Abstract
During the summer of 1989, we examined mechanisms of egg hatching in three species of brachyurans that occupy different habitats as adults near Beaufort, North Carolina, USA:Neopanope sayi (Smith) (subtidal),Uca pugilator (Bosc) (intertidal) andSesarma cinereum (Bosc) (supratidal). Results of casein assays indicated that embryos of all species release proteolytic enzymes near the time of egg hatching. Species differences in specific enzyme activity were suggested, with increased activity in the more terrestrial crabs. Embryos ofN. sayi released enzymes several hours before larval release by the female, whileU. pugilator andS. cinereum released enzymes closer to the time of larval release; enzyme release coincided roughly with time of egg-membrane breakage in all species. Direct observations of hatching showed a sequence of outer-membrane breakage apparently followed by inner-membrane breakage and emergence of the larva. Egg volumes increased most during early and/or mid-stages of development, with a marked slowing of the increase during the several days before hatching. Thus, a gradual osmotically-driven increase in water content may also be involved in egg hatching.
Similar content being viewed by others
Literature cited
Barnes, H., Barnes, M. (1977). Studies on the reproduction of cirripedes. II. Setting of the lamellae; action of protease and disintegration of the oviducal sac. J. exp. mar. Biol. Ecol. 27: 219–231
Barnes, H., Blackstock, J. (1977). Studies on the reproduction of cirripedes. III. Oviscase; properties of the enzyme released by the late stage embryos. J. exp. mar. Biol. Ecol. 27: 233–249
Bergin, M. E. (1981). Hatching rhythms inUca pugilator (Decapoda: Brachyura). Mar. Biol. 63: 151–158
Berrill, N. J. (1975). Chordata: Tunicata. In: Giese, A. C., Pearse, J. S. (eds.) Reproduction of marine invertebrates. Vol. 2. Academic Press, New York and London, p. 241–282
Carroll, E. J., Hedrick, J. L. (1974). Hatching in the toadXenopus laevis: morphological events and evidence for a hatching enzyme. Devl Biol. 38: 1–13
Christy, J. H. (1978). Adaptive significance of reproductive cycles in the fiddler crabUca pugilator. Science, N.Y. 197: 453–455
Christy, J. H. (1982). Adaptive significance of semilunar cycles of larval release in fiddler crabs (genusUca): test of an hypothesis. Biol. Bull. mar. biol. Lab., Woods Hole 163: 251–263
Christy, J. H. (1986). Timing of larval release by intertidal crabs on an exposed shore. Bull. mar. Sci. 39: 176–191
Crisp, D. J. (1956). A substance promoting hatching and liberation of young in cirripedes. Nature, London. 178: p. 263
Crisp, D. J., Spencer, C. P. (1958). The control of the hatching process in barnacles. Proc. Roy. Soc. (Ser. B) 148: 278–299
Cronin, T. W., Forward, R. B., Jr. (1988). The visual pigments of crabs. I. Spectral characteristics. J. comp. Physiol. 162: 463–478
D'Asaro, C. N. (1969). The comparative embryogenesis and early organogenesis ofBursa corrugata Perry andDistorsio clathrata Lamarck (Gastropoda: Prosobranchia). Malacologia 9: 349–389
Davis, C. C. (1959). Osmotic hatching in the eggs of some freshwater copepods. Biol. Bull. mar. biol. Lab., Woods Hole 116: 15–29
Davis, C. C. (1964). A study of the hatching process in aquatic invertebrates. IX. Hatching within the brood sac of the ovoviviparous isopodCirolana sp. (Isopoda, Cirolanidae). X. Hatching in the freshwater shrimpPotimirim glabra Kingsley (Macrura, Atyidae). Pacif. Sci. 18: 378–384
Davis, C. C. (1965). A study of the hatching process in aquatic invertebrates. XX. The blue crabCallinectes sapidus, Rathbun; XXI. The nemertean,Carcinonemertes carcinophila (Kölliker). Chesapeake Sci. 6: 201–208
Davis, C. C. (1966). A study of the hatching process in aquatic invertebrates. XVI. Events of eclosion inCalopsectra neoflavellus Malloch (Diptera, Tenipedidae). XVII. Hatching inArgulus megalops Smith (Crustacea, Branchiura). Hydrobiologia 27: 196–207
Davis, C. C. (1968). Mechanisms of hatching in aquatic invertebrate eggs. Oceanogr. mar. Biol. A. Rev. 6: 325–376
