Download Adaptations to Physical Stresses in the Intertidal Zone: The Egg

AMER. ZOOL., 39:230-243 (1999)
Adaptations to Physical Stresses in the Intertidal Zone: The Egg
Capsules of Neogastropod Molluscs1
TIMOTHY A. RAWLINGS 2
Department of Biological Sciences, Florida International University, University Park,
Miami, Florida 33199
SYNOPSIS. The encapsulation of eggs within benthic egg capsules or gelatinous egg
masses is a common phenomenon among many marine invertebrate groups, yet
the functional significance of many aspects of these egg coverings remains unexplored. In this paper I review what is known about the effectiveness of neogastropod egg capsules in protecting embryos from physical stresses associated with the
marine intertidal environment. Egg capsules spawned by intertidal neogastropod
molluscs can provide embryos with significant protection from desiccation, osmotic
stress, and ultraviolet (UV) radiation, relative to embryos devoid of such coverings.
Despite this, capsules desiccate rapidly in air, are highly permeable to small solute
molecules, and are not impervious to incident UV radiation. Egg capsules of intertidal gastropods are also substantially more permeable to water molecules than
the well studied egg cases and egg shells of insects and terrestrial vertebrates and
may be no more effective in protecting embryos from such physical stresses than
the capsules of exclusively subtidal gastropods. Hence, capsular cases appear to be
poorly adapted to protecting embryos from environmental stresses associated with
periodic exposure to air. The degree to which the encapsulated embryos of intertidal neogastropods are protected from environmental stresses thus may be more
reflective of adult spawning site selection and tolerances of encapsulated embryos
to these stresses, than properties of the capsular case, per se. Clearly, however,
there is much still to be learned about the protective nature of capsule walls and
the tremendous diversity of egg coverings that exists within the Gastropoda.
INTRODUCTION
To survive within the intertidal zone of
marine environments, plants and animals
may have to withstand exposure to desiccation, osmotic stress, temperature stress,
and UV radiation, as well as cope with
problems associated with gas exchange and
the accumulation of metabolic wastes during their periodic exposure to air. While
many adult intertidal organisms exhibit
adaptive structural, behavioral, and physiological modifications in response to these
physical stresses {e.g., Foster, 1971; Wolcott, 1973; Vermeij, 1973, 1978), relatively
little is known about the ability of embryonic stages to avoid or tolerate such potential sources of mortality (but see Brawley
and Johnson, 1991). This is surprising givnumerous marine organisms deposit
their eggs within the intertidal zone and that
interspecific differences in the ability of
these
developmental stages to withstand
such
Physical stresses can have profound
consequences for the survival and distnbution
o f
organisms within this habitat,
H o w t h e n d o em
bryos survive within this
environment?
T h e
retention of eggs within tough, multilaminated capsules or elaborate gelatinous
masses may be one means of protecting embr
y ° s f r o m s u c h Physical stresses during
their
development within benthic intertidal
habitats. Such egg coverings are common
amon
g m a n n e representatives of many invertebrate phyla, including the Platyhelminthes, Nemertinea, Annelida, and Mollusca.
1
From the Symposium Aquatic Organisms, Terres- Despite the widespread occurrence of these
trial Eggs: Early Development at the Water's Edge e g g coverings, however, little is known
e n that
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about the
at Boston, Massachusetts.
2
E-mail: [email protected]
lological consequences of depositing embryos within these benthic egg capsules and
230
P r e c i s e morphological and phys-
231
NEOGASTROPOD EGG CAPSULES
gelatinous egg masses. If such egg coverings are "protective," what are they protecting embryos from specifically, and how
do differences in the morphology of these
coverings reflect differences in their ability
to protect embryos? The functional significance of many aspects of these egg capsules
and egg masses remains unexplored.
The few studies that have examined the
protective nature of egg coverings of marine invertebrates have focused largely on
the tough, multi-laminated egg capsules of
neogastropods, a derived group of caenogastropods (Haszprunar, 1988; Harasewych
et ai, 1997). Nearly all marine neogastropod molluscs, from those inhabiting the
depths of the oceans to those living within
the highest intertidal crevices, deposit their
eggs within some form of benthic egg capsule (Ponder, 1973). While the deposition
of eggs within the protective confines of
these capsular cases may have evolved in
response to adverse conditions within the
plankton {e.g., Vance, 1973; Grant, 1980),
the elaborate egg coverings of neogastropods are clearly more than simple bags that
confine embryos during some portion of
their developmental period. Capsule walls
are structurally complex and are composed
of many discrete and chemically distinct
laminae {e.g., Tamarin and Carriker, 1967;
Sullivan and Maugel, 1984; D'Asaro,
1988). Capsule form also varies dramatically within this group, and differences in
shape, size, surface texture, and wall thickness are apparent within families (Thorson,
1935; D'Asaro, 1970, 1988, 1991, 1993,
1997; Bandel, 1973; Robertson, 1974),
among closely-related species (Ostergaard,
1950; Perron, 1981; Perron and Corpuz,
1982; Palmer et ai, 1990; Rawlings and
Palmer, in preparation) and even among
populations of a single species (Rawlings,
1990, 1994, 1995a; Rawlings and Palmer,
in preparation). Differences are also evident
in the strength of capsule walls (Perron,
1981; Rawlings 1990) and the amount of
reproductive energy invested in these extraembryonic products (Perron, 1981; Perron
and Corpuz, 1982). Such variation may thus
reflect differences in the suite of selective
pressures acting upon encapsulated embry-
os in the varied marine habitats in which
they are spawned (see Pechenik, 1986).
The objective of this paper is to review
what is known about the effectiveness of
neogastropod egg capsules in protecting
embryos from physical stresses associated
with an intertidal marine environment. Specifically, I will address the following questions: 1) Are capsules exposed to environmental stresses within the microhabitats in
which they are deposited? 2) Do capsule
walls provide embryos with significant protection from desiccation, osmotic stress and
UV radiation? 3) Do egg capsules spawned
by intertidal gastropods better protect embryos from sources of mortality associated
with periodic exposure to air versus capsules spawned by subtidal gastropods? and
4) Can any features of capsular cases be
associated with an increased resistance to
such stresses? By raising these questions, I
hope to illustrate how much we still have
to learn about the protective nature of capsule walls and also to stimulate further interest in examining the weird and wonderful array of egg coverings produced by gastropod molluscs.
DISCUSSION
Features of neogastropod egg capsules
Neogastropod egg capsules are produced
in an amazing variety of shapes and sizes,
ranging from flat hemispherical disks to tall
erect vases, and spanning a size range from
millimeters to many centimeters in length
{e.g., Bandel, 1973; de Mahieu et al, 1974;
D'Asaro 1991, 1993, 1997; and references
therein). Despite the varied form of these
capsular cases, however, all neogastropod
capsules contain a central fluid-filled chamber that houses embryos for some portion
of their development. Some capsule chambers may also have an opercular opening
bounded by a mucoid plug that seals the
chamber from the external environment and
acts as an escape hatch for planktonic larvae or juvenile snails {e.g., Pechenik,
1975). For species lacking this escape aperture, larvae or juvenile snails emerge
from the capsule once the capsule walls
have deteriorated sufficiently {e.g., Rivest,
1983) or possibly through seams in the cap-
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TIMOTHY A. RAWLINGS
sule wall. Capsules may also have one or
more prominent stalks or basal plates by
which they are attached to hard benthic substrata or to other capsules. The resulting
spawn masses of individual females can
vary dramatically in form, ranging from
small clusters of unattached capsules to
long elaborate chains or huge amorphous
masses, some spanning tens of centimeters
in length (e.g., D'Asaro, 1991, 1993, 1997).
