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Reproduction in Bathyplotes natans (Holothurioidea: Synallactidae) from bathyal depths in the north-east and western Atlantic

Published online by Cambridge University Press:  11 May 2009

P.A. Tyler ,
K. Eckelbarger  and
D.S.M. Billett
P.A. Tyler
Affiliation:
Department of Oceanography, The University, Southampton, SO9 5NH
K. Eckelbarger
Affiliation:
Darling Marine Center, University of Maine, Walpole, Maine 04573, USA
D.S.M. Billett
Affiliation:
Institute of Oceanographic Sciences, Deacon Laboratory, Wormley, Godalming, Surrey, GU8 5UB
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Abstract

The gross morphology, histology, ultrastructure and periodicity of gonad development of the bathyal aspidochirote holothurian Bathyplotes natans is described and compared with the ‘tubule recruitment model’ proposed for aspidochirote holothurians. As B. natans grows, additional gonad tubules develop at the anterior end of the gonad basis. Oocyte development in these tubules is non-seasonal and the population of oocytes consists of both pre-vitellogenic and vitellogenic oocytes as well as some large oocytes undergoing phagocytic breakdown. Vitellogenesis is similar to that described previously for holothurians, although the follicular inner epithelium cells surrounding the developing oocytes are different from those previously reported. In males the unique acrosomal complex consists of three depressions with the acrosome lying in the central depression. The tubule recruitment model of Smiley does not apply to B. natans. We do not feel this model has widespread applicability in the Aspidochirotida or the Holothurioidea in general.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 74 , Issue 2 , May 1994 , pp. 383 - 402
Copyright
Copyright © Marine Biological Association of the United Kingdom 1994

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References

Aisenshtadt, T.B. & Vassetzky, S.G., 1986. Fine structures of oocytes and accessory cells in the ovary of the starfish Patiria (Asterina) pectinifera at different stages of oogenesis and after 1-methyladenine-induced maturation. Development, Growth and Differentiation, 28, 449–460.CrossRefGoogle ScholarPubMed
Atwood, D.G., 1973. Ultrastructure of the gonadal wall of the sea cucumber, Leptosynapta clarki (Echinodermata: Holothuroidea). Zeitschrift für Zellforschung und Mikroskopische Anatomie, 141, 319–330.CrossRefGoogle ScholarPubMed
Atwood, D.G., 1974. Fine structure of spermatogonia, spermatocytes, and spermatids of the sea cucumbers Cucumaria lubrica and Leptosynapta clarki (Echinodermata: Holothuroidea). Canadian Journal of Zoology, 52, 1389–1396.CrossRefGoogle ScholarPubMed
Beams, H.W. & Kessel, R.G., 1983. Cnidaria. In Reproductive biology of invertebrates. Vol. I. Oogenesis, oviposition, and oosorption (ed. K.G., Adiyodi and R.G., Adiyodi), pp. 31–66. Chichester: John Wiley.Google Scholar
Bickell, L.R., Chia, F.-S. & Crawford, B.J., 1980. A fine structural study of the testicular wall and spermatogenesis in the crinoid, Florometra serratissima (Echinodermata). Journal of Morphology, 166, 109–126.CrossRefGoogle Scholar
Billett, D.S.M., 1988. The ecology of deep-sea holothurians. PhD thesis, University of Southampton.Google Scholar
Billett, D.S.M., 1991. Deep-sea holothurians. Oceanography and Marine Biology. Annual Review. London, 29, 259–317.Google Scholar
Buckland-Nicks, J., Walker, C.W. & Chia, F.-S., 1984. Ultrastructure of the male reproductive system and of spermatogenesis in the viviparous brittle-star Amphipholis squamata. Journal of Morphology, 179, 243–262.CrossRefGoogle ScholarPubMed
Byrne, M., 1988. Evidence for endocy tone incorporation of nutrients from the haemal sinus by the oocytes of the brittlestar Ophiolepis paucispina. In Echinoderm biology (ed. R.D., Burkeet al.), pp. 557–563. Rotterdam: A.A. Balkema.Google Scholar
