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Reproductive characteristics of Calyptogena gallardoi (Bivalvia: Vesicomyidae) from a methane seep area off Concepción, Chile

Published online by Cambridge University Press:  20 February 2009

Macarena Parra
Affiliation:
Universidad Católica del Norte, Facultad de Ciencias del Mar, Departamento de Biología Marina, Larrondo 1281, Coquimbo, Chile
Javier Sellanes*
Affiliation:
Universidad Católica del Norte, Facultad de Ciencias del Mar, Departamento de Biología Marina, Larrondo 1281, Coquimbo, Chile Centro de Investigación Oceanográfica en el Pacífico Sur-Oriental (COPAS), Universidad de Concepción, Casilla 160-C, Concepción, Chile
Enrique Dupré
Affiliation:
Universidad Católica del Norte, Facultad de Ciencias del Mar, Departamento de Biología Marina, Larrondo 1281, Coquimbo, Chile
Elena Krylova
Affiliation:
P.P. Shirshov Institute of Oceanology, Nakhimovskii Precinct, 36, Moscow, 117851, Russia
*
Correspondence should be addressed to: Javier Sellanes, Universidad Católica del Norte, Facultad de Ciencias del Mar, Departamento de Biología Marina, Larrondo 1281, Coquimbo, Chile email: sellanes@ucn.cl

Abstract

Calyptogena gallardoi is a vesicomyid bivalve inhabiting a methane seep area located at a depth of 740–870 m off the Bay of Concepción, Chile. Vesicomyids host chemoautotrophic sulphide-oxidizing endosymbiont bacteria and are always found associated to reducing environments. In this study, the gonadal structure and the gametes produced by C. gallardoi are described. Light microscopy is used to examine serial histological sections of the gonads, and scanning electron microscopy is used to visualize the external morphology of gametes. The gonads of both males and females are organized in ramified tubular acini. In males, mature sperm are stored near genital openings in acini lined with a secretor epithelium that resembles a seminal receptacle. Spermatozoids have bullet-like heads with an average length of 30.3±2.6 μm (mean±1 SD). In females, the mature oocytes are driven toward the genital opening through evacuator conduits lined by ‘paddle’ cilia. The average diameter of oogonias is 11.6±2.5 μm and that of mature oocytes is 273.8±23.1 μm, making the size of the mature oocyte among the largest reported for bivalves. In addition, C. gallardoi is shown to have external sexual dimorphism. Shells of males are significantly smaller and more elongated with sloping postero-dorsal margin compared with shells of females. The data are discussed in the context of available information on reproductive biology of vesicomyids.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2009