The distinctive shape of neogastropod
capsules derives from an unusual molding
process that occurs within a ventral pedal
gland in the base of the female's foot. Capsular material is initially secreted within the
lumen of a bilobed capsule gland in the pallial region of the female's oviduct (Fretter
and Graham, 1962). Following the deposition of eggs and albumen within this secretion, the capsule leaves the pallial oviduct
in the form of a soft pliable bag filled with
developing embryos. In most species, this
soft capsule is then transferred via a temporary groove in the propodium to the ventral pedal gland (Bingham and Albertson,
1973; Castilla and Cancino, 1976). It is
within this gland that capsules are molded
into their final form and hardened, possibly
through a process of sclerotization (Price
and Hunt, 1973, 1974, 1976). In some species, an additional outer covering may also
be applied to the capsule wall by glandular
secretions of the ventral pedal gland (Ponder, 1973; Sullivan and Maugel, 1984).
The capsule case itself is composed chiefly of proteins and carbohydrates (Bayne,
1968a; Flower et ai, 1969; Hunt, 1966,
1971; Flower, 1973; Price and Hunt, 1973;
Sullivan and Maugel, 1984; Colman, and
Tyler, 1988; Hawkins and Hutchinson,
1988; Miloslavich, 1996), although there is
also evidence for bound lipids within the
capsule wall of some species (Price and
Hunt, 1974; Colman and Tyler, 1988; Miloslavich, 1996). Proteins appear to comprise the bulk of the capsule wall, however,
with amino acids accounting for 78% of the
total weight of the capsular material of the
neogastropod whelk, Buccinum undatum
(Hunt, 1966). The chemical composition of
these proteins appears similar to certain keratin structures (Price and Hunt, 1973), and
the inert nature of the capsule walls and
their resistance to chemical treatment suggests that these proteins are stabilized by
extensive cross-linking, perhaps as the result of tanning (Hunt, 1971; Price and Hunt,
1973, 1974, 1976). Detailed morphological
and histochemical analyses of the egg capsules of Nucella lapillus and other neogastropod capsules have also shown that the
structural and chemical composition of the
capsule wall is not homogeneous throughout (Bayne, 1968a; Sullivan and Maugel,
1984; Colman and Tyler, 1988; D'Asaro,
1988; Hawkins and Hutchinson, 1988; Garrido and Gallardo, 1993; Miloslavich,
1996). Capsule walls are composed of different laminae with different chemical components. The specific role of each of these
laminae has not been determined.
The production of neogastropod egg coverings can represent a substantial energetic
investment relative to free spawning gastropods with no form of parental care. Capsular cases alone account for 40-70% of the
dry weight of whole capsules (including
eggs and intracapsular fluid) of the marine
intertidal gastropod, Nucella emarginata
(Rawlings, 1995a). In energetic terms, capsular cases of marine snails within the genus, Conus, can represent up to 37% of the
energy allocated to whole capsules (Perron,
1981). Wall strength and the proportion of
reproductive energy expended per capsular
case of Conus species also increase with the
development time of encapsulated embryos,
such that species with protracted development are enclosed in tougher, energetically
more expensive capsular cases (Perron,
1981; Perron and Corpuz, 1982). Such results suggest that the energetic costs of producing thicker, stronger capsular cases are
offset by the additional benefits conferred
by increased resistance to environmental
risks in those species with longer development. But what are these capsular cases
shielding embryos from and how does variation in capsule form confer increased resistance to such stresses?
Exposure to the elements
To understand the protective role of capsular cases, it is important to know the environmental conditions within the microhabitats in which these capsules are
NEOGASTROPOD EGG CAPSULES
spawned. Detailed descriptions of these
conditions are critical to determining the
types of stresses that encapsulated embryos
may be exposed to during their development and assessing the ability of capsule
walls to resist such stresses. If capsules are
spawned in microhabitats where physical
stresses such as desiccation, UV radiation,
and osmotic shock are minimized, then
there is little reason to expect that capsule
walls should provide an effective barrier to
such stresses or that variation in capsule
form will represent adaptive responses to
such potential sources of mortality. Where
then are capsules deposited in the field and
what types of stresses are they exposed to?
Spawning locales. Many neogastropod
species exhibit a remarkable specificity for
certain spawning substrata or locations
within intertidal or shallow subtidal marine
environments (e.g., Spight, 1974; Barnett et
al., 1980; Brenchley 1981). Individuals of
the low intertidal muricid gastropod, Nucella lamellosa, for example, continue to
return to the same spawning locations year
after year at some intertidal sites (Spight,
1974; Rawlings, personal observations). In
other species, snails have demonstrated a
significant preference for specific benthic
algae as spawning sites (Barnett et al.,
1980), and the absence of such "suitable"
substrata may limit reproduction entirely
(Brenchley, 1981). Selection of such specific microhabitats does not necessarily indicate that these sites are well protected
from physical or biological stresses, however. Spawning sites selected by Nucella lamellosa often have extremely high mortality rates of encapsulated embryos, with
43% of N. lamellosa capsules failing to produce juvenile hatchlings during one spawning season (Spight, 1977).
While the influence of specific physical
stresses in governing the selection of
spawning sites of neogastropods remains
unclear, qualitative descriptions of these
spawning sites indicate that snails select microhabitats where the intensity of physical
stresses is likely to be ameliorated relative
to surrounding areas. Many temperate intertidal gastropods, for instance, prefer to
spawn their eggs within cool, damp microhabitats (e.g., Emlen, 1966; Spight, 1977;
233
Pechenik, 1978; Gallardo, 1979). The mud
snail, Nassarius obsoletus, deposits its egg
capsules within the holdfasts of the brown
alga, Fucus spp., where encapsulated embryos experience substantially higher survival compared to other available habitats
less protected by algal cover (Pechenik,
1978). Likewise, female Nucella emarginata tend to spawn in areas associated with
a low potential for water loss, where wind
velocities are substantially lower, and humidities higher, than in the surrounding air
(Rawlings, 1995a). For species spanning
large environmental gradients, however, microhabitats used for spawning can vary substantially among locations, reflecting local
differences in the availability of specific
habitats. Capsules shaded under dense algal
canopies at one site can be directly exposed
to solar radiation at another, where such an
algal canopy is absent (Rawlings, 1995a).
The availability of specific microhabitats
can thus have a significant effect on the
types of environmental risks that embryos
may be exposed to during their development.
Microclimatic conditions. Direct measures of microclimatic conditions within
spawning sites also suggest that these locales are not completely buffered from environmental stresses. While few attempts
have been made to record these parameters
in the field, microclimatic conditions within
the spawning sites of the temperate marine
gastropod, Nucella emarginata, have
reached relative humidities as low as 66%,
air temperatures ranging up to 22°C, and
wind speeds of up to 0.3 m/sec, over a period of emersion lasting >7 hours (Rawlings, 1995a). Such conditions can also
vary markedly both within and among microhabitat types (see Brawley and Johnson,
1991; Rawlings, 1995a). The effects of
such physical stresses on encapsulated embryos may be substantially ameliorated by
the arrangement of capsules relative to one
another within a spawn mass, however (see
Bayne, 1969). For instance, water loss from
a capsule over a tidal cycle can vary dramatically depending on whether or not this
capsule is positioned in the center or the
periphery of a clutch (Rawlings, 1995a).
