ciliary or discontinuous movers, yet these foot shapes species of cypraeids which often hide underneath rocks etc.,
are not essential for effective movement. Similarly, most spe- and trochids which have a long, relatively narrow foot and
cies with ciliary locomotion have a much larger foot area thus a low tenacity.
than necessary for effective propulsion. This suggests that the Foot size and shape also show some correlation with envi-
enlarged foot serves other functions, for instance, burrowing ronmental factors. Many species with foot proportions for
and/or for stability on loose substratum. It has been suggested high tenacity occur on the upper parts of exposed shores,
that the massive foot of some Naticidae is used in prey capture while species with proportions outside the range for high
and even transport (Gonor 1965). A similar enlargement of the tenacity usually occur in lower, less exposed zones. While a
foot is seen in the mud-living nudibranch Dendronotus iris larger sole size can equate with increased adhesion, improved
adhesion can also be increased by the properties of the pedal

mucus (see Section 3.3.2.1). Species with arrhythmic locomo-
tion are found only in the low zones and often confined to
sheltered habitats and microhabitats. These and other spe-
cies with unsuitable foot proportions for effective tenacity are
mainly found in protected microhabitats.
Despite some generality with the patterns found by Miller
(1974a), intraspecific differences always occur. In a more
recent study of two intertidal snails in South Australia, Prowse
and Pile (2005) found no differences in individuals from shel-

tered and exposed sites other than a reduction in overall size
in both species, possibly indicating that smaller individuals
may gain access to refuges more effectively.
3.10.7.1 Burrowing in Soft Sediments

Caudofoveate aplacophorans burrow in soft sediment, but Heterodont bivalve
their movements are slow. Burrowing is achieved by the ante-
rior end (with the oral shield) being pushed into the sediment
hydrostatically and, with the long posterior spicules acting
as an anchor, contraction of the longitudinal muscle bands
along the body bring the posterior end forward (Scheltema
1998). Most solenogasters do not burrow, but some spe-
cies of Neomenia can do so using their protrusible pharynx
(Scheltema 1998).
Polinices (Naticidae)
The foot is modified for burrowing in many bivalves, some
gastropods, and in all scaphopods. In burrowing gastropods, direction of foot water flow direction of shell
expansion and rotation
the foot is usually dorsoventrally flattened into a plough-
contraction
shape, often with extensions from the sides of the foot or the
mantle edges to streamline the body so that the animal can FIGURE 3.39 Comparison of the burrowing mechanism in a het-
plough into and through the substratum, lubricated by mucus. erodont bivalve and a naticid gastropod. Bivalve redrawn and modi-
Although many burrowing gastropods use ciliary action, fied from Trueman, E.R. et al., J. Exp. Biol., 44, 469–492, 1966;
muscular pedal waves appear to be more effective, especially naticid from Trueman, E.R., J. Exp. Biol., 48, 663–678, 1968.
in larger species such as in many naticids (Copeland 1922)
(Figure 3.39), the nassariid Bullia melanoides (Ansell &
Trevallion 1969), and the olivid Agaronia (Cyrus et al. 2012). Downward movement can also be facilitated by a jet of water
Pedal waves are developed in some caenogastropod taxa from the mantle cavity into the surrounding sediment as the
where close relatives have ciliary action alone, and they differ shell is rapidly closed (Figure 3.40). The shell is then dragged
from the waves seen in many other caenogastropods in being through the softened sediment by the foot. Digging can also
long (1/3–1/2 foot length) and monotaxic. Some other bur- be assisted by a rocking motion caused by the alternate con-
rowing gastropods such as the Terebridae are very effective traction of the pedal retractor and protractor muscles. Rocking
burrowers (Miller 1974a). does not occur in bivalves with elongate shells, but can be
In both scaphopods and bivalves the foot is highly adapted pronounced in some with rounded shells. Upward movement
to effectively and efficiently penetrate the sediment using is accomplished by pushing down with the foot.
hydrostatic pressure. In burrowing bivalves (Figures 3.39 and Besides the similar muscular hydrostatic burrowing mech-
3.40), the movements involve the adductor and foot muscles anisms seen in living molluscs, convergent features in some
and, while basically similar (Trueman et al. 1966), there are bivalves and gastropods include the development of large hae-
differences between taxa resulting from structural (includ- mocoelic cavities. In addition to copious blood spaces, naticid
ing the shell), physiological, and behavioural differences, gastropods have an ‘aquiferous pedal system’, which takes in
and differences in the properties of the sediment. Burrowing seawater to inflate foot sinuses and is expelled when the ani-
bivalves usually have a laterally compressed hatchet-shaped mal contracts into its shell (see Section 3.8.2). Many bivalves
or plunger-shaped foot. A hydraulic system is employed, and gastropods have also developed asymmetrical ‘ratchet’
involving haemocoelic fluid being forced into the foot by sculpture that aids in preventing back slippage and thus makes
muscle contraction. This expands the foot distally and anchors burial more efficient (see Section 3.2.10). Scaphopods have
the anterior part, enabling the animal to draw down on it a unique foot morphology with a fringed epipodium which
(Figures 3.39 and 3.40). The animal may also be prevented is expanded to obtain anchorage, followed by its retraction.
from being pushed upward by dilation of the upper part of Octopods and cuttlefish also burrow, and like bivalves, use
the body, usually by the shell valves being partially opened. sediment liquefaction to facilitate their burrowing. Octopods
ligament adductor shell

muscle valve
retractor
muscle
protractor
muscle
mantle
cavity
transverse
muscle
substratum
foot
Valves press against Adductor muscles contract; Retractor muscles contract