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References

REFERENCES

Beninger, P.G. and Le Pennec, M. (1997) Reproductive characteristics of a primitive bivalve from a deep-sea reducing environment: giant gametes and their significance in Acharax alinae (Cryptodonta: Solemyidae). Marine Ecology Progress Series 157, 195206.CrossRefGoogle Scholar
Berg, C.J. (1985) Reproductive strategies of mollusks from abyssal hydrothermal vent communities. Bulletin of the Biological Society of Washington 6, 185197.Google Scholar
Berg, C.J. and Alatalo, P. (1982) Reproductive strategies of bivalves from deep-sea hydrothermal vents and interidal sulfide-rich environments. Biological Bulletin. Marine Biological Laboratory, Woods Hole 163, 397.Google Scholar
Bruce, D. (1991) Atlas of invertebrate reproduction and development. 1st edition. New York: Wiley-Liss. 252 pp.Google Scholar
Campos, B. and Mann, R. (1988) Discocilia and paddle cilia in the larvae of Mulinia lateralis and Spisula solidissima (Mollusca: Bivalvia). Biological Bulletin. Marine Biological Laboratory, Woods Hole 175, 343348.CrossRefGoogle Scholar
Cary, S.C. and Giovannoni, S.J. (1993) Transovarial inheritance of endosymbiotic bacteria in clams inhabiting deep-sea hydrothermal vents and cold seeps. Proceedings of the National Academy of Sciences of the United States of America 90, 56955699.CrossRefGoogle ScholarPubMed
Coan, E.V., Scott, P.V. and Bernard, F.R. (2000) Bivalve seashells of western North America. Marine bivalve molluscs from Arctic Alaska to BajaCalifornia. Santa Barbara, CA: Santa Barbara Museum of Natural History.Google Scholar
Colaço, A., Martins, I., Laranjo, M., Pires, L., Prieto, C., Costa, V., Lopes, H., Rosa, D., Dando, P.R. and Serrão-Santos, R. (2006) Annual spawning of the hydrothermal vent mussel, Bathymodiolus azoricus, under controlled aquarium, conditions at atmospheric pressure. Journal of Experimental Marine Biology and Ecology 333, 166171.CrossRefGoogle Scholar
Dall, H.W. (1981) On some new or interesting West American shells obtained from the dredgings of the U.S. Fish Commission steamer “Albatross” in 1888, and other sources. Proceedings of the United States National Museum 17, 675733.CrossRefGoogle Scholar
Deiner, M. and Tamm, S.L. (1991) Mechanism of paddle cilia formation in molluscan veligers. Biological Bulletin. Marine Biological Laboratory, Woods Hole 181, 335336.CrossRefGoogle ScholarPubMed
Deiner, M., Tamm, S.L. and Tamm, S. (1993) Mechanical properties of ciliary axonemes and membranes as shown by paddle cilia. Journal of Cell Science 104, 12511262.CrossRefGoogle ScholarPubMed
Dixon, D.R., Lowe, D.M., Miller, P.I., Villemin, G.R., Colaco, A., Serrao-Santos, R. and Dixon, L.R.J. (2006) Evidence of seasonal reproduction in the Atlantic vent mussel Bathymodiolus azoricus, and an apparent link with the timing of photosynthetic primary production. Journal of the Marine Biological Association of the United Kingdom 86, 13631371.CrossRefGoogle Scholar
Eckelbarger, K.J. and Watling, L. (1995) Role of phylogenetic constraints in determining reproductive patterns in deep-sea invertebrates. Invertebrate Biology 114, 256269.CrossRefGoogle Scholar
Eckelbarger, K.J. and Young, C.M. (1999) Ultrastructure of gametogenesis in a chemosynthetic mytilid bivalve (Bathymodiolus childressi) from a bathyal, methane seep environment (northern Gulf of Mexico). Marine Biology 135, 635646.CrossRefGoogle Scholar
Ehlers, U. and Ehlers, B. (1978) Paddle cilia and discocilia, genuine structures? Cell Tissue Research 192, 489501.CrossRefGoogle ScholarPubMed
Endow, K. and Ohta, S. (1990) Occurrence of bacteria in the primary oocytes of vesicomyid clam Calyptogena soyoae. Marine Ecology Progress Series 64, 309311.CrossRefGoogle Scholar
Fiala-Medoni, A. and Le Pennec, M. (1989) Adaptive features of the bivalve molluscs associated with fluid venting in the subduction zones off Japan. Palaeogeography, Palaeoelimatology, Palaeoecology 71, 161167.CrossRefGoogle Scholar
Fujiwara, Y., Tsukahara, J., Hashimoto, J. and Fuikura, K. (1998) In situ spawning of a deeep-sea vesicomyid clam: evidence for an environmental cue. Deep-Sea Research 45, 18811889.CrossRefGoogle Scholar
Heyl, T.P., Gilhooly, W.P., Chambers, R.M., Gilchrist, G.W., Macko, S.A., Ruppel, C.D. and Van Dover, C.L. (2007) Characteristics of vesicomyid clams and their environment at the Blake Ridge cold seep, South Carolina, USA. Marine Ecology Progress Series 339, 169184.CrossRefGoogle Scholar
