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Reproduction in the Apodid Sea Cucumber Polycheira Rufescens: Semilunar Spawning Rhythm and Sex Change

Published online by Cambridge University Press:  11 May 2009

Tomoyuki Kubota
Affiliation:
Department of Biology, Faculty of Science, KagoshimaUniversity, Kagoshima 890, Japan
Masakazu Tomari
Affiliation:
Department of Biology, Faculty of Science, KagoshimaUniversity, Kagoshima 890, Japan

Extract

Most fertile individuals of the apodid sea cucumber Polycheira rufescens, living in the intertidal zone near Iso Marine Station in southern Kyushu, Japan, spawned on day one and two before every full and new moon in the period from the second half of July until August or October from 1983 to 1989, the month differing in different years. Synchronous spawning associated with the same phases of the moon was also observed at Sakurajima Marine Station near Iso in 1991. Individuals ready to spawn were divided into four sexual types: two sorts of hermaphroditic males with small or larger growing oocytes and males and females. Further investigation revealed that some individuals changed from male to female or from female back to male in the two week interval between spawnings. Moreover synchronous gametogenesis occurred in association with sex changes throughout the breeding season, the period from initiation of spermatogonia proliferation to spermatozoa release was three weeks, and the period from initiation of oocyte growth to egg shedding was about five weeks.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 1998

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References

Babcock, R.C., Bull, G.D., Harrison, P.L., Heyward, A.J., Oliver, J.K., Wallace, C.C. & Willis, B.L., 1986. Synchronous spawnings of 105 scleractinian coral species on the Great Barrier Reef. Marine Biology, 90, 379394.CrossRefGoogle Scholar
Babcock, R., Mundy, C, Keesing, J. & Oliver, J., 1992. Predictable and unpredictable spawning events: in situ behavioural data from free-spawning coral reef invertebrates. Invertebrate Reproduction and Development, 22, 213228.CrossRefGoogle Scholar
Berglund, A., 1986. Sex change by a polychaete: effects of social and reproductive costs. Ecology, 67, 837845.CrossRefGoogle Scholar
Berrill, M., 1966. The ethology of the synaptid holothurian, Opheodesoma spectabilis. Canadian Journal of Zoology, 44, 457482.CrossRefGoogle Scholar
Billett, D.S.M., 1991. Deep-sea holothurians. Oceanography and Marine Biology. Annual Review, 29, 259317.Google Scholar
Caspers, H., 1984. Spawning periodicity and habitat of the palolo worm Eunice viridis (Polychaeta: Eunicidae) in the Samoan Islands. Marine Biology, 79, 229236.CrossRefGoogle Scholar
Chao, S.M., Chen, C.-P. & Alexander, P.S., 1995. Reproductive cycles of tropical sea cucumbers (Echinodermata: Holothuroidea) in southern Taiwan. Marine Biology, 122, 289295.CrossRefGoogle Scholar
Charnov, E.L., 1982. The theory of sex allocation. Princeton: Princeton University Press. [Monographs in Population Biology no. 18.]Google ScholarPubMed
Charnov, E.L., 1986. Size advantage may not always favor sex change. Journal of Theoretical Biology, 119, 283285.CrossRefGoogle Scholar
Cochran, R.C. & Engelmann, F., 1975. Environmental regulation of the annual reproductive season of Strongylocentrotus purpuratus (Stimpson). Biological Bulletin. Marine Biological Laboratory, Woods Hole, 148, 393401.CrossRefGoogle ScholarPubMed
Coe, W.R., 1943. Sexual differentiation in mollusks. I. Pelecypods. Quarterly Review of Biology, 18, 154164.CrossRefGoogle Scholar
Coe, W.R., 1945. Development of the reproductive system and variations in sexuality in Pecten and other pelecypod mollusks. Transactions of the Connecticut Academy of Arts and Sciences, 36, 673700.Google Scholar