substratum; water ejected from mantle cavity; to pull shell down onto
foot thrusts downward cavity formed in surrounding substratum; foot and into substratum
high pressure in pedal haemocoel causes
dilation of terminal foot to form anchor
FIGURE 3.40 Diagrammatic representation (in transverse section) of the mechanisms involved in bivalve burrowing. Redrawn and modi-
fied from Trueman, E.R., Locomotion in mollusks, pp. 155–198, in Salauddin, A.S.M. and Wilbur, K. M., Physiology, Part 1. The Mollusca,
Vol. 4., Academic Press, New York, 1983.
use water jets from their funnel to liquify the sediment before home site depressions in calcareous substrata. The excavation
pulling themselves into the softened sediment with their process appears to involve both chemical dissolution and rad-
arms, which function as a muscular hydrostatic burrowing ular rasping (Lindberg & Dwyer 1983) (see also Chapter 9).
mechanism. Cuttlefish and sepiolids use water jets and their
fins to create a depression in which they cover themselves
3.10.8 Bipedal Locomotion
with sediment.
Some benthic octopuses move over sandy bottoms on two of
3.10.7.2 Burrowing in Hard Substrata their arms using a rolling gait (Huffard et al. 2005; Huffard
Some bivalves burrow into hard substrata (wood, clay, soft 2006). These octopuses bipedally ‘walk’ backward by alter-
rock, or in calcareous substrata such as living or dead coral, nating the placement of each arm on the substratum and
molluscan shells, or limestone). They achieve this by either then rolling along the sucker edge of the distal half of the
mechanical boring or chemical dissolution, or a combination arm. Walking behaviour also occurs in a few cuttlefish taxa,
of the two mechanisms, chemical dissolution being only pos- including Metasepia (Roper & Hochberg 1988). Bipedal
sible on calcareous substrata. locomotion is the fastest benthic mode of locomotion in the
Chemical borers such as date mussels (the mytilid molluscs with observed rates of 60 to 140 mm/sec, equal to
Lithophaginae) do this using acidic secretions from the man- or faster than the same individuals crawling (60 mm/sec)
tle, while mechanical borers use file-like sculpture on the shell (Huffard et al. 2005).
to rasp the substratum. Thus, pholadids and teredinids file the
soft rock or wood by rotating the shell back and forth while
3.10.9 Swimming
clamping onto the side of the borehole with their sucker-like
foot (Figure 3.41). More details on bivalve boring are given in Swimming occurs in some adult gastropods and bivalves,
Chapters 9 and 15. and most cephalopods; most bivalves and cephalopods swim
A few gastropods, such as the coralliophilid Magilus and by ‘jetting’ (see Section 3.10.7.1). In bivalves, it is achieved
the large vermetid Ceraesignum maximum live embedded by rapid closures of the valves in a clapping motion with the
in massive corals. They do not bore, rather, the coral grows water being expelled from the mantle cavity. Cephalopods
around them, and they produce a tube that maintains a con- also rapidly expel water from the mantle cavity, but much
nection with the exterior. A few other limpet-like gastropods more efficiently. In coleoids, the rapid contractions of the
(other than patellogastropods) including abalone, the hipponi- muscular mantle wall enable these animals to swim using jet
cid Sabia, some siphonariids, and Trimusculus also construct propulsion, and they can also swim by flapping their fins. Fins
FIGURE 3.41 Burrowing movements of a pholadid bivalve in soft rock. The green arrows show the movements of the shell, while the
red arrows indicate the movements of the foot. Redrawn and modified from Nair, N.B. and Ansell, A.D., Proc. Malacol. Soc. Lond., 38,
179–197, 1968.
provide balance and propulsion in squid, cuttlefish, and some expelled from the mantle cavity. A few bivalves can swim for
finned octopuses. Fin swimming is often used in conjunction short periods, but no adult bivalves are long-term swimmers.
with jet propulsion. Most swimming bivalves are pteriomorphians with a single
Swimming gastropods (Figure 3.42) use parapodia or large adductor muscle which rapidly closes the valves. Limids
a modified foot. Heteropods live permanently in the water such as Limaria fragilis (Donovan et al. 2004) can swim
column and are efficient swimmers, using body movements for extended periods (15 min or more), while others, such as
like a fish. The gymnosome and thecosome pteropods are Limaria hians (Gilmour 1967) are capable of swimming for
also permanent members of the water column. The naked only a few minutes at most. Physiologically, the energy sup-
gymnosomes are predators on the shelled thecosomes, and plied for swimming is mostly aerobic, with a small anaerobic
Clione limacina and probably other gymnosomes can rapidly contribution from arginine phosphate, glycolysis, and ATP
change their normal swimming wing beat to much higher (Baldwin & Morris 1983). By way of contrast, scallops swim
speeds when involved in prey capture (Satterlie et al. 1985).
for short periods, and their swimming is largely powered
Pteropods all use a pair of parapodial ‘wings’ for swimming
anaerobically (Gäde et al. 1978; Grieshaber 1978; Livingstone
(see Gilmer & Harbison 1986 for references and details).
et al. 1981), although their swimming abilities vary consider-
In thecosome pteropods, differences in the external part of
ably. Some such as Chlamys can only swim for short distances
the mantle appear to be related to their flotation abilities
in a ‘zig-zag’ fashion, while others such as Amusium and
(Gilmer & Harbison 1986). Most cavoliniids have reduced
Placopecten are ‘long-range gliders’. Species of Amusium and
external mantles and sink slowly while feeding, but Diacria
and Cavolinia have complex mantles used for flotation and Ylistrum are the most efficient bivalve swimmers. Their thin,
in feeding. Limacina has no external mantle, but flotation smooth shells are strengthened by internal ribs, and they are
is assisted by their mucus-feeding webs. Swimming in the capable of speeds up to 1.6 m/sec and can cover distances of
pseudothecosome Peraclis reticulata, which has an external over 23 m in a single swimming event (Joll 1989). The vary-
mantle that covers the shell, is assisted by it being neutrally ing swimming abilities of scallops are determined by their
buoyant. shell morphology, including thickness, streamlining, and dif-
ferential convexity in the upper and lower valves (particularly
3.10.9.1 Jet Propulsion, Including ‘Flight’ pronounced in Pecten) to generate lift (e.g., Hayami 1991).
As noted above, in most bivalves jetting is achieved by rapid Allometric changes in shell thickness, shape, and in adductor
closures of the valves in a clapping motion with the water being muscle size also play a role (e.g., Gould 1971).
Akera
Aplysia
Limacina
Hexabranchus
FIGURE 3.42 Different swimming techniques employed by some heterobranch gastropods. Redrawn and modified from the following
sources – Akera Morton, J.E., Locomotion, pp. 383–423, in Wilbur, K.M. and Yonge, C. M., Physiology of Mollusca, Vol. 1, Academic
Press, New York, 1964; Aplysia Thompson, T.E., Biology of Opisthobranch Molluscs, Vol. 1, Ray Society, London, UK, 1976; Limacina
Morton, J.E., J. Mar. Biol. Assoc. U. K., 33, 297–312, 1954; Hexabranchus Edmunds, M., Proc. Malacol. Soc. Lond. 38, 121–133, 1968b.
Swimming in limids is less well understood, but the as 21% in circumference (Ward 1972; Ward & Wainwright
behaviour and mechanics of swimming in Limaria fragilis, 1972; Packard & Trueman 1974) with no change in length.
and paddling by its long mantle tentacles, was described by This action squeezes water out of the narrow funnel with
Donovan et al. (2004). enough force to propel the animal at speed. Squid are the fast-
Cephalopods propel themselves using jet propulsion est marine invertebrates and, using jet propulsion, the squid
achieved with a powerful contraction of the mantle muscles. Illex can achieve maximum speeds of around 1.4 m/sec, com-
Water flows through the anterior opening into the mantle cav- pared with Sepia at 0.65 m/sec, and Nautilus at 0.3 m/sec
ity and over the gills. The mantle builds internal pressure (O’Dor & Webber 1991).
by sealing off the opening except for the funnel. The thick While most of the propulsion and steering in cephalo-
muscles of the mantle wall (see below) contract by as much pods originates with the funnel, some propulsion and fine
adjustments are made with the fins. Fins provide balance and Sulawesi (Bogan & Bouchet 1998), three genera of unionoide-
propulsion in squid, cuttlefish, and some finned octopuses, ans, Acostaea (from Columbia, South America), and Etheria
and are often used in conjunction with jet propulsion from the (from Africa and Madagascar) in the Mycetopodidae and
funnel. The funnel is directed forward to escape a predator, Pseudomulleria (from India) in the Unionidae, indicating that
so that the animal propels itself backward. By pointing the cementation has evolved at least twice in fresh-water mus-
funnel backward, forward movement is achieved, such as may sels (Bogan & Hoeh 2000). Also a very poorly known small
be required in prey capture. A few species of squid escape fresh-water caenogastropod snail Helicostoa (Helicostoidae,
from predators by propelling themselves out of the water and ?Truncatelloidea) from the Yangtze River, China, apparently
travelling through the air for distances up to 50 m (Heyerdahl cements its shell to the substratum (Pruvot-Fol 1937).
1950; O’Dor et al. 2013). Fins assist in stabilising ‘flight’ and Oysters are the best known cementing bivalves (e.g.,
allow the squid to glide above the surface of the water. A so- Yonge 1960b; Stenzel 1971), with the settling oyster juvenile
called ‘flying squid’, Ommastrephes bartrami, which often using a tanned mucopolysaccharide secreted by the foot for
swim in schools, have been observed ‘flying’ in groups of its initial attachment (e.g., Cranfield 1975). Almost immedi-
more than one hundred. The ‘hooked squid’ (Onychoteuthis) ately, spherulitic calcite cement is then deposited between the
and the ‘Humboldt squid’ (Dosidicus gigas), also known as periostracum and the substratum (Harper 1992). A similar
the ‘jumbo squid’, are also capable of becoming airborne, mechanism of cementation is rather widespread in bivalves,
with large adults of the latter able to swim briefly at speeds being found in spondylids, dimyids, cleidothaerids, and myo-
approaching 30 m/sec (Benoit-Bird & Gilly 2012), and chamids (Harper 1992, 1997a, 2012). Some may become
Sthenoteuthis pteropus up to 24.5 m/sec (O’Dor et al. 2013). secondarily detached (e.g., some oysters and chamids).
The extinct rudists (Late Jurassic to the Late Cretaceous),
3.11 PERMANENT ATTACHMENT formed extensive carbonate reefs along the shores of the
Supertethys (see Chapter 15).
TO THE SUBSTRATUM
Most vermetid gastropods cement to the substratum, but
Bromley and Heinberg (2006) reviewed attachment to the this is the only gastropod group that does so other than a few
substratum by living and fossil molluscs. Benthic animals siliquariids (e.g., Stephopoma) and the supposed truncatelloi-
in the wave-swept intertidal zone require at least temporary dean Helicostoa mentioned above, although hipponicids lay
grip on the substratum. For most gastropods and chitons, down a calcareous plate on the substratum to which they are
this is achieved by foot clamping (see Section 3.10.3), but attached by their foot (e.g., Knudsen 1991). Cementation also
for bivalves this is not an option. Many, especially intertidal, occurs in a wide variety of other invertebrates, including scler-
bivalves attach using their byssus or by cementing their shell actinian and octocoral corals, craniid brachiopods, and serpu-
to the substratum (see Chapter 15). The latter method is also lid polychaetes, although the mechanisms differ in detail.
used in a few gastropods. An increase in cementing bivalve taxa in the Early
Mesozoic may be related to a marked increase in predation
pressure (e.g., Vermeij 1987; Harper 1991). In experiments
3.11.1 Byssal Attachment
carried out by Harper (1991), predators preferred byssate
Byssal threads are secreted by a gland in the foot of autobranch bivalves to cemented ones, apparently because cemented prey
bivalve larvae, but this ability is lost in many adults. Byssal was more difficult to manipulate.
attachment is important for many adult pteriomorphians and
some heterodont bivalves. Unlike cementation, byssal attach-
3.12 MUSCLES AND THE MUSCLE SYSTEMS
ment is usually flexible and can often be transitory. Even in
species that will normally remain attached (such as mussels), Here we deal with the main body muscular system, which is
they are capable of movement along the shore by detaching derived from the mesoderm. The muscular system varies con-
and reattaching their byssal threads, including reattachment if siderably from class to class, but is usually related to the head-
dislodged, if conditions allow (Paine 1974). This is achieved foot, and its interaction with the shell(s). Another important
by the byssus being released at the byssal gland, allowing the set of muscles is associated with the buccal mass (except in
animal to creep to a new location using the (usually reduced) bivalves which lack a buccal mass), and these are dealt with
foot where it reattaches by secreting a new byssus. There is in Chapter 5.
evidence to suggest that byssal attachment strength may Before looking at the main muscle systems found in mol-
increase relative to wave energy (Witman & Suchanek 1984). luscs, we briefly outline below the structure of muscle cells and
More details on the structure and function of the byssus and some of their physiological features. Molluscan muscle sys-
its role in bivalve evolution are given in Chapter 15. tems are both diverse and distinctive and have been a research
focus for over 150 years. Besides detailed morphological and
physiological studies, molluscan muscles are being investi-
3.11.2 Cementation
gated for insights into the molecular basis of contraction and
A number of bivalves and gastropods, mostly in the marine its regulation (Hooper & Thuma 2005; Hooper et al. 2008).
environment, can cement their shells to the substratum. Movement nearly always requires muscular action with
A few fresh-water taxa also cement, including a cyrenid from the energy needs scaling with increases in body size, velocity,
and mode of movement. Generally, large fast-moving animals systems of molluscan muscle are outlined below, both of
require large amounts of energy, and small, slow-moving ani- which rely on finer scale TEM micrographs, although the
mals require small amounts. Muscle tissue occupies a signifi- gross features such as the difference between striated muscles
cant component of the body mass – e.g., over 60% in Octopus and smooth muscles can be seen using a light microscope.
(Hochachka et al. 1983a), and in most other molluscs, it also Traditional schemes classifying muscle types were primarily
accounts for a large proportion of the body mass, with mus- based on the Z-lines or bodies and their alignment. All features
cles in the mantle, head, buccal mass, and many parts of the do not necessarily covary, and each component of the muscle
gut, heart, etc., and particularly the foot. Thus, for molluscs, cell is related to an aspect of muscle function. Another example
as for many other animals, muscular work represents one of of a classification of muscle types was developed by Nicaise
the main, if not the main, energy demand. Energy and oxygen and Amsellem (1983) and involved scaling six individual com-
sources for muscles are crucial for their efficient work, and ponents of molluscan muscle. It is summarised as follows.
this aspect of muscle physiology is outlined in Chapter 2.
• ‘Z’ parameter – ranges from Z1 with continuous
Z-bands, as in cross-striated muscle, to Z5, the random
3.12.1 Muscle Cell Morphology
arrangement of dense bodies seen in smooth muscle.
Chantler (1983) described the structure and biochemistry of • ‘L’ parameter – the length of the thick filaments (an
molluscan muscles. They are unicellular, composed of elon- indicator of contraction speed). This parameter is
gate cells, and their thick and thin filament organisation is less difficult to measure using TEM because of the length
ordered than that seen in most vertebrate muscles. In all mol- of the filaments (Voltzow 1994).
luscan muscles, the core of the thick filaments is p aramyosin • ‘F’ parameter – diameter of the thick filaments, a
which is surrounded by a layer of myosin molecules. It is feature readily measured in TEM micrographs.
this layering that gives the wide range of fibre diameters • ‘M’ – the organisation of mitochondria ranging
and produces fibres much longer than those of vertebrates. from rare (M1), generally present in the plane of a
Paramyosin is broadly distributed among invertebrates and is TEM section (M2), or arranged in packages (M3).
thought to stabilise and extend the myosin filaments (Schmidt- Differences in the location of the mitochondria
Rhaesa 2007). Paramyosin may also be important in maintain- within the cell are not distinguished.
ing contraction at a low energy cost, as required, for example, • ‘T’ parameter – describes three categories of the
in the opaque white catch muscle of bivalve adductors (see penetration of tubular infoldings of the plasma mem-
Section 3.12.3.6) and heart muscle (Paniagua et al. 1996). brane into the myoplasm (the contractile portion of
There are also ‘vesicles’ that can be seen in sections of the cell) and is only superficially similar to the T
the muscle cells (Figure 3.43) that are sections through vari- system in vertebrates (Nicaise & Amsellem 1983).
ous intracellular tubules and plasma membrane invaginations • ‘R’ parameter – describes the condition of the sar-
(e.g., Heyer et al. 1973; Silva & Hodgson 1987). colemma (the cell membrane of the muscle cell), R1
Invertebrate muscle cells are generally divided into where subsarcolemmal cisternae (flattened mem-
three types – smooth, transversely (or crossed) striated, and brane discs that are part of the Golgi apparatus) are
obliquely striated, which are broadly distributed among the connected to a sarcoplasmic reticulum tubule sys-
Lophotrochozoa (Table 3.6). tem extending into the myoplasm, and R2, where
These distinctions are an over-simplification of the actual the sarcoplasmic reticulum is restricted to the cell
variation present in molluscan muscle. Two classification periphery.
vesicle dense
body
dense
body thin
filament
thick thick
filament filament
vesicle
thin
filament
2 mμ
Transversely striated heart Obliquely striated fast Smooth catch muscle fibre
fibre (e. g., Achatina and Sepia) adductor fibre from adductor (e. g., Mytilus)
(e. g., Crassostrea)
FIGURE 3.43 Representative molluscan muscle fibres in each of the three main muscle types. Each diagram represents a small portion of
a fibre. Redrawn and modified from Twarog, B.M., J. Gen. Physiol., 50, 157–169, 1967.
TABLE 3.6
Distribution of the Three Main Muscle Types in the Lophotrochozoa
Taxon Smooth Transverse (or crossed) Oblique
Brachiopoda ⚪ ⚪ ⚪
Phoronida ⚪ ⚪ ⚪
Mollusca ⚫ ⚪ ⚫
Echiura ⚪
Annelida ⚪ ⚪ ⚫
Sipuncula ⚪
Nemertea ⚪ ⚪
Platyhelminthes ⚫ ⚪
Bryozoa ⚪ ⚪
Cycliophora ⚪ ⚪
Entoprocta ⚪ ⚪
Acanthocephala ⚪
Rotifera ⚪ ⚪ ⚪
Micrognathozoa ⚪ ⚪
Gastrotricha ⚪ ⚪ ⚪
Gnathostomulida ⚪
Source of data: Schmidt-Rhaesa, A., The Evolution of Organ Systems, Oxford, UK, Oxford