Cameron, J.L. & Fankboner, P.V., 1986. Reproductive biology of the commercial sea cucumber Parastichopus californicus (Stimpson) (Echinodermata: Holothuroidea). I. Reproductive periodicity and spawning behavior. Canadian Journal of Zoology, 64, 168–175.CrossRefGoogle Scholar
Conand, C., 1981. Sexual cycle of three commercially important holothurian species (Echinodermata) from the lagoon of New Caledonia. Bulletin of Marine Science, 31, 523–543.Google Scholar
Conand, C., 1989. Les holothuries aspidochirotes du lagon de Nouvelle Caledonie: biologie, ecologie et exploitation. Etudes et Thèses, ORSTOM, Paris.Google Scholar
Conand, C., 1993. Reproductive biology of the holothurians from the major communities of the New Caledonian Lagoon. Marine Biology, 116, 439–450.CrossRefGoogle Scholar
Davis, H.S., 1971. The gonad walls of Echinodermata: a comparative study based on electron microscopy. MSc thesis, University of California, San Diego.Google Scholar
Eckelbarger, K.J., 1983. Evolutionary radiation in polychaete ovaries and vitellogenic mechanisms: their possible role in life history patterns. Canadian Journal of Zoology, 61, 487–504.CrossRefGoogle Scholar
Eckelbarger, K.J., in press. Diversity of metazoan ovaries and vitellogenic processes: implications for life history theory. Proceedings of the Biological Society of Washington.Google Scholar
Eckelbarger, K.J., Linley, P.A. & Grassle, J.P., 1984. Role of ovarian follicle cells in vitellogenesis and oocyte resorption in Capitella sp. I (Polychaeta). Marine Biology, 79, 133–144.CrossRefGoogle Scholar
Eckelbarger, K.J. & Young, C.M., 1992. Ovarian ultrastructure and vitellogenesis in ten species of shallow-water and bathyal sea cucumbers (Echinodermata: Holothuroidea). Journal of the Marine Biological Association of the United Kingdom, 72, 759–781.CrossRefGoogle Scholar
Eckelbarger, K.J., Young, C.M. & Cameron, J.L., 1989. Modified sperm in echinoderms from the bathyal and abyssal zones of the deep sea. In Reproduction, genetics and distributions of marine organisms (ed. J.S., Ryland and P.A., Tyler), pp. 67–74. Fredensborg: Olsen & Olsen.Google Scholar
Engstrom, N.A., 1980. Reproductive cycles of Holothuria (Halodeima) floridana, H. (H.) mexicana and their hybrids (Echinodermata: Holothuroidea) in southern Florida, USA. International Journal of Invertebrate Reproduction, 2, 237–244.CrossRefGoogle Scholar
Ferrand, J.G., 1984. Lysosomes and yolk formation in the oocytes of Asterina gibbosa (Echinodermata, Asteroidea). International Journal of Invertebrate Reproduction and Development, 7, 143–147.CrossRefGoogle Scholar
Gage, J.D., Billett, D.S.M., Jensen, M. & Tyler, P.A., 1985. The echinoderms of the Rockall Trough and adjacent areas. II. Echinoidea and Holothurioidea. Bulletin of the British Museum (Natural History) (Zoology), 48, 173–213.CrossRefGoogle Scholar
Gage, J.D. & Tyler, P.A., 1991. Deep-sea biology: a natural history of organisms at the deep-sea floor. Cambridge University Press.CrossRefGoogle Scholar
Hansen, B., 1975. Scientific results of the Danish deep-sea expedition round the world 1950–52: systematics and biology of the deep-sea holothurians. Galathea Reports, 13, 1–262.Google Scholar
Harriott, V., 1982. Sexual and asexual reproduction of Holothuria atra Jaeger at Heron Island Reef, Great Barrier Reef. Australian Museum Memoir, no. 16, 53–66.Google Scholar
Harriott, V.J., 1985. Reproductive biology of three congeneric sea cucumber species, Holothuria atra, H. impatiens and H. edulis, at Heron Reef, Great Barrier Reef. Australian Journal of Marine and Freshwater Research, 36, 51–57.Google Scholar