Conand, C, 1993. Reproductive biology of the holothurians from the major communities of the New Caledonian Lagoon. Marine Biology, 116, 439450.Google Scholar
Fox, H.M., 1923. Lunar periodicity in reproduction. Proceedings of the Royal Society B. 95, 523550.Google Scholar
Ghiselin, M.T., 1969. The evolution of hermaphroditism among animals. Quarterly Revieiv of Biology, 44, 189208.CrossRefGoogle ScholarPubMed
Giese, A.C. & Kanatani, H., 1987. Maturation and spawning. In Reproduction of marine invertebrates. IX. General aspects: seeking unity in diversity (ed. A.C., Giese et al.), pp. 251329. Palo Alto, California: Blackwell Scientific Publications and Pacific Grove, California: The Boxwood Press.Google Scholar
Gotto, D.M. & Gotto, R.V., 1972. Labidoplax media Oestergren: a sea-cucumber new to British and Irish waters, with observational notes. Irish Naturalists Journal, 17, 250252.Google Scholar
Green, J.D., 1978. The annual reproductive cycle of an apodous holothurian Leptosynapta tenuis: a bimodal breeding season. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 154, 6878.CrossRefGoogle ScholarPubMed
Hamel, J.-F., Himmelman, J.H. & Dufresne, L., 1993. Gametogenesis and spawning of the sea cucumber Psolus fabricii (Duben and Koren). Biological Bulletin. Marine Biological Laboratory, Woods Hole, 184, 125143.Google ScholarPubMed
Hamel, J.-F. & Mercier, A., 1995. Spawning of the sea cucumber Cucumaria frondosa in the St Lawrence Estuary, eastern Canada. SPC Bêche-de-mer Information Bulletin, 7, 1218.Google Scholar
Harriott, V., 1982. Sexual and asexual reproduction of Holothuria atra Jaeger at Heron Island Reef, Great Barrier Reef. Memoirs of the Australian Museum, 16, 5366.CrossRefGoogle Scholar
Hatanaka, M., 1939. A study of the caudate holothurian, Molpadia roretzii (V. Marenzeller). Science Reports of Tohoku Imperial University. Series 4, Biology, 14, 155189.Google Scholar
Hendler, G. & Meyer, D.L., 1982. Ophiuroids Flagrante delicto and notes on the spawning behavior of other echinoderms in their natural habitat. Bulletin of Marine Science, 32, 600607.Google Scholar
Holland, N.D., 1980. A model linking environmental signals to the spawning time of Comanthus japonica (Echinodermata: Crinoidea). In Advances in invertebrate reproduction (ed. W.H., Clark Jr and T.S., Adams), pp. 7578. New York: Elsevier North Holland.Google Scholar
Hoppe, W.F. & Reichert, M.J.M., 1987. Predictable annual mass release of gametes by the coral reef sponge Neofibularia nolitangere (Porifera: Demospongiae). Marine Biology, 94, 277285.CrossRefGoogle Scholar
Hori, R., Phang, V.P.E. & Lam, T.J., 1987. Preliminary study on the pattern of gonadal development of the sea urchin Diadema setosum off the coast of Singapore. Zoological Science, 4, 665673.Google Scholar
Iliffe, T.M. & Pearse, J.S., 1982. Annual and lunar reproductive rhythms of the sea urchin Diadema antillarum (Philippi) in Bermuda. International journal of Invertebrate Reproduction, 5, 139148.CrossRefGoogle Scholar
Inaba, D., 1930. Notes on the development of a holothurian, Caudina chilensis (J. M¨ller). Science Reports of the Tohoku Imperial University. Series 4, Biology, 5, 215248.Google Scholar
Iwasa, Y., 1991. Sex change evolution and cost of reproduction. Behavioral Ecology, 2, 5668.CrossRefGoogle Scholar
Kennedy, B. & Pearse, J.S., 1975. Lunar synchronization of the monthly reproductive rhythm in the sea urchin Centrostephanus coronatus Verrill. Journal of Experimental Marine Biology and Ecology, 17, 323331.CrossRefGoogle Scholar