University Press, 2007.
Note: ⚫ = Predominant, ⚪ = Present.
These parameters differ between and within taxa. For exam- muscles where articulated taxa have adductor muscles with
ple, the Z parameter can vary between 2 (Rossia, cephalo- both smooth and transverse muscle types, while lingulid bra-
pod), 2–4 (Achatina, gastropod), and 5 (Venus, bivalve), chiopods have adductors with smooth and obliquely striated
whereas in the heterobranch gastropod Lymnaea, the head muscle types (Kuga & Matsuno 1988; James 1997). Only
retractor, shell, and diagonal muscles differ in four of the six smooth muscles are reported from adductor muscles of most
parameters (Nicaise & Amsellem 1983). other bivalves (e.g., Matsuno et al. 1993) and in the columel-
The invaginations of the sarcolemma and elaborations lar muscles of a range of gastropods (Frescura & Hodgson
of the sarcoplasmic reticulum described by the T and R 1992). The shell muscles of limpet-like gastropods – patellids,
parameters are two of the most interesting and variable Haliotis, and Siphonaria – have smooth muscle unusually rich
features of molluscan muscles (Nicaise & Amsellem in intercellular collagen (Frescura & Hodgson 1990, 1992).
1983). Thus the ultrastructure of molluscan muscle cells Most treatments of molluscan muscles categorise them into
reveals a much more complex situation than just the three three main muscle types, as seen in Figure 3.43. The follow-
categories discussed below (Nicaise & Amsellem 1983), ing account is largely based on the review by Paniagua et al.
with differences in the striations due to the ultrastructural (1996).
organisation of Z-discs and dense bodies. The latter are the
functional equivalent of the Z-line or Z-discs in vertebrate 3.12.1.1 Smooth Muscle Cells
striated muscles and are found in all molluscan muscles. Smooth muscle is the main type found in molluscs, bra-
The speed of contraction of the muscle cell is linked to chiopods, and many other animals, but is absent from
the number of contractile filaments in the cell. When mov- arthropods. The cells are fusiform with a central nucleus.
ing along a gradient of striated to smooth, the contraction Invertebrate smooth muscle differs from that of vertebrates
speed decreases, but the ability to maintain sustained ten- in having more and thicker myofilaments, but is otherwise
sion increases. superficially similar with the thick and thin filaments show-
Importantly, a single muscle mass may comprise differing little order in their arrangement (Paniagua et al. 1996).
ent kinds of muscle cells so the mix of muscles determines The force exerted by the muscle cell is related to the number
the performance (Voltzow 1994). For example, Matsuno and of thin and thick filaments per unit area and the endurance
Kuga (1989) reported that the translucent part of the adduc- to the number of mitochondria, while the speed of relax-
tor muscle of Tridacna crocea consisted of obliquely striation is determined by calcium availability (Plesch 1977).
ated muscles and the opaque part of two types of smooth Smooth catch muscle cells from the anterior adductors of the
muscle. Parallel structures are seen in brachiopod adductor brachiopod Lingula unguis range between 45 and 60 nm in
width and about 108 mm in length in Terebratalia (Eshleman Smooth muscle cells have been reported to be the only type
et al. 1982; Kuga & Matsuno 1988). Widths of myofilaments found in polyplacophorans (Eernisse & Reynolds 1994) and
range from around 25 to 37 nm in the columellar muscle monoplacophorans (Haszprunar & Schaefer 1997). Lemche
of stylommatophoran snails and 125 to 231 nm in bivalve and Wingstrand (1959) reported striated muscle in the radular
adductor muscles (Paniagua et al. 1996). The cell diameter is retractors of Neopilina galatheae.
related to the thickness of the thick myofilaments, those with The function of the smooth muscle cells is regulated by
thicker filaments being broader, at least in bivalve adductor their morphological characteristics, as the speed of contrac-
muscle (Morrison & Odense 1974). The thin myofilaments tion is directly related to the cell length, filament length, and
are 6 nm wide actin filaments with associated tropomyosin. width.
Regions of cross-linking between myofilaments are indi-