While snails select spawning sites that
234
TIMOTHY A. RAWLINGS
lower the risk of exposure of capsules to
physical stresses, capsules are not completely protected from stresses within these
microhabitats. If embryos are to survive,
therefore, they must either depend on the
capsule wall for further protection or be
able to tolerate exposure to desiccation, rapid changes in osmotic conditions, and UV
radiation. How effective then are capsule
walls in protecting embryos and is there
any evidence to suggest that intertidal egg
capsules may be better at protecting embryos from such stresses than to the capsules
of exclusively subtidal gastropods?
The protective nature of capsule walls
Protection from desiccation. Evidence
that the egg capsules of intertidal neogastropods substantially protect embryos
against desiccation stress remains equivocal. Capsule cases are highly permeable to
water molecules (Pechenik, 1978; 1982,
1983; Hawkins and Hutchinson, 1988). Egg
capsules of the high intertidal gastropod,
Nucella emarginata, for instance, have only
a 10-fold lower diffusivity to water vapor
than air (Rawlings, 1995a), and capsules of
many other intertidal species also appear to
desiccate rapidly in air even under relatively mild conditions (Bayne, 1968&; Pechenik, 1978). Sixteen percent of Nassarius obsoletus capsules exposed to 75% relative
humidity (22-23°C) for 5 hours failed to
release larvae (Pechenik, 1978) and no embryos of the low intertidal gastropod, Nucella lamellosa, survived up to 5 hr exposure to conditions of 70% relative humidity
at 23°C (Spight, 1977). Desiccation has also
been implicated as a primary cause of embryonic mortality within field-deposited
egg capsules (e.g., Emlen, 1966; Feare,
1970; Spight, 1977; Pechenik, 1978), although direct evidence for this is minimal.
Thus, do the walls of neogastropod capsules
really represent a biologically significant
barrier to water loss?
If capsules spawned intertidally are welladapted to protect embryos from desiccation, then one would predict such capsules
to be more resistant to water loss than subtidal capsules. Surprisingly, no evidence
supports this contention. Pechenik (1978)
determined that capsules of the intertidal
snail, Nassarius obsoletus, did not desiccate
more slowly than capsules produced by
their subtidal congener, Nassarius trivittatus. Likewise, Bayne (1968£>) found a relatively similar rate of water loss per unit
surface area from intertidal egg capsules of
Nucella lapillus versus shallow-water gelatinous egg masses of Aplysia punctata
and Lymnaea stagnalis. Since both studies
measured desiccation rates in either still or
slow-moving air, however, these results
should be interpreted with caution (see
Ramsay, 1935): under such conditions, estimates of water loss may largely reflect the
resistances of boundary layers rather than
the capsule wall or jelly mass. To understand the dynamics of water loss from these
egg coverings, therefore, it is important to
know the resistance of both the capsule wall
and boundary layer to water loss under a
variety of wind conditions, as well as the
specific microclimatic conditions that intertidal capsules are exposed to in the field.
The egg coverings of many fully terrestrial organisms appear to provide embryos
with more substantial protection from the
rigors of desiccation than the capsule walls
of marine intertidal gastropods. Although
quantitative estimates of the resistance of
egg coverings of marine intertidal and terrestrial gastropods to water loss are rare, estimates for egg shells and cases of other
terrestrial organisms are common. For instance, bird egg shells exhibit resistances of
=38,500 s/m under conditions of moving
air (assuming a shell thickness of 0.3 mm;
Spotila et al., 1981). Insect egg membranes
are also extremely resistant to water loss
(McFarlane, 1966, 1970), and eggs of some
species can withstand incubation at low humidities (e.g., <5% relative humidity) for
days to weeks without any net water loss
(Biemont et al., 1981). The parchment
shelled eggs of lizards and snakes have resistances to water loss that are considerably
lower, however, ranging from 210 to 526
s/m (24-26°C) in conditions of still air
(Ackerman et al., 1985). Nevertheless,
these values are still an order of magnitude
higher than the capsule wall resistance of
the high intertidal gastropod, Nucella emarginata, which ranges from 22.4 to 33.6 s/m
(assuming a wall thickness of 53 to 79 u,m;
NEOGASTROPOD EGG CAPSULES
Rawlings, 1995a). Thus, if the capsule
walls of N. emarginata can be considered
representative of other intertidal neogastropod capsules, these egg coverings are substantially more permeable to water than the
egg coverings of terrestrial vertebrates and
insects. Quantitative estimates of shell resistances are now needed from terrestrial
gastropod egg shells for comparison.
The rate of water loss from the central
chamber containing encapsulated embryos
depends both on the resistance of the capsule wall (or shell) to water movement and
on the resistance of the surrounding boundary layer. Because the resistance of bird egg
shells to water transport ranges from 200 to
685 times greater than the resistance of the
boundary layer, a decrease in boundary layer thickness associated with increasing
wind speed has negligible effects on water
loss from avian eggs (Tracy and Sotherland,
1979; Spotila et al., 1981). This is in significant contrast to capsules of reptiles
where the egg shell and boundary layer resistances are usually within the same order
of magnitude (Ackerman et al., 1985), and
thus, desiccation rates are very sensitive to
air movement. Boundary layer resistances
for Nucella emarginata capsules have been
estimated to decline from >70 s/m to 32 s/
m over an increase in wind speed from 0—
1.5 m/sec, compared to capsule wall resistances of 22-34 s/m (Rawlings, 1995a).
Hence, given that these capsules are normally exposed to relatively low wind velocities in the field (<0.3 m/sec), under
conditions where the boundary layer resistance is almost double that of the capsule
wall resistance, rates of water loss from TV.
emarginata egg capsules are largely governed by the thick boundary layer rather
than by the capsule wall. If the capsule wall
resistances of other intertidal neogastropods
are substantially higher than N. emarginata
capsules, or these capsules are exposed to
more severe wind velocities in the field,
however, the capsule wall could play a
more critical role in influencing rates of water loss.
To understand the role of capsule walls
in protecting embryos from desiccation, it
is also important to understand how variation in capsule traits, including wall micro-
235
structure, wall thickness, wall stiffness, capsule shape, and surface sculpture, can affect
the resistance of the capsule wall and
boundary layer to water loss. Simple diffusion models of water loss from capsules
of Nucella emarginata suggest that variation in capsule size, shape, and wall thickness, can profoundly affect the rate of water
loss from the capsule chamber and, consequently, the survival of encapsulated embryos (Rawlings, 1995a). The specific benefits of increased wall thickness and a lower
surface area/volume ratio, however, will depend on the severity of microclimatic conditions that capsules are exposed to in the
field (Rawlings, 1995a). Capsule wall stiffness may also have an important influence
on rates of water loss from neogastropod
capsules (Daniel and Pechenik, unpublished
data). Stiffer capsule walls appear to reduce
rates of desiccation by increasing the resistance of the capsule wall to deformation associated with water loss from the capsule
chamber ( see Feder et al., 1982). Given,
therefore, that variation in some capsule
traits can potentially affect the survival of
encapsulated embryos exposed to desiccation, is there any evidence of adaptive variation in the expression of these traits
among intertidal egg capsules? Surprisingly, no studies have compared these features
of neogastropod capsules between intertidal
and subtidal habitats, or even between intertidal and subtidal congeners. To date,
therefore, there is no evidence of habitatrelated differences in capsule form suggestive of adaptive responses to desiccation.