Kobayashi, N., 1967. Spawning periodicity of sea urchins at Seto. I. Mespila globulus. Publications of the Seto Marine Biological Laboratory, 14, 403414.CrossRefGoogle Scholar
Kobayashi, N. & Nakamura, K., 1967. Spawning periodicity of sea urchins at Seto. II. Diadema setosum. Publications of the Seto Marine Biological Laboratory, 15, 173184.Google Scholar
Kobayashi, M. & Ujima, H., 1982. Studies on marine culture of the sea cucumber Stichopus japonicus (II). Annual Report of the Buzen Fishery Experimental Station of Fukuoka Prefecture, Japan, 1982, 5565.Google Scholar
Kojis, B.L. & Quinn, N.J., 1981. Aspects of sexual reproduction and larval development in the shallow water hermatypic coral, Goniastrea australensis (Edwards & Haime, 1857). Bulletin of Marine Science, 31, 558573.Google Scholar
Kubota, H., 1980. Synchronization of spawning in the crinoid, Comanthus japonica. In Advances in invertebrate reproduction (ed. W.H., Clark Jr, and T.S., Adams), pp. 6974. New York: Elsevier North Holland.Google Scholar
Leigh, E.G., Charnov, E.L. & Warner, R.R., 1976. Sex ratio, sex change and natural selection. Proceedings of the National Academy of Sciences of the United States of America, 73, 36563660.CrossRefGoogle ScholarPubMed
Lessios, H.A., 1984. Possible prezygotic reproductive isolation in sea urchins separated by the Isthmus of Panama. Evolution, 38, 11441148.CrossRefGoogle ScholarPubMed
Lessios, H.A., 1991. Presence and absence of monthly reproductive rhythms among eight Caribbean echinoids off the coast of Panama. Journal of Experimental Marine Biology and Ecology, 153, 27–17.CrossRefGoogle Scholar
Levitan, D.R., 1991. Influence of body size and population density on fertilization success and reproductive output in a free-spawning invertebrate. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 181, 261268.Google Scholar
Maruyama, Y.K., 1980. Artificial induction of oocyte maturation and development in the sea cucumbers Holothuria leucospilota and Holothuria pardalis. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 158, 339348.CrossRefGoogle Scholar
McEuen, F.S., 1988. Spawning behaviors of northeast Pacific sea cucumbers (Holothuroidea: Echinodermata). Marine Biology, 98, 565585.CrossRefGoogle Scholar
Minchin, D., 1992. Multiple species, mass spawning events in an Irish sea lough: the effect of temperatures on spawning and recruitment of invertebrates. Invertebrate Reproduction and Development, 22, 229238.CrossRefGoogle Scholar
Noumura, T. & Kanatani, H., 1962. Induction of spawning by radial nerve extracts in some starfishes. Journal of the Faculty of Science. Section 4. Zoology. Tokyo University, 9, 397402.Google Scholar
Nyholm, K.-G., 1951. The development and larval form of Labidoplax buskii. Zoologiska Bidrag fran Uppsala, 29, 239255.Google Scholar
Ohshima, H., 1921. On the development of Cucumaria echinata v. Marenzeller. Quarterly Journal of Microscopical Science, 65, 173246.Google Scholar
Pearse, J.S., 1969. Reproductive periodicities of Indo-Pacific invertebrates in the Gulf of Suez. III. The echinoid Diadema setosum (Leske). Bulletin of Marine Science, 19, 580613.Google Scholar
Pearse, J.S., 1975. Lunar reproductive rhythms in sea urchins. A review. Journal of Interdisciplinary Cycle Research, 6, 4752.CrossRefGoogle Scholar
Pearse, J.S., 1990. Lunar Reproductive Rhythms In Marine Invertebrates: Maximizing Fertilization? In Advances in invertebrate reproduction. Vol. 5. (ed. M., Hoshi and O., Yamashita), pp. 311316. Amsterdam and New York: Elsevier Science Publishers [Biomedical Division.]Google Scholar
Pearse, J.S., McClary, D.J., Sewell, M.A., Austin, W.C., Perez-Ruzafa, A. & Byrne, M., 1988. Simultaneous spawning of six species of echinoderms in Barkley Sound, British Columbia. Invertebrate Reproduction and Development, 14, 279288.CrossRefGoogle Scholar