cated by dense (or Z) bodies, rather than the Z-lines seen 3.12.1.2 Transverse Striated Muscle Cells
when these regions are aligned. The thin filaments attach to In transverse or cross-striated muscle, the thick and thin fila-
these bodies. ments are organised into arrays of distinct A-bands, I-bands,
The morphology of smooth muscles varies not only Z-lines, etc. (see above). This most closely resembles vertebrate
between species, but also between different muscle systems skeletal muscle, but differs from the striated muscle of verte-
in the same species (e.g., Plesch 1977). Matsuno (1987) classi- brates and arthropods in its poorly defined Z-lines which are
fied smooth muscle into at least four types (A–D), which have discontinuous in appearance, consisting of multiple small elec-
been found in molluscs. They are based mainly on the diam- tron-dense patches. Because the sarcomeres are poorly defined,
eter of the thick myofilaments and the density and arrange- this has sometimes resulted in an incorrect interpretation of
ment of the dense (or Z) bodies that anchor the small filaments transverse striated muscles as either obliquely striated or smooth
(Matsuno 1987). (Paniagua et al. 1996). Like smooth muscles, these cells have a
single central nucleus. These muscles are found in the adductor
• In type A, the thick myofilament diameter is less muscles of some bivalves, in the hearts of many bivalves, and in
than 14 nm and there are a few irregularly arranged the heart (e.g., Plesch 1977), radular retractors, and foot of some
dense Z-bodies. This type of smooth muscle is typi- heterobranch gastropods (e.g., Huang & Satterlie 1989). Each
cal of vertebrates, but has been recorded from the thick filament in striated muscle is surrounded by 10–12 thin fil-
adductor and foot muscle of a few bivalves and gas- aments, with thick filaments ranging from 17 to 20 nm in diam-
tropods (Matsuno 1987; Lee et al. 2012) and from eter in bivalve adductor muscles and 24–29 nm in heart muscle
some other invertebrates. (Paniagua et al. 1996). In bivalves, mitochondria are more abun-
• The B type is found in various invertebrates includ- dant in heart muscle than in adductor muscle (Paniagua et al.
ing many molluscs and echinoderms and differs from 1996). Interestingly, as noted by Voltzow (1994), typical striated
the A type in having thicker myofilaments (diam- muscle has not been found in ‘prosobranchs’. Fretter and Graham
eter about 40 nm) and larger irregularly arranged (1962: 614) commented that in a scissurellid (Vetigastropoda) all
Z-bodies. In the foot of the caenogastropod Bullia, muscles were composed of striped fibres except the columellar
the Type A muscle is found only in the propodium, muscle, which they noted was ‘remarkable’. This observation,
while Type B is found in the metapodium (Silva & however, needs ultrastructural verification.
Hodgson 1987). The Z-band in transverse muscle is composed of multiple
• The C type cell has even thicker myofilaments electron-dense bodies made up of thin filament attachment
(diameter 60–120 nm) and few, but large, Z-bodies. plaques intermingled with tubules and vesicles of sarcoplas-
This type of muscle cell has been reported mic reticulum. Although less developed, there is a transverse
from the adductor muscles of several bivalves and longitudinal component to the ‘sarcotubular’ system sim-
(Matsuno 1987). ilar to that seen in vertebrate striated muscles. Some tubules
• D type cells have thick myofilaments of 14–40 nm are T-tubules that originate as invaginations of the plasma
diameter, and the dense bodies are small, numerous, membrane. The sarcoplasmic reticulum tubules and vesicles
and more regularly arranged (Matsuno 1987), giving join in the Z-lines forming dyads comprising the transverse
them a similar appearance to obliquely striated mus- component. The longitudinal component comprises sinuous
cle, and it appears to be intermediate between these tubules running parallel to the myofilaments, and they con-
two types of muscle (Paniagua et al. 1996). This type nect the sarcoplasmic reticulum tubules of transverse compo-
of muscle is found in several groups of invertebrates, nents (Paniagua et al. 1996).
notably annelids, and occurs in the siphonal and
mantle retractor muscles of cephalopods and in some 3.12.1.3 Oblique Striated Muscle Cells
muscles associated with the buccal mass in vetigas- In obliquely striated muscle cells, the myofilaments are heli-
tropods and caenogastropods, but is otherwise appar- cally arranged sarcomeres (Figure 3.44), and they have a few
ently uncommon in molluscs. In cross sections using large mitochondria at either end of the cell. Like smooth and
a light microscope, this type of muscle appears to be transversely striated muscles, they have a single centrally
striated. located nucleus, and as in other striated muscles, there are
As in the transversely striated muscle of molluscs, the

Z-lines in molluscan obliquely striated muscle are discontinu-
mitochondria tubule
ous (Matsuno & Kuga 1989), which has sometimes resulted
in these muscles being wrongly interpreted as smooth muscles
(Paniagua et al. 1996). The sarcotubular system is very similar to
that in molluscan transversely striated muscle described above,
Golgi with the oblique system equivalent to the transverse component
thick
apparatus of the transversely striated muscle (Paniagua et al. 1996).
filament
Some striated muscles do not fit neatly into the above cat-
endoplasmic
egories. A type of pseudostriated muscle cell in the theco-
reticulum
some pteropod Clione differs from those in other molluscs.
nucleus The dense bodies form small sarcomere-like units (called
pseudosarcomeres) with A-bands and I-bands, which are
partially surrounded by sarcoplasmic reticulum (Huang &
H band Satterlie 1989). Another variation, which appears to be inter-
mediate between the helical and oblique forms of striated
I band
muscle has been recorded in the propodial foot muscle of
Bullia (a caenogastropod) (Silva & Hodgson 1987).
Cephalopod muscles are typically obliquely striated,
A band
enabling them to contract quickly and powerfully, and paral-
lels have been made between them and the striated muscles
of vertebrates (e.g., Mommsen et al. 1981). Unlike most ver-
tebrates, they rely mainly on carbohydrates and amino acids
electron-dense rather than fats for their metabolism (Hochachka 1994) (see
body Chapter 2). Also, in vertebrates, the mitochondria tend to be
grouped centrally within each sarcomere.
FIGURE 3.44 A diagrammatic representation of an obliquely
In squid and cuttlefish, all mantle muscles are obliquely
striated muscle cell of a coleoid cephalopod. Redrawn and modi-
fied from González-Santander, R. and Garcia-Blanco, E.S.,
striated (Bone et al. 1995), but there are significant differences
J. Submicrosc. Cytol., 4, 233–245, 1972; Paniagua, R. et al., Histol. in their attributes. The circular muscle of the mantle wall of
Histopathol., 11, 181–201, 1996. cuttlefish and squid contains two main types of fibres. Thin
inner and outer layers are comprised of larger cells, with more
mitochondria and better blood supply than the smaller cells in
thick and thin myofilaments forming sarcomeres delimited by the wider middle layer (Bone et al. 1981; Milligan et al. 1997).
Z-lines. The myofilaments are not perpendicular, but instead The ultrastructure of the arm transverse muscle fibres of
are oblique to the Z-lines because of the coiling of the fibres, decabrachian coleoids are like those known in most other
the myofilaments remain aligned with the longitudinal axis muscular systems in cephalopods, being obliquely (i.e., heli-
of the cell. Because the sarcomeres spiral through the cell, cally) striated and having relatively long thick filaments.
this type of muscle has also been called spiral striated muscle The myofilaments are arranged parallel to the long axis of the
or, in cephalopods, helical smooth muscle by Chantler (1983). fibre, but are staggered, forming a helical alignment. In the
Obliquely striated muscle occurs in several other invertebrate tentacles, the transverse muscles have more elements in series
groups, notably brachiopod adductor muscles, nematodes, and have much shorter myofilaments and sarcomeres com-
some pelagic tunicates, annelids, and chaetognaths, although pared with those in the arms, although the muscle biochemis-
each has its own characteristics (Paniagua et al. 1996). try is similar (Kier & Schachat 2008 and references therein).
Obliquely striated muscle was first described in cephalo- While the change in myofilament length appears to account
pods, where it is a dominant muscle type, and was later shown for the increased contraction speed, the change in striation
to be common in the translucent part of the adductor muscles pattern is less obvious (Kier & Schachat 2008). The evolu-
of several bivalves and brachiopods and in various muscle tion of different structural attributes to provide differences
systems in Lymnaea (see Paniagua et al. 1996 for references). in performance contrasts with the situation in vertebrates,
The thick filaments are fusiform in shape, and in many where muscle structure is relatively similar and variances in
molluscs each is surrounded by 12 thin filaments, although contractile performance relate to biochemical modifications,
nine thin filaments for each thick filament have been observed with different myofilament proteins being expressed (Kier &
in Lymnaea (Plesch 1977). The maximum width of thick Schachat 2008). Transcriptome studies of coleoids, cuttlefish,
filaments is usually around 20–30 nm, but in some bivalve and octopods have failed to identify muscle-specific myosin
adductor muscle can be up to 60 nm (Paniagua et al. 1996). isoforms involved in the adjustment of contractile veloci-
The thick filaments are comprised of a paramyosin core cov- ties, and only alteration of sarcomeric ultrastructure appears
ered by myosin (Elliot 1979), while the thin filaments are responsible for contractile velocity adjustments (Shaffer &
composed of actin, like those in other muscle types. Kier 2016).
3.12.2 Metabolism of Contraction 3.12.2.1 Catch Muscle and Twitchin