Protection from osmotic shock. While
capsule walls of many intertidal neogastropods are permeable to water and salts, capsular cases may still play an important role
in protecting embryos from low-salinity
stress under conditions similar to those encountered during a rainstorm at low tide
(Pechenik, 1982, 1983). Embryos removed
from the capsule chamber, for instance, suffer significantly higher mortality than encapsulated embryos when exposed to conditions of low salinity (Pechenik, 1982,
1983), even though the intracapsular solute
concentration will eventually approach
close to that of the surrounding environment (Pechenik, 1982, 1983; Hawkins and
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TIMOTHY A. RAWLINGS
Hutchinson, 1988; Roller and Stickle,
1989). Capsule walls thus appear to confer
higher embryonic survival by reducing the
rate of salinity change within the capsule
chamber, possibly allowing time for mechanisms that regulate the cellular volumes of
encapsulated embryos to adjust to the
changing osmotic environment (Woods and
DeSilets, 1997). Enclosure within capsule
walls, however, does not guarantee the survival of embryos exposed to hypo- or hypersaline conditions. Substantial mortality
of encapsulated embryos can occur in some
intertidal species even after relatively short
exposures of capsules to low or high salinities (Pechenik, 1982, 1983; Hawkins and
Hutchinson, 1988).
Do intertidal egg capsules exhibit any
specific adaptations to protect embryos
from osmotic stress relative to the capsular
cases of subtidal gastropods? While capsule
walls of different intertidal species vary significantly in their permeability to salt molecules (Pechenik, 1982, 1983), permeabilities of intertidal and exclusively subtidal
gastropod capsule walls have not been compared. Features of the multilaminated capsule wall that determine the permeability to
small solute molecules also remain largely
unexplored. Does one lamina provide the
rate limiting step and if so, do the properties
of this lamina vary among species? Pechenik (1982, 1983) observed that the thick
outer capsule wall of Nucella spp. provided
the primary barrier to solute diffusion, but
did not determine if the permeability to solute molecules varied among laminae within
this outer wall. Interestingly, interspecific
differences in the rate of solute exchange
across the capsule were not related to the
thickness of the outer wall, however, thus
suggesting that wall permeability is not a
simple function of wall thickness (Pechenik, 1982, 1983). Additional studies of capsule wall microstructure are now required
to understand how capsular wall permeabilities differ among species and if the
ability of capsule walls to protect embryos
from osmotic shock is an attribute of intertidal capsules alone or a general feature of
all neogastropod egg capsules.
Protection from ultraviolet radiation.
The ability of the egg coverings of marine
gastropods to protect embryos from exposure to UV radiation is only just beginning
to be explored. The gelatinous coverings of
shallow water opisthobranch egg masses,
for instance, do not appear to provide embryos with much protection from exposure
to direct solar radiation, although embryos
embedded deeper within these egg masses
do survive better than peripheral embryos
(Biermann et al., 1992). The tough capsular
cases of neogastropod molluscs, however,
may be much more effective shields against
UV radiation. Capsule walls of the intertidal whelk, Nucella emarginata, allow <5%
UV-B (300 nm) and <55% UV-A (360 nm)
to cross the capsule wall, and capsules of
congeners, N. lamellosa, and N. canaliculata, also absorb a significant fraction of incident UV radiation (Rawlings, 1996). Interestingly, variation in the UV-absorbing
properties of these species appears related
to the frequency of exposure of capsules to
solar radiation. Nucella lamellosa typically
has a lower intertidal distribution than N.
canaliculata and N. emarginata (Palmer,
1980), resulting in reduced exposure to UV
radiation due to the attenuation of short
wavelengths of radiation in seawater. Correspondingly, the thinner-walled N. lamellosa capsules are significantly more transparent to UV radiation than thicker-walled
capsules of the higher intertidal species
(Rawlings, 1996). The generality of this
trend among egg capsules from other high
and low intertidal species now remains to
be tested.
Given that some intertidal neogastropod
capsules may protect embryos from UV radiation, the question remains as to how capsules absorb this radiation and also how
prevalent this characteristic is among intertidal and subtidal neogastropod species.
While mycosporine-like amino acids
(MAAs) have been identified as biochemical defenses against UV in many marine
gastropods, including the neogastropod
snail Trophon cf. geversianus, MAAs do
not appear to be present in their capsular
cases (Karentz et al., 1991a; Rawlings,
1996). Since UV absorption is dependent
on the thickness of the capsule wall and
there is no polarity to UV absorption across
the wall of N. emarginata capsules (Raw-
NEOGASTROPOD EGG CAPSULES
lings, 1996), the UV-absorbing properties
of capsules appear associated with some
general component of the outer capsule
wall itself. One candidate component is a
yellow fluorophore, identified in the capsule
walls of a subtidal neogastropod, Buccinum
undatum (Price and Hunt 1974), that is covalently bound to peptides within the capsule wall and fiuoresces under UV illumination. While this fluorophore is not associated with material secreted by the capsule
gland, capsules of B. undatum do fluoresce
once they are molded and hardened within
the ventral pedal gland, suggesting that the
product originates in this gland (Price and
Hunt, 1976). Since similar fluorescence has
been observed from structural proteins of
molluscs, arthropods and mammals observed under UV illumination (Price and
Hunt, 1976, and references therein), however, this feature of capsule walls may be a
byproduct of tanning and thus not necessarily an adaptive attribute of intertidal capsular cases.
Is UV-absorption specific to intertidal
capsules or is it a general property of all
neogastropod capsules? Unfortunately, we
do not know enough about the spectral
properties of neogastropod capsular cases to
be able to answer this question. If capsule
walls of the exclusively subtidal neogastropod, Buccinum undatum, also exhibit the
same UV-absorbing properties as N. emarginata, as suggested by the experiments of
Price and Hunt (1974), this would indicate
that UV-absorbance is not exclusive to intertidal capsules. Further research is now
needed to examine the spectral properties of
neogastropod egg capsules collected from
other intertidal and subtidal habitats and to
explore the mechanisms by which capsule
walls may protect embryos from UV radiation.
Tolerance of embryos to physical stresses
Given that capsules desiccate rapidly in
air, are highly permeable to small solute
molecules, and are not impervious to incident UV radiation, survival of encapsulated
embryos exposed to physical stresses in the
intertidal zone may depend less on the
properties of the capsule wall, per se, and
more on the ability of embryos to tolerate
237
poor conditions. If so, one might expect the
embryos of intertidal neogastropods to be
able to withstand significant exposure to
desiccation, osmotic stress, and UV radiation, and to tolerate more extreme conditions than the embryos of strictly subtidal
species. Is there any evidence to support
this?
While the capsular cases of marine intertidal gastropods may not resist water loss
as well as terrestrial egg coverings, the encapsulated embryos of intertidal species appear able to tolerate water loss as well as
some terrestrial species. Late-stage Nucella
emarginata embryos, for instance, can
withstand up to 80% water loss from the
capsule chamber before suffering substantial mortality (Rawlings, 1995a). Interestingly, mortality in this experiment may
have resulted largely from buckling capsule
walls rather than from stress-related causes
associated with increased salinity (Rawlings, 1995a). In contrast, embryos of the
terrestrial slug Agriolimax can survive 6080% weight loss from their shelled eggs
and those of Limax flavus 85% weight loss
before death (Carmicheal and Rivers, 1932;
Bayne, 1969). Older embryos of Agriolimax, like Nucella emarginata, also tolerate
desiccation better than younger embryos
(Bayne, 1969; Rawlings, 1995a), although
this may not be true for other species {e.g.,
Carmicheal and Rivers, 1932). Unfortunately, comparative data on the desiccation tolerances of subtidal neogastropod embryos
are lacking. Hence, it remains to be determined if the ability of embryos to tolerate
extensive water loss from the capsule or
shelled egg is an attribute of all encapsulated gastropod embryos or only those exposed to aerial environments.
