Egg-Mass Gel of Melanochlamys diomedea (Bergh) Protects Embryos From Low Salinity

Abstract

Many opisthobranch gastropods embed their embryos in gelatinous egg masses; however, the functions of gel are not well known. We analyze the hypothesis that egg-mass gel protects embryos from salinity change. Using egg masses of Melanochlamys diomedea, we found that experimental removal of gel decreased the ability of embryos to survive osmotic stress. We evaluate several possible protective mechanisms by estimating osmotic influx of water into egg masses and by modeling salt efflux from an egg mass. On immersion in low-salinity water, egg masses lost roughly 23% of their mass, indicating that osmotic influx of water did not occur. Therefore, the principal route of salinity change within the egg mass is probably salt efflux. The model suggests that this efflux occurs quite slowly even when ambient salinity changes rapidly. Slow salinity change may be less stressful for embryos because the mechanisms that regulate cellular volume have more time to adjust. We show experimentally that slow salinity changes are less harmful to veligers than rapid ones by isolating capsules from egg-mass gel and exposing them to gradual or abrupt salinity change. The results support the hypothesis that rate of change of salinity is an important determinant of embryo survival and that egg-mass gel retards the rate of salinity change.

On the advantages and disadvantages of larval stages in benthic marine invertebrate life cycles

“…Developmental stages are also susceptible to fluctuations in salinity and temperature (Pechenik 1987, Richmond & Woodin 1996, but again, it is not clear that free-living larvae are more susceptible than encapsulated or brooded embryos to such stresses. For the few gastropod and polychaete species that have been studied to date, egg capsules and egg masses were found to be permeable to water and salts (Galtsoff et al 1937, Carriker 1955, Pechenik 1982, Eyster 1986, Medernach 1995, Bhaud & Duchene 1996, Woods & DeSilets 1997. For example, rapid declines in ambient salinity are accon~panied by rapid declines in the osmotic concentration of intracapsular fluid for the prosobranch gastropod Nucella lapillus (Pechenik 1983); encapsulation therefore does not spare embryos exposure to salinity fluctuation in that species.…”

“…On the other hand, encapsulated embryos of several gastropod species survived exposure to salinity stress far better than embryos exposed to the same magnitude of salinity stress after being removed from their capsules or egg masses (Pechenik 1982, Woods & DeSilets 1997. Thus, encapsulation can protect developmental stages from salinity stress even when the capsules and egg masses are permeable to salts and/or water; protection is probably achieved by slowing the rate of salinity change (Pechenik 1983, Woods & DeSilets 1997.…”

“…Thus, encapsulation can protect developmental stages from salinity stress even when the capsules and egg masses are permeable to salts and/or water; protection is probably achieved by slowing the rate of salinity change (Pechenik 1983, Woods & DeSilets 1997.…”

“…However, the results of laboratory experiments comparing embryonic and larval tolerances of salinity and other stress factors may mislead us about the relative susceptibilities of embryos and larvae in the field: encapsulation potentially imprisons embryos in stressful situations that free-living larvae can avoid by passive dispersal or active vertical migration (Carriker 1951, Richter 1973, Pechenik 1979, Heslinga 1976, Pennington & Emlet 1986, Sulkin et al 1983, Forward 1985. Encapsulating structures may in fact increase exposure to osmotic stress (Carriker 1955, Gibbs 1968, Pechenik 1982, Richmond & Woodin 1996, Woods & DeSilets 1997, desiccation stress (Kohn 1961, Spight 1975, Pechenik 1978, and oxygen deprivation (Perron & Corpuz 1982, Chaffee & Strathmann 1984, Cohen & Strathmann 1996, Lee & Strathmann 1998. The degree to which developing embryos are protected from these and many other stresses may depend more on where parents attach capsules and egg masses than on the properties of encapsulating structures per se (Spight 1977, Pechenik 1978, Biermann et al 1992.…”

“…Middaugh & Floyd (1978 suggested that extraembryonic membranes protect embryos of the crustacean Palaemonetes pugio from heavy-metal exposure, but they made no permeability measurements. The egg capsules of several prosobranch gastropods are permeable to glucose and other small organic molecules (Galtsoff et al 1937, Carriker 1955, Pechenik 1982, and the gelatinous egg masses of the opisthobranch gastropod Melanochlamys diomedea (Woods & DeSilets 1997), the polychaete Euypolymnia nebulosa (Bhaud 8? Duchsne 1996), and several species in the gastropod genus Lacuna (Hertling 1928) are permeable to salts.…”