The egg capsules of neogastropod molluscs

Adaptations to physical stresses in the intertidal zone: The egg capsules of neogastropod molluscs

Rawlings, Timothy A

Adaptations to Physical Stresses in the Intertidal Zone: The Egg Capsules of Neogastropod Molluscs’

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 given that numerous 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 distribution of organisms within this habitat. How then do embryos survive within this environment?

The retention of eggs within tough, multilaminated capsules or elaborate gelatinous masses may be one means of protecting embryos from such physical stresses during their development within benthic intertidal habitats. Such egg coverings are common among marine representatives of many invertebrate phyla, including the Platyhelminthes, Nemertinea, Annelida, and Mollusca. Despite the widespread occurrence of these egg coverings, however, little is known about the precise morphological and physiological consequences of depositing embryos within these benthic egg capsules and 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 al., 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 al., 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 extra– embryonic products (Perron, 1981; Perron and Corpuz, 1982). Such variation may thus reflect differences in the suite of selective pressures acting upon encapsulated embryos 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 capsule 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 al., 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 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; 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 degC, 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 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, 1968b; Pechenik, 1978). Sixteen percent of Nassarius obsoletus capsules exposed to 75% relative humidity (22-23 degC) 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 degC (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 well– adapted 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 (1968b) 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.,

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 slm to 32 s/ m over an increase in wind speed from 01.5 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 (

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 microstructure, 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 habitat– related 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 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 CS% UV-B (300 nm) and

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 (Rawlings, 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 fluoresces 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 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 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 15%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., 1991b; 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 emersion, 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 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, 1995b). Perron (1981) has also suggested that the production of tougher, energetically more– expensive 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 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.

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Corresponding Editor: Paul Verrell

TIMOTHY A. RAWLINGS2

Department of Biological Sciences, Florida International University, University Park, Miami, Florida 33199

1From the Symposium Aquatic Organisms, Terrestrial Eggs: Early Development at the Water’s Edge presented at the annual meeting of the Society for Integrative and Comparative Biology, 3-7 January 1998, at Boston, Massachusetts.

2 E-mail: rawlings@fiu.edu

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