The ability of embryos to tolerate extensive water loss from the capsule chamber
also implies an underlying ability to withstand tremendous fluctuations in solute concentration. Increasing solute concentration
is associated with water loss from both animals and plants (Slayter, 1967). For instance, death by desiccation of intertidal
limpets may be attributed entirely to the
high concentration of internal solutes resulting from evaporative water loss (Wolcott, 1973). Likewise, mortality of intertidal
238
TIMOTHY A. RAWLINGS
barnacles from desiccation is associated
with a substantial increase in solute concentrations in the blood (Foster, 1971). In general, however, little is known about the ability of neogastropod embryos to survive exposure to low or high salinities. Encapsulated embryos of intertidal Nucella spp. can
tolerate low salinity conditions, yet their
survival depends on the rate of salinity
change, the duration of exposure, and the
development stage of these embryos (Pechenik, 1982, 1983). The ability of excapsulated embryos (i.e., embryos removed from
the capsule chamber) to withstand osmotic
shock also differs among these species, although it is not known if this result reflects
underlying differences in the osmoregulatory or volume regulatory capabilities of these
embryos (Pechenik, 1982). It also remains
unclear if intertidal embryos are better
adapted to withstanding osmotic stress than
the embryos of subtidal species. Encapsulated embryos of at least one subtidal species
can develop successfully over salinities
ranging from I5%o to 35%o, although development is prolonged and survival reduced at
salinities lower than 15%o (Roller and Stickle, 1989). Thus, embryos of subtidal species
may be just as well equipped to deal with
changes in their osmotic environment as embryos of intertidal neogastropods. Future research must attempt to explore the mechanisms by which encapsulated embryos adjust to changes in solute concentration within the capsule chamber, and to compare the
tolerances of encapsulated embryos from intertidal and subtidal species directly.
Although little is known about the ability
of neogastropod embryos to tolerate UV radiation, it is possible that these embryos can
withstand exposure to UV radiation or even
repair its damaging effects. Some aquatic
organisms, for instance, exhibit an elevated
tolerance to UV radiation that is associated
with a) higher levels of enzymes involved
in the repair of nucleic acids damaged by
UV (e.g., Karentz et al, \99lb; Blaustein
et al, 1994), b) increased pigmentation
(Garcia-Pichel and Castenholz, 1991), or c)
the presence of UV-absorbing or reflecting
compounds in the body (e.g., Shibata, 1969;
Cheng et al, 1977; Jokiel and York, 1982;
Dunlap et al, 1986; Karentz et al., 1991a;
Shick et al., 1992). Recently, many marine
species have been found to depend largely
on MAAs, with absorption maxima between 310 and 360 nm, for increased protection from harmful UV radiation, with
higher concentrations of MAAs present in
shallow versus deep populations of corals
(e.g., Dunlap et al., 1986), and in locations
of the body more vulnerable to UV exposure (e.g., Shick et al., 1992). In fact,
MAAs have also been recorded in the eggs
of limpets with planktonic development
(Karentz et al., 1992), and in the gelatinous
masses (including eggs) of the sea hare,
Aplysia dactylomela (Carefoot et al., 1998).
To date, however, no MAAs have been extracted from the encapsulated embryos of
neogastropods despite at least one attempt
(Karentz et al., 1991a; D. Karentz, personal
communication). Whether the apparent lack
of MAAs in these embryos is a consequence of poor sampling or reflects the fact
that the capsule walls of neogastropods provide these embryos with sufficient protection from UV radiation remains to be determined.
Does any evidence exist to suggest that
encapsulated embryos of intertidal neogastropods are better adapted to withstanding
exposure to physical stresses than the embryos of strictly subtidal species? Unfortunately, we still know too little about the tolerances of encapsulated embryos to these
stresses, and the mechanisms involved in
protecting embryos, to make any generalizations; nevertheless, the evidence to date
is not overwhelming. Further studies are
now needed to address this question specifically and to compare the tolerances of both
encapsulated and excapsulated embryos to
these physical stresses. Along these lines,
research is currently underway to compare
the oxygen consumption and ammonia tolerance of encapsulated embryos of three
species of Nucella during periods of emersion and immersion (Newel and Bourne,
1997). Because these three species occupy
different vertical positions within the intertidal zone, their capsules spend differing
lengths of time exposed to an aerial environment. By comparing the effect of nitrogenous waste accumulation on the metabolic
rates of encapsulated embryos during emer-
NEOGASTROPOD EGG CAPSULES
sion, therefore, we may begin to understand
how embryos cope with physical stresses
encountered within the intertidal zone and
to determine if there is any evidence of
adaptive variation in the responses of embryos to these stresses.
Adaptations to the intertidal zone
Given that there is little evidence to indicate that the capsules of intertidal neogastropod molluscs are more resistant to
desiccation, osmotic stress or UV radiation
than capsules of subtidal species, capsular
cases do not appear well-adapted to protect
embryos from local physical stresses within
the marine intertidal zone (see also Pechenik, 1983). In part, this result may reflect
the fact that we know very little about the
functional significance of many features of
neogastropod egg capsules and that few
comparisons have been made between the
properties of intertidal and subtidal neogastropod capsules. Nevertheless, since capsule
walls provide embryos with only partial
protection from desiccation stress, osmotic
shock, and UV radiation, and capsules appear only weakly resistant to these stresses
relative to the egg cases of many fully terrestrial organisms, the selection of benign
capsule deposition sites may be the most
important factor affecting embryo survival.
If capsule walls provide relatively little
protection from physical stresses within the
marine environment, then why do neogastropod molluscs invest so much energy in
making these cases and what explains the
stunning variety of capsule forms? One of
the chief benefits associated with encapsulating eggs may not be protection against
physical stresses, but rather protection
against micro-organisms and intertidal and
subtidal predators. Predation on the encapsulated eggs of many neogastropod species
can be severe {e.g., MacKenzie, 1961; Emlen, 1966; Phillips, 1969; West, 1973; Race,
1982; Abe, 1983; Rawlings, 1990), and
while capsular cases are rarely invulnerable
to potential predators, capsule walls do protect embryos from a number of them {e.g.,
Spight, 1977; Brenchley, 1982; Rawlings,
1990, 1994). Likewise, variation in capsule
features, such as the thickness of capsule
walls, can have significant effects on the
239
vulnerability of encapsulated embryos to
some predators (Rawlings, 1990, 1994) and
the absence of specific capsule laminae can
dramatically increase the susceptibility of
embryos to attack by bacteria and microorganisms (Lord, 1986; Rawlings, 1995i>).
Perron (1981) has also suggested that the
production of tougher, energetically moreexpensive capsular cases in Conus spp. with
protracted development may reflect adaptive responses associated with increased exposure to shallow-water capsule-eating
predators. Variation in capsule form may
thus be more reflective of differential defenses against biotic factors than against
physical stresses.
Future directions
The joint mapping of spawn characteristics and other life-history and ecological
attributes onto well-supported phylogenies
of gastropod groups represents a promising
opportunity to understand the adaptive significance of gastropod egg coverings more
fully. While some attempts to interpret the
direction of spawn evolution within and
among neogastropod families have suffered
from the lack of robust phylogenies {e.g.,
Bandel, 1973; Ponder, 1973), the recent development of well supported morphological
and molecular phylogenies has enabled
spawn evolution to be tracked within specific gastropod clades (Reid, 1990, 1991;
Kool, 1993; Rawlings and Palmer, in preparation). These studies have provided the
opportunity to examine capsule features
within a phylogenetic context, thus enabling formal comparative tests of adaptive
explanations {sensu Harvey and Pagel,
1991). As yet, however, no phylogenetic
comparative studies have addressed questions concerning the adaptive features of intertidal neogastropod egg capsules. Nevertheless, future studies will be able to examine changes in capsule form associated
with the movement of gastropods into or
away from marine intertidal environments,
thereby, allowing those capsule features
that reflect adaptive responses to physical
and biological stresses in the intertidal zone
to be identified.