The underlying chemistry of muscle contraction is complex Smooth muscle may contract and relax rapidly (phasic con-
(see Box 3.1). At least two main kinds of muscle contraction traction) or may exhibit slow, sustained contraction (tonic
are found in molluscs. contraction), the latter using low calcium and low energy to
In the first type of contraction, typical of smooth muscle in maintain contraction over long periods. Molluscan catch mus-
molluscs and other invertebrates, contraction is initiated with cle, such as occurs in the dense white part of bivalve adductor
calcium ions binding directly to the myosin head and then muscles and in bivalve byssus retractor muscles, is unusual in
rapidly cycling cross-bridges to generate force. This involves maintaining contraction for very long periods of time while
myosin control of ATPase activity. In these cells, calcium ions using little energy. This property has been known for over a
(Ca2+) initiate contraction by their interaction with calmodulin18 century (see Bayliss 1927 for an early review).
to stimulate phosphorylation of the light chain of myosin by Both cholinergic and serotonergic nerves19 control mollus-
way of myosin light chain kinase. The calcium ions act directly can catch muscle. Stimulation by a cholinergic nerve causes
on the myosin head forming cross-bridges which bind with an increase in intracellular Ca2+ which results in phasic con-
the actin filament. These rapidly cycling cross-bridges gener- traction, and the subsequent decrease in Ca2+ concentration
ate force, allowing contraction to begin. This process is facili- initiates the catch state. Catch tension is maintained until
tated by energy released from ATP by myosin ATPase activity. serotonin is released, accumulating cAMP in the muscle cell
Relaxation of the muscle occurs when Ca2+ ions are removed (Funabara et al. 2005) (see Figure 3.46).
and myosin phosphatase is released, which inhibits the dephos- Catch is initiated by cholinergic nerve stimulation and
phorylation of the myosin. Calcium ions are removed from occurs with a temporary increase in calcium in the nerve cell
the muscle cell by the Ca2+ATPase pump in the sarcoplasmic which is quickly reduced to near baseline levels. This sus-
reticulum and/or by similar pumps in the plasma membrane. As tained phase of contraction, or catch phase, is attributed
with vertebrate smooth muscle, there is also a sustained ‘catch’ to a protein similar to titin and connectin, called twitchin
phase with low calcium and where contraction can be main- (Butler & Siegman 2010). Twitchin is also known in nema-
tained with low energy utilisation (see Section 3.12.2.1). todes, while in insects a different protein, projectin, functions
The second type of contraction is found in vertebrate in much the same way. Projectin also occurs in scallops and
striated muscle and in some molluscan muscles, and differs Aplysia (Benian et al. 1996).
markedly from that seen in smooth muscle in having an actin- Activation of the muscle by stimulating a serotonergic nerve
linked regulatory system. On the thin filaments, a protein activates a calcium-dependent phosphatase. This dephosphor-
(tropomyosin) covers the myosin binding sites of the actin ylates twitchin and allows catch force to be maintained when
molecules. For contraction to occur, calcium ions are pumped the level of intracellular calcium decreases. During the catch
from the sarcoplasmic reticulum into the sarcomere. The cal- phase, the rate of ATP utilisation and cross-bridge cycling is
cium binds to the protein troponin (Tanaka et al. 2008), and extremely slow and calcium levels are low (Funabara et al.
then alters the structure of tropomyosin, so the binding sites 2005; Butler & Siegman 2010).
on the actin myofilament are uncovered. These exposed bind- Twitchin binds to both thick and thin filaments, but bind-
ing sites can then bind to the ‘heads’ of the myosin molecules. ing to the thin filaments depends on phosphorylation, and
This process is powered by ATP binding to each myosin head its uncoupling occurs with dephosphorylation. Regulating
resulting in the chemical energy in that molecule being con- catch is thus based on both the attachment of myosin cross-
verted into mechanical energy by hydrolysis of ATP (involv- bridges to actin and the state of phosphorylation of twitchin.
ing an ATPase, myosin head ATPase) to ADP and phosphate. The process proceeds as follows: on stimulation of the catch
This results in each myosin head ratcheting its way along the muscle, calcium increases in the muscle cell and activates the
actin filament. While most of the physiological details have formation of cross-bridges and twitchin is dephosphorylated.
been worked out on vertebrate muscles, myosin head ATPase Myosin to actin cross-bridges displace twitchin from the thin
has been demonstrated, for example, in some molluscan filaments and phasic muscle contraction proceeds, but as
muscles including squid muscle (e.g., Shaffer & Kier 2012; intracellular calcium concentration is reduced catch ensues,
Yamada et al. 2013). In contrast to the myosin in vertebrate with the myosin cross-bridges detaching from the actin fila-
striated muscle, molluscan myosin specifically binds two ments. At this stage, there is a three-way complex between
calcium ions, and these sites are essential for the regulatory myosin, twitchin, and actin which tethers the thick and thin
activity of contraction (Bagshaw 1993). filaments. Catch is released when serotonergic nerves are
The sarcoplasmic reticulum (a form of endoplasmic reticu- stimulated, causing an increase in cAMP and activation of
lum) controls the concentration of calcium ions. When calcium protein kinase A. This enzyme activates phosphorylation of
is released it activates muscle contraction and when removed twitchin and the twitchin tethers detach from the thin fila-
relaxation occurs. Magnesium ions, although not directly ments (Funabara et al. 2005; Butler & Siegman 2010).
involved in muscle contraction, play a role in the enzymes The catch muscle has a high proportion of paramyosin to
involved (e.g., Yamada et al. 2013). myosin (2–10:1 in mass) and thick filaments that are very long
A calcium-binding messenger protein.

18 See Chapters 2 and 7.
19
BOX 3.1 THE STRUCTURE AND FUNCTION OF MUSCLE CELLS

Muscle cells have similar functions and properties in animals generally, although invertebrate muscles have single nuclei
while skeletal striated muscle in vertebrates comprises multinucleate cells. Muscle cells can be very elongate and contract
actively and elongate passively. Their contractile properties are conferred by contractile elements (myofibrils) that run the
length of the cells and are comprised of bundles of thin and thick filaments composed of elongate complex proteins. The
thin filaments are composed of actin and the thicker filaments of myosin. Each myosin molecule has a globular ‘head’
and an elongate ‘tail’.
The filaments are organised into repeated subunits (sarcomeres – the contractile units) along the myofibril. If the
sarcomeres are lined up across the myofibrils in the muscle cell, it appears to be striped, and that type of muscle cell is
called ‘striated’. In smooth muscle cells there is no alignment.
Some details of the morphology of each sarcomere are provided here, and, although largely based on vertebrate
muscle, the same terms are used in accounts of molluscan muscle. Each sarcomere is delimited by thin dark bands of
dense protein, the Z-material (or Z-bodies or dense bodies), which is arranged in Z-lines (or Z-discs). Both types of
filaments are attached to the Z-bodies by the giant protein titin (or connectin), with the myosin filaments being linked
across the I-band and the actin filaments cross-linked with titin in the Z-line via the protein α-actinin. The structure of
the Z-material is thus related to the probable tension within the muscle fibre. Abutting the Z-lines in a relaxed state are
the pale I-bands, which contain the actin filaments. The remainder of the sarcomere is the slightly darker A-band which
contains both the thicker myosin filaments and actin filaments. A narrow, paler H-band lies in the centre of each A-band
when the muscle is relaxed, and it does not contain the actin filaments (see Figure 3.45).
When the muscle contracts, the actin and myosin filaments do not change length, but slide past each other – this is
known as the sliding filament concept. The actin filaments are pulled along the myosin filaments toward the middle of
the sarcomere where they overlap. This results in the H-band becoming narrower and disappearing when the muscle is
fully contracted, and the two Z-lines (discs) are pulled closer together (Figure 3.44).
FIGURE 3.45 A diagrammatic representation of the sliding filament model of muscle contraction. Creative Commons Attribution
4.0 International.
relaxed active catch relaxed cholinergic and serotonergic nerves causes a phasic contrac-
serotonin
tion of smooth muscle, while a serotonergic nerve impulse
alone initiates the catch phase (Butler & Siegman 2010) (see
acetylcholine
te n
si o n also Chapter 6).
The point where a nerve and muscle connect is the neu-
tension
Ca2+ romuscular junction (or myoneural junction) and is a kind
Ca2+
of synapse. Striated muscle contractions are initiated from
nerves ending in neuromuscular junctions. The typical situ-
ation in vertebrate skeletal muscles is that nerve impulses
(action potentials) pass from the neuron to the muscle fibre