Pennington, J.T., 1985. The ecology of fertilization of echinoid eggs: the consequences of sperm dilution, adult aggregation, and synchronous spawning. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 169, 417430.CrossRefGoogle ScholarPubMed
Policansky, D., 1982. Sex change in plants and animals. Annual Review of Ecology and Systematics, 13, 471495.Google Scholar
Reichenbach, N., 1995. Spawning observations of tropical holothurians from Male and Laamu Atoll, Republic of Maldives. SPC B^che-de-mer Information Bulletin, 7, 11.Google Scholar
Runström, S., 1927. Éber die Entwicklung von Leptosynapta inhaerens (O.F. Müller). Bergens Museum Arbok. Naturvitenskapelig rekke, 1927, 180.Google Scholar
Sewell, M.A., 1994. Small size, brooding, and protandry in the apodid sea cucumber Leptosynapta clarki. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 187, 112123.CrossRefGoogle ScholarPubMed
Sewell, M.A. & Bergquist, P.R., 1990. Variability in the reproductive cycle of Stichopus mollis (Echinodermata: Holothuroidea). Invertebrate Reproduction and Development, 17, 17.CrossRefGoogle Scholar
Sewell, M.A. & Chia, F.-S., 1994. Reproduction of the intraovarian brooding apodid Leptosynapta clarki (Echinodermata: Holothuroidea) in British Columbia. Marine Biology, 121, 285300.CrossRefGoogle Scholar
Sewell, M.A. & Levitan, D.R., 1992. Fertilization success during a natural spawning of the dendrochirote sea cucumber Cucumaria miniata. Bulletin of Marine Science, 51, 161166.Google Scholar
Shelley, C.C., 1981. Aspects of the distribution, reproduction, growth and ‘fishery’ potential of holothurians (Beche-de-mer) in the Papuan coastal lagoon. MSc thesis, University of Papua New Guinea.Google Scholar
Smiley, S., McEuen, F.S., Chaffee, C. & Krishnan, S., 1991. Echinodermata: Holothuroidea. In Reproduction of marine invertebrates. VI. Echinoderms and lophophorates (ed. A.C., Giese et al.), pp. 663750. Pacific Grove, California: Boxwood Press.Google Scholar
Teuchert, G., 1968. Zur Fortplanzung und Entwicklung der Macrodasyoidea (Gastrotricha). Zeitschrift für Morphologie der Tiere, 63, 343418.CrossRefGoogle Scholar
Tyler, P.A., Young, Cm., Billett, D.S.M. & Giles, L.A., 1992. Pairing behaviour, reproduction and diet in the deep-sea holothurian genus Paroriza (Holothurioidea: Synallactidae). Journal of the Marine Biological Association of the United Kingdom, 72, 447462.CrossRefGoogle Scholar
Utsumi, F., 1979. Polycheira rufescens (Brandt). In Illustrated encyclopedia of the fauna of Japan (ed. T., Uchida), p. 518. Tokyo: Hokuryukan.Google Scholar
Vail, L., 1993. Holothurian spawning - Lizard Island - 18/1/93. SPC Bêche-de-mer Information Bulletin, 5, 2122.Google Scholar
Warner, R.R., 1975. The adaptive significance of sequential hermaphroditism in animals. American Naturalist, 109, 6182.CrossRefGoogle Scholar
Warner, R.R., Robertson, D.R. & Leigh, E.G., 1975. Sex change and sexual selection. Science, New York, 190, 633638.CrossRefGoogle ScholarPubMed
Yoshida, M., 1952. Some observations on the maturation of the sea-urchin, Diadema setosum. Annotationes Zoologicae Japonenses, 25, 265271.Google Scholar
Yoshioka, E., 1987. Annual reproductive cycle of the chiton Acanthopleura japonica. Marine Biology, 96, 371374.CrossRefGoogle Scholar
Young, Cm., Tyler, P.A., Cameron, J.L. & Rumrill, S.G., 1992. Seasonal breeding aggregations in low-density populations of the bathyal echinoid Stylocidaris lineata. Mamie Biology, 113, 603612.Google Scholar
Yund, P.O., 1990. An in situ measurement of sperm dispersal in a colonial hydroid. Journal of Experimental Zoology, 253, 102106.CrossRefGoogle Scholar