To date, however, attempts to provide
adaptive explanations for derived forms of
240
TIMOTHY A. RAWLINGS
gastropod egg coverings, even within closely-related groups of gastropods, have met
only with modest success (e.g., Reid, 1990;
Kool, 1993). Often, because spawn products have been described for relatively few
species within the group of interest, and because only general information is available
on the life-histories or habitat types of these
gastropods, comparative tests of adaptive
explanations are weak. Likewise, since so
few studies have tested the functional significance of specific capsule traits independently, support for the tentative conclusions
of such comparative tests has also been
lacking. Thus, given our poor understanding of the functions of such egg coverings,
simply knowing the direction of spawn evolution and associated changes in environmental conditions may not be enough to interpret the adaptive significance of subtle
changes in spawn morphology.
Recent interest in using phylogenetic relationships to infer adaptive explanations
for the evolution of gastropod egg coverings thus must be balanced with similar enthusiasm for examining and describing the
spawn products of neogastropod molluscs
and investigating the functional properties
of these egg coverings (see Pechenik,
1986). In addition, interpretations of the
adaptive significance of neogastropod egg
capsules must consider not only the protective benefits of enclosing eggs within capsules in response to biotic and abiotic
stresses (as in Pechenik, 1978, 1982, 1983;
Perron, 1981; Brenchley, 1982; Hawkins
and Hutchinson, 1988; Rawlings, 1990,
1994, 1996), but also the energetic costs of
capsule production (Perron, 1981), and the
diffusive constraints associated with the encasing embryos behind thick-walled barriers (Rawlings and Bourne, in preparation).
Recent studies have demonstrated significant diffusive constraints associated with
the packaging of eggs within the gelatinous
masses of opisthobranch gastropods (see
Strathmann and Chaffee, 1984; Strathmann
and Strathmann, 1989, 1995; Cohen and
Strathmann, 1996; Lee and Strathmann,
1998). Such constraints may also have
played an important role in the evolution of
neogastropod egg capsules.
ACKNOWLEDGMENTS
I would like to thank Karen Martin and
Richard Strathmann for the opportunity to
participate in this symposium, and The Society for Integrative and Comparative Biology for providing travel support to attend
this meeting. I am also indebted to Louis
Gosselin, Michael Newel, Paul Verrell, and
two anonymous reviewers for their comments on this paper, and to my Ph.D. supervisor, Rich Palmer, for all his advice and
encouragement. Many of the ideas in this
paper were spawned during my dissertation
research on neogastropod egg capsules at
the University of Alberta, Edmonton, Alberta, and the Bamfield Marine Station,
Bamfield, British Columbia, Canada. Support for this research was provided by an
NSERC operating grant to Dr. A. R. Palmer.
REFERENCES
Abe, N. 1983. Breeding of Thais clavigera (Kuster)
and predation of its eggs by Cronia margariticola
(Broderip). In B. Morton and D. Dudgeon (eds.).
Proceedings of the Second International Workshop on the Malacofauna of Hong Kong and
Southern China, pp. 381-392. Hong Kong University Press, Hong Kong.
Ackerman, R. A., R. Dmi'el, and A. Ar. 1985. Energy
and water vapor exchange by parchment-shelled
reptile eggs. Physiol. Zool. 58:129-137.
Bandel, K. 1973. Spawning and development of some
Columbellidae from the Caribbean sea of Columbia (South America). Veliger 16:271-282.
Barnett, P. R. O., B. L. S. Hardy, and J. Watson. 1980.
Substratum selection and egg-capsule deposition
in Nassarius reticulatus (L.). J. Exp. Mar. Biol.
Ecol. 45:95-103.
Bayne, C. J. 1968a. Histochemical studies on the egg
capsules of eight gastropod molluscs. Proc. Malac.
Soc. London 38:199-212.
Bayne, C. J. 19686. A study of the desiccation of egg
capsules of eight gastropod species. J. Zool., London 155:401-411.
Bayne. C. J. 1969. Survival of embryos of the grey
field slug Agriolimax reticulatus, following desiccation of the egg. Malacologia 9:391-401.
Biemont, J. C . G. Chauvin, and C. Hamon. 1981. Ultrastructure and resistance to water loss in eggs of
Acanthoscelides obtectus Say (Coleoptera: Bruchidae). J. Insect. Physiol. 27:667-679.
Biermann C. H., G. O. Schinner, and R. R. Strathmann.
1992. Influence of solar radiation, microalgal fouling, and current on deposition site and survival of
embryos of a dorid nudibranch gastropod. Mar.
Ecol. Prog. Ser. 86:205-215
Bingham, F. O. and H. D. Albertson. 1973. Observations on the attachment uf egg capsules to a .substrate by Melongena corona. Veliger 16:233—237.
NEOGASTROPOD EGG CAPSULES
Blaustein A. R., P. D. Hoffman, D. G. Hokit, J. M.
Kiesecker, S. C. Walls, and J. B. Hays. 1994. UV
repair and resistance to solar UV-B in amphibian
eggs: A link to population declines? Proc. Natl.
Acad. Sci. U.S.A. 91:1791-1795
Brawley, S. H. and L. E. Johnson. 1991. Survival of
fucoid embryos in the intertidal zone depends on
development stage and microhabitat. J. Phycol.
27:179-186.
Brenchley, G. A. 1981. Limiting resources and the limits to reproduction in the "mud" snail Ilyanassa
obsoleta in Barnstable Harbor, Massachusetts.
Biol. Bull. 161:323A
Brenchley, G. A. 1982. Predation on encapsulated larvae by adults: effects of introduced species on the
gastropod Ilvanassa obsoleta. Mar. Ecol. Prog.
Ser. 9:255-262.
Carefoot, T. H., M. Harris, B. E. Taylor, D. Donovan,
and D. Karentz. 1998. Mycosporine-like amino
acids: possible UV protection in eggs of the sea
hare Aplysia dactylomela. Mar. Biol. 130:389—
396.
Carmichael, E. B. and T. D. Rivers. 1932. The effects
of dehydration upon the hatchability of Limaxflavus eggs. Ecology 13:375—380.
Castilla, J. C. and J. Cancino. 1976. Spawning behaviour and egg capsules of Concholepas concholepas (Mollusca: Gastropoda: Muricidae). Mar.
Biol. 37:255-263.
Cheng, L., M. Douek, and D. A. I. Goring. 1977. UV
absorption by gerrid cuticles. Limnol. Oceanogr.
23:554-556.
Cohen, C. S. and R. R. Strathmann. 1996. Embryos at
the edge of tolerance: Effects of environment and
structure of egg masses on supply of oxygen to
embryos. Biol. Bull. 190:8-15.
Colman, J. G. and P. A. Tyler. 1988. The egg capsules
of Colus jeffreysianus (Fischer. 1868) (Prosobranchia: Neogastropoda) from the Rockall Trough,
North East Atlantic. Sarsia 73:139-145.
D'Asaro, C. N. 1970. Egg capsules of prosobranch
mollusks from south Florida and the Bahamas and
notes on spawning in the laboratory. Bull. Mar.
