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Gametogenic cycle of the tropical vermetids Eualetes tulipa and Dendropoma corrodens (Mollusca: Caenogastropoda: Vermetidae)

Published online by Cambridge University Press:  09 December 2009

Patricia Miloslavich*
Affiliation:
Universidad Simón Bolívar, Departamento de Estudios Ambientales, Apartado Postal 89.000, Caracas 1080, Venezuela
Eduardo Klein
Affiliation:
Universidad Simón Bolívar, Departamento de Estudios Ambientales, Apartado Postal 89.000, Caracas 1080, Venezuela
Pablo Penchaszadeh
Affiliation:
Laboratorio de Invertebrados, Departamento de Biología, Facultad de Ciencias Exactas y Naturales, Universidad de Buenos Aires, Argentina
*
Correspondence should be addressed to: P. Miloslavich, Universidad Simón Bolívar, Departamento de Estudios Ambientales, Apartado Postal 89.000, Caracas 1080, Venezuela email: [email protected]

Abstract

The population density, annual gametogenic cycle, and size at sexual maturity of two vermetid species, Eualetes tulipa (invasive) and Dendropoma corrodens was studied in the southern Caribbean at the Planta Centro power plant intake channel and at Punta Mayorquina, Morrocoy National Park, respectively. Minimal size of mature females of E. tulipa and D. corrodens was 5.0 and 0.7 cm in body length respectively. The gonad represented between 44 to 47% of total body length, while it represented between 15 to 18% of total body volume (for both males and females). Gonad volume was significantly related to total body volume. A significant quadratic relationship between the number of capsules and female body volume was obtained for E. tulipa, indicating that females measuring 6–10 cm in body length are those that have the highest number of egg capsules. Females larger than 11 cm have a lower fecundity in terms of brooded capsules. Gonad sections of males and females of both species showed that several gametogenesis stages are simultaneous within the same individual. In the female, germ cells, oogoniums and primary oocytes with yolk granules were observed simultaneously. In the male, the spermatogonium, primary and secondary spermatocytes, spermatids and sperm cells were also observed within one gonad. The same pattern was observed throughout the year, showing no maturation/resting period or annual cycle. The area covered by D. corrodens was about 700 m2 with a mean density of 13,000 ind/m2. The area covered by the invasive E. tulipa was at least about 1000 m2, with a density of 27,000 to 29,000 ind/m2 in the first 3 m of depth. A follow up of the E. tulipa population showed that its density is increasing in time and has doubled in 20 years. This population increment could be related to an increase in organic suspended matter as evidenced in the region.