Hirai, S. & Kanatani, H., 1971. Site of production of meiosis-inducing substance in ovary of starfish. Experimental Cell Research, 67, 224–227.CrossRefGoogle ScholarPubMed
Hodgson, A.N. & Bernard, R.T.F., 1992. Spermatozoon structure of eight species of South African holothurians (Echinodermata). Journal of Morphology, 211,179–186.Google Scholar
Hylander, B.L. & Summers, R.G., 1975. An ultrastructural investigation of the spermatozoa of two ophiuroids, Ophiocoma echinata and Ophiocoma wendti: acrosomal morphology and reaction. Cell and Tissue Research. 158, 151–168.Google Scholar
Jamieson, B.G.M., 1985. The spermatozoa of the Holothuroidea (Echinodermata): an ultrastructural review with data on two Australian species and phylogenetic discussion. Zoological Scripta, 14, 123–135.CrossRefGoogle Scholar
Kessel, R.G., 1966. Some observations on the ultrastructure of the oocyte of Thyone briareus with special reference to the relationship of the golgi complex and endoplasmic reticulum in the formation of yolk. Journal of Ultrastructure Research, 16, 305–319.Google Scholar
Kessel, R.G., 1968. An electron microscope study of differentiation and growth in oocytes of Ophioderma panamensis. Journal of Ultrastructure Research, 22, 63–89.CrossRefGoogle ScholarPubMed
Kille, F.R., 1939. Regeneration of gonad tubules following extirpation in the sea-cucumber, Thyone briareus (Lesueur). Biological Bulletin. Marine Biological Laboratory, Woods Hole, 76, 70–79.CrossRefGoogle Scholar
Kille, F.R., 1942. Regeneration of the reproductive system following binary fission in the sea-cucumber, Holothuria parvula (Selenka). Biological Bulletin. Marine Biological Laboratory, Woods Hole, 83, 55–66.CrossRefGoogle Scholar
Krishnan, S., 1968. Histochemical studies on reproductive and nutritional cycles of the holothurian, Holothuria scabra. Marine Biology, 2, 54–65.CrossRefGoogle Scholar
Krishnan, S. & Dale, T., 1975. Ultrastructural studies on the testis of Cucumaria frondosa (Holothuroidea: Echinodermata). Norwegian Journal of Zoology, 23, 1–15.Google Scholar
Lönning, S., 1976. Reproductive cycle and ultrastructure of yolk development in some echinoderms from the Bergen area, western Norway. Sarsia, 62, 49–72.Google Scholar
Merrett, N.R. & Marshall, N.B., 1981. Observations on the ecology of two deep-sea bottom-living fishes collected off northwest Africa (08°-27°N). Progress in Oceanography, 9, 185–244.CrossRefGoogle Scholar
Miller, J.E. & Pawson, D.L., 1984. Holothurians (Echinodermata: Holothuroidea). Memoirs of the Hourglass Cruises, 7, 1–79.Google Scholar
Mortensen, T., 1927. Handbook of the echinoderms of the British Isles. Oxford University Press.CrossRefGoogle Scholar
Ohta, S., 1983. Photographic census of large-sized benthic organisms in the bathyal zone of Suruga Bay, central Japan. Bulletin of the Ocean Research Institute. University of Tokyo, no. 15, 1–244.Google Scholar
Ong, Che R.G. & Gomez, E.D., 1985. Reproductive periodicity of Holothuria scabra Jaeger at Calatagan, Batangas, Philippines. Asian Marine Biology, 2, 21–30.Google Scholar
Pearse, J.S., 1968. Patterns of reproductive periodicities in four species of Indo-Pacific echinoderms. Proceedings of the Indian National Science Academy, Part B, 67, 247–279.CrossRefGoogle Scholar
Piatigorsky, J., 1975. Gametogenesis. In The sea urchin embryo: biochemistry and morphogenesis (ed. R.A., Boolootian), pp. 63–71. New York: Interscience-Wiley.Google Scholar
Pladellorens, M. & Subirana, J.A., 1975. Spermiogenesis in the sea cucumber Holothuria tubulosa. Journal of Ultrastructure Research, 52, 235–242.CrossRefGoogle ScholarPubMed
Rice, A.L., Aldred, R.G., Darlington, E. & Wild, R.A., 1982. The quantitative estimation of deepsea megabenthos: a new approach to an old problem. Oceanologica Acta, 5, 63–72.Google Scholar
Ruppert, E.E. & Smith, P.R., 1988. The functional organization of filtration nephridia. Biological Reviews, 63, 231–258.Google Scholar