Davis, C. C. (1981). Mechanisms of hatching in aquatic invertebrate eggs. II. Oceanogr. mar. Biol. A. Rev. 19: 95–123
DeCoursey, P. J. (1979). Egg hatching rhythms in three species of fiddler crabs. In: Naylor, E., Hartnoll, R. G. (eds.) Cyclic phenomena in marine plants and animals, Pergammon Press, Oxford, p. 399–406
DeCoursey, P. J. (1983). Biological timing. In: Vernberg, F. J., Vernberg, W. B. (eds.) The biology of Curstacea. Vol. 7. Behavior and ecology. Academic Press, New York, p. 107–162
De Vries, M. C., Forward, R. B., Jr. (1989). Rhythms in larval release of the sublittoral crabNeopanope sayi and the supralittoral crabSesarma cinereum (Decapoda: Brachyura). Mar. Biol. 100: 241–248
De Vries, M. C., Forward, R. B., Jr. (1991). Control of egg-hatching time in crabs from different tidal heights. J. Crustacean Biol. 11: 29–39
Dollard, H. A. (1980). Larval release patterns in the wharf crab,Sesarma cinereum from North Inlet, South Carolina. Masters thesis. University of South Carolina
Forward, R. B., Jr. (1987). Larval release rhythms of decapod crustaceans: an overview. Bull. mar. Sci. 41: 165–176
Forward, R. B., Jr., Cronin, T. W. (1979). Spectral sensitivity of larvae from intertidal crustaceans. J. comp. Physiol. 133: 311–315
Forward, R. B., Jr., Lohmann, K. J. (1983). Control of egg hatching in the crabRhithropanopeus harrisii (Gould). Biol. Bull. mar. biol. Lab., Woods Hole 165: 154–166
Forward, R. B., Jr., Lohmann, K., Cronin, T. W. (1982). Rhythms in larval release by an estuarine crab (Rhithropanopeus harrisii). Biol. Bull. mar. biol. Lab., Woods Hole 163: 287–300
Giese, A. C., Pearse, J. S. (1974). Reproduction of marine invertebrates. Vol. 1. Acoelomate and pseudocoelomate metazoans. Academic Press, New York
Grant, G. A., Eisen, A. Z., Bradshaw, R. A. (1981). Collagenolytic protease from fiddler crab (Uca pugilator). Meth. Enzym. 80: 722–734
Gray, E. H. (1942). Ecological and life history aspects of the redjointed fiddler crab,Uca minax (Le Conte), region of Solomons Island, Maryland. Contr. Chesapeake biol. Lab. 51: 1–20
Guidice, G. (1973). Developmental biology of the sea urchin embryo. Academic Press, New York
Ishida, J. (1936). An enzyme dissolving the fertilization membrane of sea-urchin eggs. Annotnes zool. jap. 15: 453–459
Ishida, J. (1944a). Hatching enzyme in the fresh-water fish,Oryzias latipes. Annotnes zool. jap. 22: 137–154
Ishida, J. (1944b). Further studies on the hatching enzyme of the fresh-water fish,Oryzias latipes. Annotnes zool. jap. 22: 155–164
Iwata, F. (1970). Studies on the development of the crabPugettia quadridens (De Haan): 1. Hatching and zoeae. Publs Seto mar. biol. Lab. 3: 189–197
Kaighn, M. E. (1964). A biochemical study of the hatching process inFundulus heteroclitus. Devl Biol. 9: 56–80
Katagiri, C. (1975). Properties of the hatching enzyme from frog embryos. J. exp. Zool. 193: 109–118
Katre, S., Pandian, T. (1972). On the hatching mechanism of the freshwater prawnMacrobrachium idae. Hydrobiologia 40: 1–18
Kearn, G. C. (1975). The model of hatching of the monogeneanEntobdella soleae, a skin parasite of the common sole (Solea solea). Parasitology 71: 419–431
Knowlton, R. E. (1973). Larval development of the snapping shrimpAlpheus heterochaelis Say, reared in the laboratory. J. nat. Hist. 7: 273–306
Kopac, M. J. (1941). Disintegration of the fertilization membrane ofArbacia by the action of an enzyme. J. cell. comp. Physiol. 18: 215–220
Mahieu, G. C., de, Penchaszadek, P. E., Casal, A. B. (1974). Algunos aspectos de las varaciones de proteinas y aminoacidos libres totales del liquido intracapsular en relacion al desarrollo embrionario enAdelomelon brasiliana (Lamarck, 1811) (Gastropoda, Prosobranchia, Volutidae). (1). Cah. Biol. mar. 15: 215–227
Marshall, S. M., Orr, A. P. (1954). Hatching inCalanus finmarchicus and some other copepods. J. mar. biol. Ass. U.K. 33: 393–401
Okazaki, K. (1975). Normal development to metamorphosis. In: Czihak, G. (ed.) The sea urchin embryo: biochemistry and metamorphosis. Springer-Verlag, Berlin, p. 172–232