(cell) where they terminate and cause the muscle to contract.
phosphorylated dephosphorylated phosphorylated The terminal part of the nerve contains many vesicles which
twitchin typically contain acetylcholine (ACh). A nerve impulse causes
phosphorylation of twitchin vesicles to discharge ACh onto a special membrane on the
muscle fibre. This area contains a cluster of transmembrane
FIGURE 3.46 Schematic representation of the contraction of catch channels that ACh opens and allows sodium ions (Na+) to
muscle. Redrawn and modified from Funabara, D. et al., J. Muscle diffuse in to activate the fibre, stimulating the release of cal-
Res. Cell Motil., 26, 455–460, 2005. cium ions which interact with troponin (see Section 3.12.2).
This process is terminated by the enzyme acetylcholinester-
(25–100 nm) and very thick (diameter 20–100 nm). This type ase breaking down the ACh in the neuromuscular junction
of muscle is unlike others found in molluscs, although para- allowing the sodium channels to close, and the resting poten-
myosin is found in all invertebrate muscles (Funabara et al. tial of the muscle fibre is restored by an outflow of potassium
2005). Its content varies depending on species and tissues, ions. This sequence of reactions also occurs in molluscs (and
and correlates with the tension which the muscle can develop. other animals). Many molluscan neuromuscular junctions
Because it is most abundant in catch muscles, it has been sug- employ neurotransmitters other than ACh, such as glutamate,
gested that paramyosin plays a role in the thick filaments being dopamine, serotonin, and FMRFamide (Muneoka & Twarog
able to stand very high tensions (Funabara et al. 2005). As 1983). This diversity of neurotransmitters means that the ner-
noted above, paramyosin is not found in vertebrate muscles. vous control of muscles is often complex.
An example of a well-studied molluscan muscle sys-
3.12.2.2 Muscle Activation and Control tem is the anterior byssus retractor muscle of Mytilus. Both
Muscle fibres (cells) connect to nerve, muscle, and glio- excitatory and relaxing nerves innervate this muscle with
interstitial tissue. The significance of the glio-interstitial the principal neurotransmitters released from these nerves
connections is not certain, but these cells, which have being acetylcholine and serotonin, respectively. Various other
granular contents, may play a role in the ionic regulation monoamines (e.g., dopamine, octopamine) and peptides may
of the nerve and/or muscle cells (Nicaise 1973; Muneoka & also be involved in regulating this muscle as neurotransmit-
Twarog 1983). ters or neuromodulators (Muneoka et al. 1991). The control by
Muscles can be controlled extrinsically, or by hormones multiple neurotransmitters and neuromodulators of the ante-
or other humoral factors (see Chapter 2), other muscles or rior byssus retractor muscle of Mytilus appears to be typical of
nerves, or intrinsically by autoregulation or local humoral many molluscan and other invertebrate muscles.
control (either autocrine or paracrine – see Chapter 2).
Three kinds of muscle-muscle junctions (or myomuscular
junctions) occur in molluscs and are generally similar to those 3.12.3 Some Muscular Systems in Molluscs
seen in other animals. These are: (1) gap-junctions (nexus)20, Eight main muscle systems were recognised in molluscs by
(2) junctions with wider gaps and no basal lamina, and (3) Haszprunar and Wanninger (2000). These are the body wall
attachment via desmosomes21 (Nicaise & Amsellem 1983). musculature, the buccal musculature, dorsoventral muscula-
Smooth muscle contraction is initiated by the release ture (including the shell muscles), mantle retractor muscles,
of membrane-bound vesicles (neurotransmitter vesicles) gut muscles, adductor muscles, enrolling muscles (in chitons
into the space between the cells. Sympathetic fibres cause and aplacophorans), and extraocular eye muscles. Below we
both constriction and relaxation of smooth muscle via dif- look at some of these and other categories of muscles.
ferent receptors; α adrenergic receptors primarily cause
contraction, and β adrenergic receptors cause relaxation. 3.12.3.1 Retractor Muscles
The simultaneous stimulation of smooth muscle by both The foot retractor muscles carry out various retraction
responses. They are robust in burrowing bivalves and in
gastropods where pedal manipulation and retraction is well
20 Gap junctions (= nexus or septate junction) are intercellular cytoplasmic
developed. Retractor muscles perform a variety of functions
connections that allow communication between cells.
21 Desmosomes are protein structures that serve to adhere cells to each including locomotion, feeding actions, reproductive behav-
other. iour, and retraction of a body part away from tactile stimuli.
Some of the studies on their structure in gastropods include 3.12.3.3 Body Wall Musculature
those on head retractors (Plesch 1977), buccal retractors This basic molluscan body musculature found in most mol-
(Dorsett & Roberts 1980), gill withdrawal muscles (Carew luscs consists of outer circular, medial diagonal, and inner
et al. 1974), pteropod wing retractors (Huang & Satterlie longitudinal muscles. In addition, dorsoventral fibres stabilise
1989), and penis retractors (Wabnitz 1975). The byssal retrac- the body (Haszprunar et al. 2008). Variations exist in dif-
tors in bivalves are derived from pedal retractor muscles. ferent groups – for example, in both classes of the shell-less
The complex muscle system of cephalopods also includes aplacophorans four thick bands of muscle run the length of
retractor muscles such as the large retractors of the head. the body with an extra two ventral bands in Solenogastres.
These muscles, along with the body wall muscles, maintain
3.12.3.2 Antagonistic Muscles body shape. In the caudofoveates the body musculature is
These are sets of muscles which work against each other by responsible for body movement as these animals lack a foot.
acting in opposite directions. They work in a variety of ways, The details of body wall musculature in gastropods has
not the least of which is forcing (stretching) muscles back to not been well studied, but usually consists of an outer layer
their original size and shape after contraction (because mus- of circular muscles and inner longitudinal muscles (Voltzow
cle cells can only contract). This term is commonly applied to 1994). In the hygrophilan Lymnaea there is an outer layer
opposing sets of muscles attached to bones in the vertebrate of circular muscle, a middle layer of diagonal muscles, and
body, but the same functional arrangement is common in mol- an inner layer of longitudinal muscles (Plesch et al. 1975)
luscan muscular systems ranging from pairs of muscles attached (Figure 3.47).
to the shell to sheets of muscles attached to connective tissue.
tentacle
Circular muscle system Diagonal muscle system
cephalopedal
sinus
Horizontal foot muscle system
foot
Longitudinal muscle system
Columellar muscle system
cephalopedal
sinus
FIGURE 3.47 Major muscle systems in the hygrophilan Lymnaea stagnalis. Redrawn and modified from Plesch, B. et al., Neth. J. Zool.,
25, 332–352, 1975.
The most developed body wall muscles in molluscs are Voltzow (1988) noted that in patellogastropod limpets, which
seen in coleoid cephalopods (see Section 3.12.3.8.2). have ditaxic pedal waves, there was little crossing of muscle
fibres between the left and right lateral pedal muscle blocks,
3.12.3.4 Foot (Pedal) Musculature as in monoplacophorans. This contrasts with other kinds of
The molluscan foot is highly modified from the assumed plesi- limpets [such as fissurellids (Vetigastropoda), Crepidula
omorphic arrangement seen in chitons (see Section 3.8.2), but (Caenogastropoda), and Siphonaria (Heterobranchia)] and
even the plesiomorphic state is highly complex with the shell chitons, which all have monotaxic pedal waves and inter-
muscles (Figure 3.49) comprising much of that complexity spersed fibres from the left and right pedal muscle blocks
(Wingstrand 1985). The foot musculature in monoplacopho- (Figures 3.34 and 3.48).
rans has been described in Neopilina (Lemche & Wingstrand

1959; Wingstrand 1985), where there is an outer layer of circu- 3.12.3.5 Shell Muscles
lar muscles running around the circumference of the foot, this Both polyplacophorans and monoplacophorans have up to eight
outer part is thickened and the shell muscles are embedded in pairs of composite shell attachment muscles (Figure 3.49).
it. Unlike the situation in chitons, the inner part of the sole is The dorsoventral and oblique muscles which make up the
thin and lacking in substantive musculature. In solenogasters shell muscles are thought to be homologous in conchiferan
the rudimentary foot is not muscularised, however, oblique taxa although there are different patterns of loss in different
retractor muscles extend from the lateral sides of the body groups. In bivalves, the plesiomorphic shell muscles are the
to the pedal groove (Thiele 1894). In Proneomenia, retractor dorsoventral and oblique pedal muscles, while the adductor
muscle fibres from either side of the body cross and intersperse muscles are new structures necessitated by the two-part shell
over the pedal groove (Hoffmann 1949). (see Section 3.12.3.6 and Chapter 15).
The column-like foot in scaphopods is surrounded by an The earliest bivalves such as Pojetaia have multiple mus-
outer layer of circular muscles, inside which are the blocks cle attachment scars and living protobranchs have up to seven
of longitudinal muscles and radial muscles that make up the pairs of dorsoventral and oblique pedal muscles. Scaphopods
bulk of the pedal musculature (Shimek & Steiner 1997) (see have two pairs of dorsoventral shell muscles as does Nautilus,
Chapter 16 for details). Well-developed circular muscles are although some fossil nautiloid shells have multiple muscle
also present in the foot of protobranch bivalves (Heath 1937), scars (see Chapter 17).
but are comparatively weakly developed in the autobranch Thus, in living molluscs, it may seem that multiple, paired
arcid Tegillarca and the venerid Gomphina (Lee et al. 2007; shell muscles are plesiomorphic (Figure 3.50) with apomorphic
Park et al. 2012), while the foot of the tellinoidean Donax reduction or, possibly, fusion of muscles, ultimately leading
has only oblique and dorsoventral muscle fibres (Trueman & to single pair or single muscle, as in cephalopods and gastro-
Brown 1985). In cephalopods the foot is markedly modified as pods. This is in contrast to the condition in the earliest supposed
the arms (Shigeno et al. 2008) and their complex musculature molluscan ancestors (the small shelly fossils) which have been
is briefly described below (see Section 3.12.3.8.1). reported to have only a single pair of muscle scars. However, at
In gastropods, the highly muscular foot is very flexible and least some of these are probably not molluscs (see Chapter 13).
although well studied externally, surprisingly, the detailed inter- Some gastropods have a pair of shell muscles, including
nal muscular structure has only been studied in a few taxa (see the patellogastropods, haliotids, scissurellids, the phasianel-
Voltzow 1994 for review). In general, the foot of a snail is com- lid Tricolia (Marcus & Marcus 1960), and most neritimorphs,
posed almost entirely of muscle which can be divided into two but in most others (i.e., vetigastropods, caenogastropods, and
distinct sections – the dorsal columellar muscle and the ventral heterobranchs), there is a single shell dorsoventral attachment
‘tarsos’ (Voltzow 1985, 1986, 1994). In both, the muscles are muscle, the columellar muscle (Figures 3.51 and 3.52). The few
packed in bundles bound in connective tissue, but the fibres in instances of paired shell muscles in heterobranchs (such as
the tarsos are smaller in diameter and radiate to connections in Rissoellidae) and the caenogastropod Velutinidae and Triviidae
connective tissue just internal to the sole epithelium. There is no may be explained by heterochrony (Ponder & Lindberg 1997).
outer circular muscle layer. The columellar muscle of snails is In some gastropods, (Patellogastropoda, Neritimorpha,
the shell muscle and attaches to the shell on the columella. It is some Cocculinoidea, and Lepetellidae in Lepetelloidea) the
also attached to the operculum (if present) and/or the dorsal part shell muscles are superficially divided by blood sinuses pass-
of the foot. Interspersed with these fibres are bundles of fibres at ing through them. Given the distribution of this phenomenon
right angles, and this combined muscle functions as an antago- within gastropods, it has probably arisen independently in the
nistic muscular hydrostat (Voltzow 1994). The gastropod foot four main groups (Ponder & Lindberg 1997).
does not, however, function primarily as a hydrostatic organ, In coiled gastropods, the shell muscle is attached to the
and shows variation in the relative importance of fluid spaces, columella (Figure 3.51) which, in some, bears folds thought to
ranging from being a solid muscular hydrostat to a more fluid- increase the surface area for the attachment of that muscle, but
dependent system (Voltzow 1994). Two of the most detailed other ideas have also been advanced. These columellar folds
descriptions of the complex head-foot musculature in gastro- were reviewed in ‘turritelliform’ gastropods by Signor and
pods are those of the panpulmonates Lymnaea (Plesch et al. Kat (1984), who noted two additional hypotheses to explain
1975) (Figure 3.47) and Helix (Trappmann 1916) (Figure 3.51). the existence of such folds: (1) that they were deposited by
cuticle with spicules