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

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References

REFERENCES

Bandel, K. (1975) Das Embryonalgehause karibischer Meso- und Neogastropoden (Mollusca). Akademie der Wissensschaften und der Literatur, Mainz 1, 1133.Google Scholar
Bandel, K. (1976) Observations on spawn, embryonic development and ecology of some Caribbean lower mesogastropoda. The Veliger 18, 249271.Google Scholar
Barroso, C.M. and Moreira, M.H. (1998) Reproductive cycle of Nassarius reticulatus in the Ria de Aveiro, Portugal: implications for imposex studies. Journal of the Marine Biological Association of the United Kingdom 78, 12331246.CrossRefGoogle Scholar
Bieler, R. (1996) Mörch's worm-snail taxa (Caenogastropoda: Vermetidae, Siliquariidae, Turritellidae). American Malacological Bulletin 13, 2335.Google Scholar
Birkeland, C. (1977) The importance of the rate of biomass accumulation in early successional stages of benthic communities to the survival of coral recruits. In Taylor, D.L. (ed.) Proceedings of the Third International Coral Reef Symposium, Miami, Florida, Volume 1: Biology. Rosenstiel School of Marine and Atmospheric Research, pp. 1521.Google Scholar
Birkeland, C. (1987) Nutrient availability as a major determinant of differences among coastal hard-substratum communities in different regions of the tropics. In Birkeland, C. (ed.) Comparison between Atlantic and Pacific tropical marine coastal ecosystems: community structure, ecological processes, and productivity. UNESCO Reports in Marine Science, 46, pp. 4398.Google Scholar
Calvo, M. (1999) Biología reproductora de tres especies de la familia Vermetidae (mollusca: Gastropoda) de las costas mediterráneas de la Península Ibérica. PhD thesis. Universidad Autónoma de Madrid, Madrid, Spain.Google Scholar
Calvo, M., Templado, J. and Penchaszadeh, P.E. (1998) Reproductive biology of the gregarious Mediterranean vermetid gastropod Dendropoma petraeum. Journal of the Marine Biological Association of the United Kingdom 78, 525549.CrossRefGoogle Scholar
Calvo, M. and Templado, J. (2004a) Reproduction and development in a vermetid gastropod, Vermetus triquetrus. Invertebrate Biology 123, 289303.CrossRefGoogle Scholar
Calvo, M. and Templado, J. (2004b) Reproduction and sex reversal of the solitary vermetid gastropod Serpulorbis arenarius. Marine Biology 146, 963973.CrossRefGoogle Scholar
Calvo, M., Templado, J., Oliverio, M. and Machordom, A. (2009) Hidden Mediterranean biodiversity: molecular evidence for a cryptic species complex within the reef building vermetid gastropod Dendropoma petraeum (Mollusca: Caenogastropoda). Biological Journal of the Linnean Society 96, 898912.CrossRefGoogle Scholar
Chaparro, O.R., Oyarzun, R.F., Vergara, A.M. and Thompson, R.J. (1999) Energy investment in nurse eggs and egg capsules in Crepidula dilatata Lamarck (Gastropoda, Calyptraeidae) and its influence on the hatching size of the juvenile. Journal of Experimental Marine Biology and Ecology 232: 261274.CrossRefGoogle Scholar
Chenu, J.C. (1842–1853) Illustrations conchyliologiques ou description et figures de toutes les coquilles connues vivantes et fossiles, classées suivant le système de Lamarck modifié d'après les progrès de la science et comprenant les genres nouveaux et les espèces rècemment découvertes. Paris: A. Franck.Google Scholar
Chollet, I. and Bone, D. (2007) Effects of heavy rainfall on polychaetes: differential spatial patterns generated by a large-scale disturbance. Journal of Experimental Marine Biology and Ecology 340, 113125.CrossRefGoogle Scholar
Coles, S.L. and Eldredge, L.G. (2002) Nonindigenous species introductions on coral reefs: A need for information. Pacific Science 56, 191209.CrossRefGoogle Scholar
Coles, S.L., DeFelice, R.C. and Eldredge, L.G. (2002) Nonindigenous marine species at Waikîkî and HawaìI Kai, ÒAhu, HawaìI. Final Report prepared for the David and Lucile Packard Foundation and the State of Hawaii Department of Land and Natural Resources, Division of Aquatic Resources, Honolulu. Bishop Museum Technical Report No. 25, 245 pp.Google Scholar
D'Orbigny, A. (1841) Mollusques—histoire physique, Politique et Naturelle de l'île de Cuba 1. Paris: Arthus Bertrand, pp. 1240.Google Scholar
Díaz, J.M. and Puyana, M. (1994) Moluscos del Caribe Colombiano. Un catálogo ilustrado. 1st edition. Colombia: Colciencias-Fundación Natura–INVEMAR.Google Scholar