Healy, J.M. (1996) Molluscan sperm ultrastructure: correlation with taxonomic units within the Gastropoda, Cephalopoda and Bivalvia. In Taylor, J. (ed.) Origin and evolutionary radiation of the Mollusca. Oxford: Oxford University Press, pp. 99113.Google Scholar
Healy, J., Buckland-Nicks, J. and Barrie, G.M. (2001) Spermatozoal ultrastucture of spiny oysters (Spondylidae, Bivalvia) including a comparison with other bivalves. Invertebrate Reproduction and Development 41, 2737.CrossRefGoogle Scholar
Holmes, A., Oliver, P.G. and Sellanes, J. (2005) A new species of Lucinoma (Bivalvia: Lucinoidea) from a methane gas seep off the southwest coast of Chile. Journal of Conchology 38, 673682.Google Scholar
Jespersen, A. and Lützen, J. (2001) Ultrastructure of the seminal receptacle and the dimorphic sperm in the commensal bivalve Mysella bidentata (Veneroida; Galeommatoidea; Montacutidae). Acta Zoologica (Stockholm) 82, 107111.CrossRefGoogle Scholar
Jespersen, A., Lützen, J. and Morton, B. (2002) Ultrastructure of dimorphic sperm and seminal receptacle in the hermaphrodites Barrimysia siphonosomae and Pseudopythina ochetostomae (Bivalvia, Galeommatoidea). Zoomorphology 121, 159172.CrossRefGoogle Scholar
Kojima, S., Fujikura, K. and Okutani, T. (2004) Multiple trans-Pacific migrations of deep-sea vent/seep-endemic bivalves in the family Vesicomyidae. Molecular Phylogenetics and Evolution 32, 396406.CrossRefGoogle ScholarPubMed
Krylova, E.M. and Janssen, R. (2006) Vesicomyidae from Edison Seamount (South Western Pacific: Papua New Guinea: New Ireland fore-arc basin) (Bivalvia: Glossoidea). Archiv für Molluskenkunde 135, 233263.CrossRefGoogle Scholar
Krylova, E. and Sahling, H. (2006) Recent bivalve molluscs of the genus Calyptogena (Vesicomyidae). Journal of Molluscan Studies 72, 359395.CrossRefGoogle Scholar
Le Pennec, M. and Beninger, P.G. (1997) Ultrastructural characteristics of spermatogenesis in three species of deep-sea hydrothermal vent mytilids. Canadian Journal of Zoology 75, 308316.CrossRefGoogle Scholar
Le Pennec, G., Le Pennec, M., Beninger, P. and Dufour, S. (2002) Spermatogenesis in the archaic hydrothermal vent bivalve, Bathypecten vulcani, comparison of spermatozoon ultrastructure with littoral pectinids. Reproduction and Development 41, 1319.Google Scholar
Lisin, E.S., Hannan, E.E., Kochevar, R.E., Harrold, C. and Barry, J.P. (1997) Temporal variation in gametogenic cycles of vesicomyid clams. Invertebrate Reproduction and Development 31, 307318.CrossRefGoogle Scholar
Oliver, P.G. and Sellanes, J. (2005) Thyasiridae from a methane seepage area off Concepción, Chile. Zootaxa 1092, 120.CrossRefGoogle Scholar
Popham, J.D. (1979) Comparative spermatozoon morphology and bivalve phylogeny. Malacological Review 12, 120.Google Scholar
Sastry, A.N. (1979) Pelecypoda (excluding Ostreidae). In Giese, A. and Pearse, J.S. (eds) Reproduction of marine invertebrates. Volume V, Molluscs: pelecypods and lesser classes. New York: Academic Press, pp. 113292.CrossRefGoogle Scholar
Saleuddin, A. (1964) The gonads and reproductive cycle of Astarte sulcata (Da Costa) and sexuality in A. elliptica (Brown). Proceedings of the Malacological Society of London 36, 141148.Google Scholar
Sellanes, J. and Krylova, E. (2005) A new species of Calyptogena (Bivalvia: Vesicomyidae) from a recently discovered methane seepage area off Concepción Bay, Chile (~36° S). Journal of the Marine Biological Association of the United Kingdom 85, 969976.CrossRefGoogle Scholar
Sellanes, J., Quiroga, E. and Gallardo, V.A. (2004) First direct evidences of methane seepage and associated chemosynthetic communities in the bathyal zone off Chile. Journal of the Marine Biological Association of the United Kingdom 84, 10651066.CrossRefGoogle Scholar
Tyler, P.A. and Young, C.M. (1999) Reproduction and dispersal at vents and cold seeps. Journal of the Marine Biological Association of the United Kingdom 79, 193208.CrossRefGoogle Scholar
Tyler, P.A., Young, C.M., Dolan, E., Arellano, S.M., Brooke, S.D. and Baker, M. (2007) Gametogenic periodicity in the chemosynthetic cold-seep mussel ‘Bathymodiolus’ childressi. Marine Biology 150, 829840.CrossRefGoogle Scholar
Zar, H. (1998) Biostatistical analysis. 4th edition. Upper Saddle River, NJ: Prentice-Hall.Google Scholar