shell plate
superior rectal
dorso commissure
-ventral gut
muscle
lateral
nerve girdle
transverse cord
muscle foot
pedal nerve cord Polyplacophora
foot
Solenogastres
transverse muscle dorso-ventral
fused transverse muscle
and dorso-ventral shell
muscles subrectal commissure
lateral nerve
cord
foot pedal
nerve cord
Gastropoda-Patellogastropoda Monoplacophora
ligament
transverse
muscle
subrectal commissure
dorso-ventral shell
muscle valve
lateral nerve cord
fused transverse
and dorso-ventral
muscles
foot
Bivalvia- Protobranchia Bivalvia-Autobranchia
FIGURE 3.48 Diagrammatic transverse sections showing the relationship between shell muscles (i.e., the dorsoventral muscles) (in blue),
intestine and rectum, and the main nerve cords in Solenogastres, Polyplacophora, Gastropoda (Patellogastropoda) and Bivalvia. Redrawn
and modified from Haszprunar, G., Z. Zool. Syst. Evol., 27, 1–7, 1989a.
an enlarged, folded mantle, and (2) that they were related to a In extinct rostroconchs, the putative foot retractor muscles
siphonal notch in the aperture. Based on their observations, they appear as a circular or horseshoe-shaped grouping around the
rejected all three of these hypotheses. They also noted that they upper part of the shell interior, while in most bivalves, they
were highly correlated with burrowing tall-spired taxa. Price are divided into paired anterior and posterior groups (Waller
(2003) investigated four parameters of the columellar muscle 1998). Protobranch bivalves have multiple pairs of anterior
in taxa with and without columellar folds. These were the area shell muscles and usually three posterior pairs (Heath 1937;
and length of attachment, the total area of contact between the Driscoll 1964). The number of muscles has been reduced in
muscle and the columella, and the depth of attachment inside autobranch bivalves which often have only a single pair of
the shell. She found no significant differences between spe- anterior and posterior oblique retractors and a single anterior
cies with and without folds. Thus, the functional significance oblique protractor (Figure 3.52).
of columellar folds is still not understood and, given that they There are parallel trends in the reduction in the number
have certainly arisen independently in several groups of gastro- of shell muscles in bivalves, gastropods, and cephalopods.
pods, their utility may differ across taxa. In some extinct nautiloids with conical shells there were
post-apophysial pre-apophysial lateral transverse oblique

pedal retractor pedal retractor longitudinal muscle muscle
muscle muscle muscle
FIGURE 3.49 Comparison of the shell and foot musculature of a monoplacophoran and a chiton. Redrawn and modified from Wingstrand,
K.G., On the Anatomy and Relationships of Recent Monoplacophora. Galathea Report, 16: 1–94., 1985.
multiple shell muscles (see Chapter 17), which may have bivalved gastropods, but not the extinct bivalved group the
been reduced to two pairs (as in living Nautilus) or a single rostroconchs. The anterior adductor muscle develops first in
pair as in coleoids. Fossil nautiloids have three main mus- ontogeny. All bivalve juveniles are dimyarian, even if mono-
cle attachment areas, all in the posterior part of the body myarian as adults (Waller 1998), and the rectum always lies
chamber (Mutvei 1957). These consist of two continuous above the posterior adductor muscle.
bands for attachment of the body and mantle muscles and The adductor muscles of bivalves have been the subject of
two pairs of scars for the attachment of the dorsoventral many ultrastructural and physiological studies, in part through
retractor muscles. In some Cretaceous ammonites, there interest in the diversity of muscle fibres, especially the smooth
was a pair of muscles dorsally and a single ventral muscle catch muscle (e.g., see Section 3.12.2.1).
(Jones 1961).
Adult and larval shell muscles are not necessarily homolo- 3.12.3.7 Odontophoral Muscles
gous (see Chapter 8 for an overview of their ontogeny). The muscles involved in the movement of the mouth, buc-
cal cavity, and the odontophoral apparatus (including the rad-
3.12.3.6 Adductor Muscles ula) comprise the most complex set of muscles in the body.
Adductor muscles are the muscles that pull the valves together Bivalves have less complexity than other molluscs because
in a bivalved shell. In living molluscs they have been inde- of the lack of a radula, although multiple pairs of mouth
pendently evolved in Bivalvia and in the bivalved sacoglossan muscles, large buccal muscles, and palp musculature are
heterobranch gastropods (see Chapter 20). present in protobranchs (Heath 1937) since they are deposit
The adult adductor muscles of bivalves have undergone feeders, but are lacking in suspension-feeders (autobranchs).
many transformations in bivalve evolution (see Chapter 15). In
radula-bearing groups, these muscles are usually red
Adductor muscles are a ‘functional requirement of a bivalved because of the myoglobin they contain. Details of the arrange-
shell’ (Waller 1998, p. 10), as they are present in bivalved ment and functioning of the buccal and odontophoral muscles
animals as diverse as various crustaceans, brachiopods, and are given in Chapter 5.
Solenogastres (∞)
Caudofoveata (∞)
Polyplacophora (8)
Monoplacophora (8)
Protobranchia (3-8)
Autobranchia (2)
Scaphopoda (1-2)
Patellogastropoda (1)
Orthogastropoda (1)
Cephalopoda (1)
‘worm-like’ body wall musculature () number of sets of adult dorso-ventral muscles
adult cephalic retractors present
FIGURE 3.50 The main muscles in molluscs. Redrawn and modified from Wanninger, A. and Haszprunar, G., J. Morphol., 254, 53–64,
2002a. The dark blue muscle indicates the cephalic retractor muscles.
3.12.3.8 Specialised Hydrostatic Muscular found in Chapter 17. These include the muscles in the mantle,
Systems in Coleoids fins, and arms and tentacles.
There are several molluscan systems that are muscular hydro-
stats. Bivalve siphons are a good example (see Chapter 15) 3.12.3.8.1 Arms and Tentacles
as is the proboscis of certain caenogastropods (Golding et al. The arms and tentacles of coleoids are almost entirely
2009b) (see Chapter 5). composed of muscle arranged in a complex series of lay-
Among the most specialised are the muscular hydrostat ers (Figure 3.53), and they typically bear suckers (see
systems of coleoid cephalopods (e.g., Kier 1988), which we Section 3.12.3.8.4). The arm musculature functions as a
briefly review below. More details on these structures can be muscular hydrostat (Kier 1985, 1988). An outer layer of
lung mantle
penis retractor muscle
diaphragm
mantle collar
columella
ocular tentacle of shell
ocular tentacle
retracted retractor muscle
columellar
muscle
anterior
tentacle
retractor
anterior dorso-ventral
tentacle pedal
horizontal muscles
jaw longitudinal
buccal
cavity
radular sac buccal retractor pedal retractor foot sole

muscles muscles
Muscles in Helix pomatia, seen in longitudinal section from the left side of the body with
the shell removed (other than a small part of the columella). Odontophore not shown.
nerve ocular tentacle

ring retractor muscle
oesophagus
cephalopedal
buccal levator muscle haemocoel
external labial
levator muscle
columella
upper ventral buccal of shell
protractor muscle
buccal mass
columellar
muscle
anterior tentacle
anterior tentacle
retractor muscle cut body wall
head
ocular tentacle
buccal retractor foot
muscles pedal retractor
muscles
Dorsal view of muscles in Helix pomatia, with the dorsal wall and shell removed.
FIGURE 3.51 Musculature of Helix pomatia. Redrawn and modified from Trappmann, W., Z. wiss. Zool., 115, 489–585, 1916.
longitudinal muscle is underlaid by connective tissue and tentacles of decabrachians are used only for prey capture and
oblique muscle layers. This relatively thin sheath of muscle are capable of very rapid extension. In the squid Doryteuthis
encases a thick ring of bundles of longitudinal muscles that pealei, this involves the eight arms flaring open and the two
surround a thick core of transverse muscle with the fibres tentacles extending very rapidly (about 20–40 ms) (Kier &
running at right angles to each other and extending between Leeuwen 1997). The terminal part of the tentacles has suck-
the longitudinal bundles. The axial nerve cord and an artery ers and grasps the prey. The transverse muscles are primar-
run through the centre of the transverse muscle. The cirri of ily responsible for this remarkably rapid extension of the
Nautilus are comprised of similar layers of muscles, but the tentacles. Very similar, and probably homologous, muscles
longitudinal bundles are relatively larger and the transverse bend and support the arms, but those in the tentacles are
muscle mass smaller. modified and differ in several ways from the arm muscles
The arms are used in feeding and mating, and sometimes (Kier & Schachat 2008).
can be involved in locomotion or signalling (Hanlon & The arms of octopuses are extremely flexible – much
Messenger 1996) and even burying (e.g., sepiolids, more so than ‘limbs’ in other animals. Recent studies have
Boletzky & Boletzky 1970; Huffard et al. 2005). The paired investigated the system of movement in some detail. It is only
anterior pedal posterior pedal

protractor muscle retractor muscle
Bivalve (= oblique protractor) (= oblique retractor)
anterior
adductor posterior
muscle adductor
muscle
anterior pedal
retractor muscle
(= oblique retractor)
siphons
foot
Bullia
columellar
muscle
pedal operculum
transverse
muscles
pedal retractor pedal dorso-ventral pedal longitudinal foot