Sci. 20:414-440.
D'Asaro, C. N. 1988. Micromorphology of neogastropod egg capsules. Nautilus 102:134—148.
D'Asaro, C. N. 1991. Gunnar Thorson's world-wide
collection of prosobranch egg capsules: Muricidae. Ophelia 35:1-101.
D'Asaro, C. N. 1993. Gunnar Thorson's world-wide
collection of prosobranch egg capsules: Nassariidae. Ophelia 38:149-215.
D'Asaro, C. N. 1997. Gunnar Thorson's world-wide
collection of prosobranch egg capsules: Melongenidae. Ophelia 46:83-125.
de Mahieu, G. C , P. E. Penchaszadeh, and A. B. Casal.
1974. Algunos aspectos de las variaciones de proteinas y aminoacidos libres totales del liquido intracapsular en relacion al desarrollo embrionario
en Adelomelon brasiliana (Lamarck, 1811) (Gastropoda, Prosobranchia, Volutidae) (I). Cah. Biol.
Mar. XV: 215-227.
Dunlap W. C , B. E. Chalker, and J. K. Oliver. 1986.
Bathymetric adaptations of reef-building corals at
241
Davies Reef, Great Barrier Reef, Australia. III.
UV-B absorbing compounds. J. Exp. Mar. Biol.
Ecol. 104:239-248.
Emlen, J. M. 1966. Time, energy and risk in two species of carnivorous gastropods. Ph.D. Diss. University of Washington, Seattle, Washington.
Feare, C. J. 1970. Aspects of the ecology of an exposed shore population of dogwhelks Nucella lapillus (L.). Oecologia 5:1-18.
Feder, M. E., S. L. Satel, and A. G. Gibbs. 1982. Resistance of the shell membrane and mineral layer
to diffusion of oxygen and water in flexibleshelled eggs of the snapping turtle (Chelydra serpentina). Resp. Physiol. 49:279-291.
Flower, N. E., A. J. Geddes, and K. M. Rudall. 1969.
Ultrastructure of the fibrous protein from the egg
capsules of the whelk Buccinum undatum. J. Ultrastruct. Res. 26:262-273.
Flower, N. E. 1973. The storage and structure of proteins used in the production of egg capsules by
the mollusc Cominella maculosa. J. Ultrastruct.
Res. 44:134-145.
Foster, B. A. 1971. Desiccation as a factor in the intertidal zonation of barnacles. Mar. Biol. 8:12—29.
Fretter, V. and A. Graham. 1962. British prosobranch
molluscs. Ray Society, London.
Gallardo, C. S. 1979. Developmental pattern and adaptations for reproduction in Nucella crassilabrum
and other muricacean gastropods. Biol. Bull. 157:
453-463.
Garcia-Pichel, F. and R. W. Castenholz. 1991. Characterization and biological implications of scytonemin, a cyanobactenal sheath pigment. J. Phychol. 27:395-409.
Garrido, O. and C. S. Gallardo. 1993. Ultraestructura
de la capsula ovifera de Concholepas concholepas
(Brugiere, 1789) (Gastropoda: Muricidae). Rev.
Biol. Mar. 28:191-201.
Grant, A. 1980. On the evolution of brood protection
in marine benthic invertebrates. Am. Nat. 122:
549-555.
Harasewych, M. G., S. L. Adamkewicz, J. A. Blake,
D. Saudek, T. Spriggs, and C. J. Bult. 1997. Neogastropod phylogeny: A molecular perspective. J.
Moll. Stud. 63:327-351.
Harvey, P. H. and M. D. Pagel. 1991. The comparative
method in evolutionary biology. Oxford University Press, Oxford, UK.
Haszprunar, G. 1988. On the origin and evolution of
major gastropod groups, with special reference to
the Streptoneura. J. Moll. Stud. 54:367-441.
Hawkins, L. E. and S. Hutchinson. 1988. Egg capsule
structure and hatching mechanism of Ocenebra
erinacea (L.) (Prosobranchia: Muricidae). J. Exp.
Mar. Biol. Ecol. 119:269-283.
Hunt, S. 1966. Carbohydrate and amino-acid composition of the egg capsule of the whelk Buccinum
undatum L. Nature 210:436-437.
Hunt, S. 1971. Comparison of the three extracellular
structural proteins in the gastropod mollusc Buccinum undatum L., the periostracum, egg capsule
and operculum. Comp. Biochem. Physiol. 40B:
37-46.
Jokiel, P. L. and R. H. York, Jr. 1982. Solar ultraviolet
242
TIMOTHY A. RAWLINGS
photobiology of the reef coral Pocillopora damicornis and symbiotic zooxanthellae. Bull. Mar.
Sci. 32:301-315.
Karentz, D., F. S. McEuen, M. C. Land, and W. C.
Dunlap. 1991a. Survey of mycosporine-like amino acid compounds in Antarctic marine organisms: Potential protection from ultraviolet exposure. Mar. Biol. 108:157-166.
Karentz, D., J. E. Cleaver, and D. L. Mitchell. 19916.
Cell survival characteristics and molecular responses of Antarctic phytoplankton to ultravioletB radiation. J. Phycol. 27:326-341.
Karentz, D., I. Bosch, and W. C. Dunlap. 1992. Distribution of UV-absorbing compounds in the antarctic limpet, Nacella concinna. Antarct. J. U.S.
27:121-122.
Kool, S. P. 1993. Phylogenetic analysis of the Rapaninae (Neogastropoda: Muricidae). Malacologia 35:
155-259.
Lee, C. E. and R. R. Strathmann. 1998. Scaling of
gelatinous clutches: Effects of siblings' competition for oxygen on clutch size and parental investment per offspring. Am. Nat. 151:293-310.
Lord, A. 1986. Are the contents of egg capsules of the
marine gastropod Nucella lapillus (L.) axenic?
Am. Malac. Bull. 42:201-203.
MacKenzie, C. L., Jr. 1961. Growth and reproduction
of the oyster drill Eupleura caudata in the York
River, Virginia. Ecology 42:317-338.
McFarlane, J. E. 1966. The permeability of the cricket
eggshell to water. J. Insect. Physiol. 12:15671575.
McFarlane, J. E. 1970. The permeability of the cricket
egg shell. Comp. Biochem. Physiol. 37:133—141.
Miloslavich, P. 1996. Biochemical composition of
prosobranch egg capsules. J. Moll. Stud. 62:133135.
Newel, M. S. and G. B. Bourne. 1997. Physiological
constraints on the development of the egg capsules of Nucella spp. (Gastropoda: Muricidae).
Amer. Zool. 37:554A
Ostergaard, J. M. 1950. Spawning and development of
some Hawaiian marine gastropods. Pac. Sci. 4:75115.
Palmer, A. R. 1980. A comparative and experimental
study of feeding and growth in thaidid gastropods.
Ph.D. Diss. University of Washington, Seattle.
Palmer, A. R., S. D. Gayron, and D. S. Woodruff.
1990. Reproductive, morphological, and genetic
evidence for two cryptic species of northeastern
Pacific Nucella. Veliger 33:325-338.
Pechenik, J. A. 1975. The escape of veligers from the
egg capsules of Nassarius obsoletus and Nassarius trivittalus (Gastropoda, Prosobranchia). Biol.
Bull. 149:580-589.
Pechenik, J. A. 1978. Adaptations to intertidal development: Studies on Nassarius obsoletus. Biol.
Bull. 154:282-291.
Pechenik, J. A. 1982. Ability of some gastropod egg
capsules to protect against low-salinity stress. J.