Pandian, T. J. (1970). Ecophysiological studies on the developing eggs and embryos of the European lobsterHomarus gammarus. Mar. Biol. 5: 154–167
Pearson, J. C. (1939). The early life histories of some American Penaeidae, chiefly the commercial shrimp,Penaeus setiferus (Linn.). Bull. Bur. Fish., Wash. 49: 1–73
Pechenik, J. A. (1975). The escape of veligers from the egg capsules ofNassarius obsoletus andNassarius trivittatus (Gastropoda, Prosobranchia). Biol. Bull. mar. biol. Lab., Woods Hole 149: 580–589
Rick, W. (1963). Trypsin. In: Bergmeyer, H. (ed.) Methods of enzymatic analysis. Academic Press, New York, p. 807–818
Rittschof, D., Forward, R. B., Jr. Erickson, B. W. (1990). Larval release in brachyuran crustaceans: functional similarity of the peptide receptor and the catalytic site of trypsin. J. chem. Ecol. 16: 1359–1370
Rittschof, D., Forward, R. B., Jr., Mott, D. (1985). Larval release in the crabRhithropanopeus harrisii (Gould): chemical cues from hatching eggs. Chem. Senses 10: 567–577
Saigusa, M., Hidaka, T. (1978). Semilunar rhythms in zoeae-release activity of the land crabSesarma. Oecologia 37: 163–176
Salmon, M., Hyatt, G. W. (1983). Spatial and temporal aspects of reproduction in North Carolina fiddler crabs (Uca pugilator Bosc). J. exp. mar. Biol. Ecol. 70: 21–43
Salmon, M., Seiple, W. H., Morgan, S. G. (1986). Hatching rhythms of fiddler crabs and associated species at Beaufort, North Carolina. J. Crustacean Biol. 6: 24–36
Seiple, W. H. (1979). Distribution, habitat preferences, and breeding periods in the crustaceansSesarma cinereum andS. reticulatum (Brachyura: Decapoda: Grapsidae). Mar. Biol. 52: 77–86
Smith, W. K., Miller, P. C. (1973). The thermal ecology of two south Florida fiddler crabs;Uca rapax Smith andU. pugilator Bosc. Physiol. Zoöl. 46: 186–207
Sokal, R. R., Rohlf, R. J. (1981). Biometry. The principles and practice of statistics in biological research. 2nd ed. W. H. Freeman & Co., San Francisco
Stearns, L. W. (1974). Sea urchin development: cellular and molecular aspects. Dowden, Hutchinson & Ross, Stroudsburg, Pennsylvania
Sukô, T. (1969). Studies on the development of the crayfish. VIII. The hatching and the hatched young. Sci. Rep. Saitama Univ. (Ser. B) 4: 37–42
Teal, J. M. (1958). Distribution of fiddler crabs in Georgia salt marshes. Ecology 39: 185–193
Wallace, H. (1961). The breeding and development ofStyela mammiculata Carlisle. J. mar. biol. Ass. U.K. 41: 187–190
Wear, R. G. (1967). Life history studies on New Zealand Brachyura. N.Z. Jl. mar. Freshwat. Res. 1: 482–535
Wells, M. J., Wells, J. (1977). Cephalopoda: Octopoda. In: Giese, A. C., Pearse, J. S. (eds.) Reproduction of marine invertebrates. Vol. IV. Molluscs: gastropods and cephalopods, Academic Press, New York, p. 291–336
Williams, A. B. (1984). Shrimps, lobsters, and crabs of the Atlantic coast of the Eastern United States, Maine to Florida. Smithsonian Institution Press, Washington D.C.
Winnicki, A., Slomianko, M. (1970). Taking up of water by the eggs of the crabRhithropanopeus harrisii (Gould) subsp.tridentatus (Maitland) during embryonic development. Zoologica Pol. 20: 415–422
Yamagami, K. (1970). A method for rapid and quantitative determination of the hatching enzyme (chorionase) activity of the medakaOryzias latipes. Annotnes zool. jap. 43: 1–9
Yasumasu, I. (1958). Hatching enzyme of the sea urchins,Hemicentrotus pulcherrimus andHeliocidaris crassispina. Bull. mar. biol. Stn Asamushi 9: 83–84
Zwilling, R., Neurath, H. (1981). Invertebrate proteases. Meth. Enzym. 80: 633–664
Author information
Authors and Affiliations
Additional information
Communicated by J.M. Lawrence, Tampa
Rights and permissions
About this article
Cite this article
De Vries, M.C., Forward, R.B. Mechanisms of crustacean egg hatching: Evidence for enzyme release by crab embryos. Mar. Biol. 110, 281–291 (1991). https://doi.org/10.1007/BF01313715
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF01313715