muscles retractor muscles muscles
FIGURE 3.52 Comparison of the main shell and foot musculature in a heterodont bivalve and a gastropod (Bullia). Bivalve redrawn
and modified from Trueman, E.R., Locomotion in mollusks, pp. 155–198, in A. S. M. Salauddin & Wilbur, K. M., Physiology, Part 1.
The Mollusca, Vol. 4, Academic Press, New York, 1983, and Bullia redrawn and modified from Trueman, E.R. and Brown, A.C., J. Zool.,
178, 365–384, 1976.
ridge
circumferential muscle
external oblique muscle
epidermis
connective tissue
trabeculae (thin sheets sheath vein
of radial muscle fibres
separating longitudinal dermal
connective
muscle) tissue and
muscle
transverse muscle
artery
axial nerve cord
internal longitudinal
oblique muscle muscle
median suckers
longitudinal
muscle oblique muscle
FIGURE 3.53 Details of the musculature of an arm of Octopus. Redrawn and modified from Kier, W.M., The arrangement and f unction of mol-
luscan muscle, pp. 211–252, in Trueman, E.R. and Clarke, M.R., Form and Function. The Mollusca, Vol. 11, Academic Press, New York, 1988.
possible because of the highly organised and complex system flaps, the circular muscle fibres of the mantle are not involved
of motor control. Octopuses also can transform the arm that is (Bone et al. 1995).
carrying out precise movements into a pseudo-jointed struc- In Nautilus, the funnel is a mobile fold of tissue that can
ture (Yekutieli et al. 2002, 2005a, b; Sumbre et al. 2005), with be rolled into a tube, while in coleoids it is a tubular struc-
many of these actions independent of the brain (Sumbre et al. ture. The jet stream of water from the mantle cavity is directed
2001, 2005). through the funnel and is used in steering the animal by it
pointing in a particular direction. Other functions include
3.12.3.8.2 Mantle Wall and Funnel squirting a jet of water at a predator, and (for female octo-
The contraction of mantle muscle fibres in the mantle wall puses) aerating their egg mass, while some benthic octopuses
powers the jet propulsion that is a hallmark of cephalopods, direct it downward to blow a cavity in soft substratum so they
and the whole system acts as a muscular hydrostat (Ward & can bury themselves (Hanlon & Messenger 1996).
Wainwright 1972) with the mantle wall muscles pressuris-
ing the water in the muscle tissue (Gosline & Demont 1985). 3.12.3.8.3 Coleoid Fins
In all cases there is an antagonistic action of circular and Fins are present in all decabrachians, in cirrate octopods, and
radial muscles. Contraction of the circular fibres expels the Vampyroteuthis, and they vary in size, shape, and function
water (as the locomotory jet) from the mantle cavity while (Hanlon & Messenger 1996). In sepioids and squid the trans-
tension in the longitudinal muscles prevents lengthening of verse and dorsoventral muscle bundles work antagonistically
the mantle, and the radial muscles are stretched as the walls and are divided horizontally in the middle section of the fin by
thicken (Gosline & Demont 1985). Contraction of the radial a layer of connective tissue (the median fascia) which provides
fibres makes the mantle wall thinner (and increases the volume elastic support. There are also strands of connective tissue that
of the mantle cavity) and water is drawn in. As in octopods, run diagonally through the muscles. Again, the whole system acts
there are radial and circular muscles in decabrachians, but the as a muscular hydrostat as do the arms and tentacles (Kier 1985).
longitudinal muscles are replaced by outer and inner layers
of stiff tunic composed of layers of collagen fibres that run 3.12.3.8.4 Suckers
at right angles to each other. Connective tissue fibres also run Coleoids often have suckers arranged in rows on their arms
diagonally through the muscles (e.g., Budelmann et al. 1997) (see Chapter 17). Each sucker can be divided into an inner
(Figure 3.54). The tunics prevent the mantle from lengthen- cavity (acetabulum) and the outer part that attaches, the infun-
ing when either the radial or circular muscles contract and dibulum, both separated by a narrow section ringed with a
also provide a firm insertion surface for the radial muscles. sphincter muscle. The infundibulum may be attached broadly
The arrangement in octopods enables greater flexibility and to the arm or by a narrow stalk. Its rim forms the outer part of
movement of the mantle than is possible in the much more the sucker and may be lined with chitin which can be denticu-
rigid arrangement in decabrachians. late or toothed or form one or more hooks.
In decabrachian coleoids, the radial muscles are entirely Three sets of muscles act for both the acetabulum and
fast twitch, glycogenic fibres, contracting during jetting. infundibulum. Radial muscles lie perpendicular to the inner
The thick layer of circular muscles consists of a central mito- surface of the sucker and there are circular muscles (including
chondria-poor zone of fast twitch fibres used in jetting and an the sphincter already mentioned) around the circumference of
outer and inner layer of mitochondria-rich slow-twitch, aero- the sucker. In addition, meridial muscles run at right angles
bic fibres used in slow swimming. The complex arrangement to the two other sets of muscles and with the circular mus-
of collagen fibres consists of some that are stretched on con- cles presumably act antagonistically with the radial muscles.
traction of the circular muscles and others that stretch when The coordination of this complex musculature is assisted by a
the radial muscles contract when the mantle cavity fills, with small ganglion that lies below each sucker.
their elastic rebound helping to expel the water (Gosline &
Demont 1985). 3.12.3.8.5 Skin Papillae and Chromatophores
The mantle muscle is markedly thicker in coleoid cepha- Both sepioids and octopods have complex muscles that change
lopods that utilise powerful jet propulsion than in those that the skin texture – from smooth to spike-like papillae that can
do not (Trueman & Packard 1968). The pulsating mantle also be 10 mm or more high (Hanlon & Messenger 1996).
has an important role in respiration when the animal is at rest. Chromatophores have a muscular system that enables them
In Sepia at least, this is due to the alternating activity of the to rapidly expand or contract, thus quickly changing the skin
radial muscles of the mantle and the musculature of the collar colour (see Chapter 17).
inner tunic
(connective tissue)
radial muscle fibre

superficial collagen fibres
mitochondria
-rich zone crimped
circular central collagen fibres
muscle mitochondria
fibres -poor zone collagen fibres
superficial
mitochondria
-rich zone
radial muscle
circular outer tunic
muscle fibres (connective tissue)
collagen fibres
muscle
collagen
longitudinal muscle fibres
longitudinal connective tissue fibres
intramuscular connective
tissue fibres
radial muscle fibres
radial muscle longitudinal
muscle fibres
circular connective
muscle fibres tissue fibres
longitudinal
connective
tissue fibres
FIGURE 3.54 Diagram of the musculature and connective tissue in a ventral region of the mantle of a squid and an octopus, with outer
(skin) layer at the bottom. Redrawn and modified from Kier, W.M. and Thompson, J.T., Berl. Paläobio. Abh., 3, 141–162, 2003.

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Biology and Evolution of the Mollusca

Winston F. Ponder, David R. Lindberg, Juliet M. Ponder

Shell, Body, and Muscles

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Polyplacophora Monoplacophora Aplacophora

dorso-ventral axis of body gut

Patellid (Patellogastropod) Vermetid

Olivid (Caenogastropod) Heteropod Cephalaspidian (Heterobranch) Doridid (Heterobranch)

--- dorso-ventral axis --- axis of volution --- life-orientation axis

--- dorsoventral axis

FIGURE 3.3 Axes of symmetry in bivalves. Original.

called the brachiophore. In the Inarticulata, the shell is com-

cle attachment scars (Vinn & Zatoń 2012). Annelid calcar-

3.2.1 Comparison with Outgroups θ

large factor produces a slight curve, as in a scaphopod shell. If

Whorl expansion rate (W) w1 w 2 wn − 1

of the shell edge grow relatively faster, with points further

m more inflated (Vermeij 1990).

ce Various shell shapes have evolved multiple times in gas-

d tropods. For example, the limpet and conical shell shape have

in often evolved in many lineages. In most gastropod limpets

cr ‘anterior’ (i.e., post-torsional anterior) dilation exceeds (or in a

few species equals) ‘posterior’ and lateral aperture expansion,

Asymmetry of bivalve shell valves between left and right

Snails employ a combination of these two processes to achieve

FIGURE 3.13 The two main types of aperture recognised

vertical shell axis

ing the valves. In monoplacophorans, scaphopods, and shelled

microvilli shell plate stragulum mucoid mucoid

Initial stage of spine formation

organic pellicle calcareous

HAEMOLYMPH MANTLE EPITHELIUM EXTRAPALLIAL SHELL

+ via paracellular pathway +

A- Any exchanged anion ATP Adenosine triphosphate

septate junction vesicle with

Structure of natural pearl Structure of cultured pearl

3.2.6.6 Pearl Formation

inner prismatic layer

Hyolitha cephalopods, but present in some pteriomorphian

share the same mineralogy and that the foliated layer

‘Pores’ 2,3 Absent Sparse Abundant Abundant

The most famous examples are some members of the

2013). For example, Colonese et al. (2013) have analysed

However, a true cuticular layer is found in the mouth region of

Mucus-secreting cells are also present in the epithelia of

ylate groups abundant in the acidic material (Park et al. 2012).

cilia sole 3.3.4 Modifications for Terrestrial Life

Meghimatium (= Incilaria) fruhstorferi (Yamaguchi et al.

(Smith 2010). In stylommatophorans, the peripodial groove

Dorsal surface septate junction

muscle sensory cell

Epithelial tendon shell

in the cell walls of fungi, the exoskeleton of arthropods, and in

nucleus conchiolin (main) layer

concentric with terminal nucleus

concentric with internal nucleus

Sections through opercula

bivalves because they lack a head. It also has other secretory

chemicals are sometimes concentrated on the mantle edge

Some species with ciliary locomotion, such as those in the

Source of data: Schmidt-Rhaesa, A., The Evolution of Organ Systems, Oxford, UK, Oxford