Sars, M., 1868. Om nogle Echinodermer og Coelenterater funde ved Lofoten. Forhandlinger i Videnskabs-Selskabet i Kristiania, 1867, 19–23.Google Scholar
Sewell, M.A., 1992. Reproduction of the temperate aspidochirote Stichopus mollis (Echinodermata: Holothuroidea) in New Zealand. Ophelia, 35, 103–121.CrossRefGoogle Scholar
Sewell, M.A. & Bergquist, P.R., 1990. Variability in the reproductive cycle of Stichopus mollis (Echinodermata: Holothuroidea). Invertebrate Reproduction and Development, 17, 1–7.CrossRefGoogle Scholar
Smiley, S., 1988. The dynamics of oogenesis and the annual ovarian cycle of Stichopus californicus (Echinodermata: Holothuroidea). Biological Bulletin. Marine Biological Laboratory, Woods Hole, 175, 79–93.CrossRefGoogle Scholar
Smiley, S., 1990. A review of echinoderm oogenesis. Journal of Electron Microscopy Techniques, 6, 93–114.CrossRefGoogle Scholar
Smiley, S. & Cloney, R.A., 1985. Ovulation and the fine structure of the Stichopus californicus (Echinodermata: Holothuroidae) fecund ovarian tubules. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 169, 342–364.CrossRefGoogle ScholarPubMed
Smiley, S., McEuen, F.S., Chaffee, C. & Krishnan, S. 1991. Echinodermata: Holothuroidea. In Reproduction of marine invertebrates. Vol. VI. Echinoderms and lophophorates (ed. A.C., Gieseet al.), pp. 663–750. Pacific Grove, California: Boxwood Press.Google Scholar
Tanaka, Y., 1958. Seasonal changes occurring in the gonad of Stichopus japonicus. Bulletin of the Faculty of Fisheries, Hokkaido University, 9, 29–36.Google Scholar
Théel, H., 1882. Holothurioidea. Report on the Scientific Results of the Voyage of HMS Challenger, 1873–76. Zoology, IV(8), 1–176.Google Scholar
Théel, H., 1901. On a singular case of hermaphrodism in Holothurids. Bihang Till K. Svenska Vetenskaps-Akademiens Handlingar (Zoology), 27, 1–38.Google Scholar
Tuwo, A. & Conand, C., 1992. Reproductive biology of the holothurian Holothuria forskali (Echinodermata). Journal of the Marine Biological Association of the United Kingdom, 72, 745–758.Google Scholar
Tyler, P.A. & Billett, D.S.M., 1988. The reproductive ecology of elasipodid holothurians from the NE Atlantic. Biological Oceanography, 5, 273–296.Google Scholar
Tyler, P. A., Billett, D.S.M. & Gage, J.D. 1987. The ecology and reproductive biology of Cherbonniera utriculus and Molpadia blakei from the NE Atlantic. Journal of the Marine Biological Association of the United Kingdom, 67, 385–387.CrossRefGoogle Scholar
Tyler, P.A. & Gage, J.D., 1983. The reproductive biology of Ypsilothuria talismani (Holothuroidea: Dendrochirota) from the NE Atlantic. Journal of the Marine Biological Association of the United Kingdom, 63, 609–616.Google Scholar
Tyler, P.A., Gage, J.D. & Billett, D.S.M., 1985a. Life-history biology of Peniagone azorica and P. diaphana (Echinodermata: Holothurioidea) from the north-east Atlantic Ocean. Marine Biology, 89, 71–81.CrossRefGoogle Scholar
Tyler, P.A., Muirhead, A., Billett, D.S.M. & Gage, J.D. 1985b. Reproductive biology of the deepsea holothurians Laetmogone violacea and Benthogone rosea (Elasipoda: Holothurioidea). Marine Ecology Progress Series, 23, 269–277.Google Scholar
Tyler, P.A., Young, C.M., 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, 447–462.CrossRefGoogle Scholar
Walker, M., Tyler, P.A. & Billett, D.S.M., 1987a. Biochemical and calorific content of deep-sea aspidochirotid holothurians from the northeast Atlantic Ocean. Comparative Biochemistry and Physiology, 88A, 549–551.CrossRefGoogle Scholar
Walker, M., Tyler, P.A. & Billett, D.S.M., 1987b. Organic and calorific content of the body tissues of deep-sea elasipodid holothurians in the northeast Atlantic Ocean. Marine Biology, 96, 277–282.CrossRefGoogle Scholar