Exp. Mar. Biol. Ecol. 63:195-208.
Pechenik, J. A. 1983. Egg capsules of Nucella lapillus
(L.) protect against low-salinity stress. J. Exp.
Mar. Biol. Ecol. 71:165-179.
Pechenik, J. A. 1986. The encapsulation of eggs and
embryos by molluscs: An overview. Am. Malacol.
Bull. 4:165-172.
Perron, F. E. 1981. The partitioning of reproductive
energy between ova and protective capsules in
marine gastropods of the genus Conus. Am. Nat.
118:110-118.
Perron, F. E. and G. C. Corpuz. 1982. Cost of parental
care in the gastropod Conus pennaceus: Age specific changes and physical constraints. Oecologia
55:319-324.
Phillips, B. F. 1969. The population ecology of the
whelk Dicalhais aegrola in western Australia.
Aust. J. Freshw. Res. 20:225-265.
Ponder, W. F. 1973. The origin and evolution of the
Neogastropoda. Malacologia 12:295—338.
Price, N. R. and S. Hunt. 1973. Studies of the crosslinking regions of whelk egg-capsule proteins.
Biochem. Soc. Trans. 1:158-159.
Price, N. R. and S. Hunt. 1974. Fluorescent chromophore components from the egg capsules of the
gastropod mollusc Buccinum undatum (L.), and
their relation to fluorescent compounds in other
structural proteins. Comp. Biochem. Physiol. 47B:
601-616.
Price, N. R. and S. Hunt. 1976. An unusual type of
secretory cell in the ventral pedal gland of the
gastropod mollusc Buccinum undatum L. Tiss.
Cell. Res. 8:217-228.
Race, M. S. 1982. Competitive displacement and predation between introduced and native mud snails.
Oecologia 54:337-347.
Ramsay, J. A. 1935. Methods of measuring the evaporation of water from animals. J. Exp. Biol. 12:
355-372.
Rawlings, T. A. 1990. Associations between egg capsule morphology and predation among populations of the marine gastropod, Nucella emarginata. Biol. Bull. 179:312-325.
Rawlings, T. A. 1994. Encapsulation of eggs by marine
gastropods: Effect of variation in capsule form on
the vulnerability of embryos to predation. Evolution 48:1301-1313.
Rawlings, T. A. 1995a. Encapsulation of eggs by the
rocky shore marine gastropod Nucella emarginata: costs and benefits of variation in capsule form.
Ph.D. Diss. University of Alberta, Edmonton.
Rawlings, T. A. 1995£>. Direct observation of encapsulated development in muricid gastropods. Veliger 38:54-60.
Rawlings, T. A. 1996. Shields against ultraviolet radiation: An additional protective role for the egg
capsules of benthic marine gastropods. Mar. Ecol.
Prog. Ser. 136:81-95.
Reid, D. G. 1990. A cladistic phylogeny of the genus
Littorina (Gastropoda): Implications for evolution
of reproductive strategies and for classification.
Hydrobiologia 193:1-19.
Reid, D. G. 1991. The evolution of spawn and larval
development in the Littorinidae (Gastropoda, Prosobranchia). Proc. Tenth Intern. Malacol. (Tubingen. 1989) 1991:515-516.
Rivest, B. R. 1983. Development and the influence of
nurse egg allotment on hatching size in Searlesia
NEOGASTROPOD EGG CAPSULES
dira (Reeve, 1846) (Prosobranchia: Buccinidae).
J. Exp. Mar. Biol. Ecol. 69:217-241.
Robertson, R. 1974. Marine prosobranch gastropods:
Larval studies and systematics. Thalassia Jugosl.
10:213-238.
Roller, R. A. and W. B. Stickle. 1989. Temperature and
salinity effects on the intracapsular development,
metabolic rates, and survival to hatching of Thais
haemastoma canaliculata (Gray)(Prosobranchia:
Muricidae) under laboratory conditions. J. Exp.
Mar. Biol. Ecol. 125:235-251.
Shibata, K. 1969. Pigments and a UV-absorbing substance in corals and a blue-green alga living in the
Great Barrier Reef. Plant Cell Physiol. 10:325335.
Shick J. M., W. C. Dunlap, B. E. Chalker, A. T. Banaszak, and T. K. Rosenzweig. 1992. Survey of ultraviolet radiation-absorbing mycosporine-like
amino acids in organs of coral reef holothuroids.
Mar. Ecol. Prog. Ser. 90:139-148.
Slayter, R. O. 1967. Plant-Water Relationships. Academic Press, London, 366 pp.
Spight, T. M. 1974. Size of populations of a marine
snail. Ecology 55:712-729.
Spight, T. M. 1977. Do intertidal snails spawn in the
right places? Evolution 31:682-691.
Spotila, J. R., C. J. Weinheimer, and C. V. Paganelli.
1981. Shell resistance and evaporative water loss
from bird eggs: Effects of wind speed and egg
size. Physiol. Zool. 54:195-202.
Strathmann, R. R. and C. Chaffee. 1984. Constraints
on egg masses. II: Effect of spacing, size, and
number of eggs on ventilation of masses of embryos in jelly, adherent groups, or thin-walled capsules. J. Exp. Mar. Biol. Ecol. 84:85-93.
Strathmann, R. R. and M. F. Strathmann. 1989. Evolutionary opportunities and constraints demonstrated by artificial gelatinous egg masses. In J. S.
Ryland and P. A. Tylor (eds.), Reproduction, genetics, and distributions of marine organisms,
243
23rd European Marine Biology Symposium, pp.
201-209. Olsen and Olsen, Fredensborg, Denmark.
Strathmann, R. R. and M. E Strathmann. 1995. Oxygen supply and limits on aggregation of embryos.
J. Mar. Biol. Ass. U.K. 75:413-428.
Sullivan, C. H., and T. K. Maugel. 1984. Formation,
organization, and composition of the egg capsule
of the marine gastropod, Ilyanassa obsoleta. Biol.
Bull. 167:378-389.
Tamarin, A. and M. R. Carriker. 1967. The egg capsule
of the muricid gastropod Urosalpinx cinerea: An
integrated study of the wall by ordinary light, polarized light, and electron microscopy. J. Ultrastrue. Res. 21:26-40.
Thorson, G. 1935. Studies on the egg capsules and
development of Arctic marine prosobranchs.
Medd. Gr0nland 100:1-71.
Tracy, C. R. and P. R. Sotherland. 1979. Boundary
layers of bird eggs: Do they ever constitute a significant barrier to water loss? Physiol. Zool. 52:
63-66.
Vance, R. 1973. On reproductive strategies in marine
benthic invertebrates. Am. Nat. 107:339-352.
Vermeij, G. J. 1973. Morphological patterns in highintertidal gastropods: adaptive strategies and their
limitations. Mar. Biol. 20:319-346.
Vermeij, G. J. 1978. Biogeography and adaptation:
Patterns of marine life. Harvard Univ. Press,
Cambridge, Mass.
West, D. L. 1973. Notes on the development of Colus
stimpsoni (Prosobranchia: Buccinidae). Nautilus
87:1-4.
Wolcott, T. G. 1973. Physiological ecology and intertidal zonation in limpets (Acmaea): A critical look
at "limiting factors". Biol. Bull. 145:389-422.
Woods, H. A. and R. L. DeSilets, Jr. 1997. Egg-mass
gel of Melanochlamys diomedea (Bergh) protects
embryos from low salinity. Biol. Bull. 193:341349.
Corresponding Editor: Paul Verrell