Gendron, L. (1992) Determination of the size at sexual maturity of the waved whelk Buccinum undatum Linnaeus, 1758, in the Gulf of St. Lawrence, as a basis for the establishment of a minimum catchable size. Journal of Shellfish Research 11, 17.Google Scholar
Giménez, J. and Penchaszadeh, P.E. (2002) Reproductive cycle of Zidona dufresnei (Caenogastropoda: Volutidae) from the southwestern Atlantic Ocean. Marine Biology 140, 755761.Google Scholar
Giménez, J. and Penchaszadeh, P.E. (2003) Size at first sexual maturity in Zidona dufresnei (Caenogastropoda: Volutidae) of the south-western Atlantic Ocean (Mar del Plata, Argentina). Journal of the Marine Biological Association of the United Kingdom 83, 293296.CrossRefGoogle Scholar
Gould, S.J. (1994) Petaloconchus sculpturatus alaminatus, a new Pliocene subspecies of Vermetid gastropods lacking its defining generic character, with comments on Vermetid systematics in general. Journal of Paleontology 68, 10251036.CrossRefGoogle Scholar
Hadfield, M.G., Kay, E.A., Gillete, M.U. and Lloyd, M.C. (1972) The Vermetidae (Mollusca: Gastropoda) of the Hawaiian Islands. International Journal on Life in Oceans and Coastal Waters 12, 8198.Google Scholar
Harding, J.M., Mann, R. and Kiduff, C.W. (2007) The effects of female size on fecundity in a large marine gastropod Rapana venosa (Muricidae). Journal of Shellfish Research 26, 3342.CrossRefGoogle Scholar
Heller, J. (1993) Hermaphroditism in molluscs. Biological Journal of the Linnean Society 48, 1942.CrossRefGoogle Scholar
Himmelman, J.H. and Hamel, J.F. (1993) Diet, behaviour and reproduction of the whelk Buccinum undatum in the northern Gulf of St. Lawrence, eastern Canada. Marine Biology 116, 423430.CrossRefGoogle Scholar
Hodgson, A.N. and Eckelbarger, K. (2000) Ultrastructure of the ovary and oogenesis in six species of patellid limpets (Gastropoda: Patellogastropoda) from South Africa. Invertebrate Biology 119, 265277.CrossRefGoogle Scholar
Hughes, R.N. (1979) Notes on the reproductive strategies of the South African vermetid gastropods Dendropoma corallinaceum and Serpulorbis natalensis. The Veliger 21, 423427.Google Scholar
Hughes, R.N. and Lewis, A.H. (1974) On the distribution, feeding and reproduction of the vermetid gastropod Dendropoma maxima. Journal of Zoology, London 172, 531547.CrossRefGoogle Scholar
Jaeckle, W.B. (1995) Variation in the size, energy content, and biochemical composition of invertebrate eggs: correlates to the mode of larval development, In McEdward, L. (ed.) Ecology of marine invertebrate larvae. CRC Marine Science Series 6, pp. 4977.Google Scholar
Keen, A.M. (1961) A proposed reclassification of the gastropod family Vermetidae. Bulletin of the British Museum (Natural History) (Zoology) 7, 183214, pls. 54–55.Google Scholar
Keen, M. (1971) Sea-shells of tropical west America (marine mollusks from Baja California to Peru). 2nd edition. Stanford: Stanford University Press.Google Scholar
Lee, J.H. (1999) Gametogenesis and reproductive cycle of the rock shell, Reishia (Thais) clavigera (Neogastropoda: Muricidae), on the west coast of Korea. Korean Journal of Biological Sciences 3, 375383.CrossRefGoogle Scholar
Losada, F., Martín, A., Feragotto, W. and Alamo, C. (1988) Interacciones biológicas en el canal de toma de la planta termoeléctrica del centro en Punta Morón, Venezuela. Ecotrópicos 1, 5570.Google Scholar
Marshall, D.J. and Keough, M.J. (2008) The evolutionary ecology of offspring size in marine invertebrates. Advances in Marine Biology 53, 160.Google Scholar
Martel, A., Larrivée, D.H., Klein, K.R. and Himmelman, J.H. (1986a) Reproductive cycle and seasonal feeding activity of the neogastropod Buccinum undatum. Marine Biology 74, 7378.Google Scholar
Martel, A., Larrivée, D.H., Klein, K.R. and Himmelman, J.H. (1986b) Behaviour and timing of copulation and egg-laying in the neogastropod Buccinum undatum L. Journal of Experimental Marine Biology and Ecology 96, 2742.CrossRefGoogle Scholar
Miloslavich, P. (1987) Biología y estrategias reproductivas de Vermetus sp. y Dendropoma corrodens, dos especies pertenecientes a la familia Vermetidae (Gasterópodos, Prosobranquios). Licenciatura thesis. Universidad Simón Bolívar, Caracas, Venezuela.Google Scholar
Miloslavich, P. and Dufresne, L. (1994) Development and effect of female size on egg and juvenile production in the neogastropod Buccinum cyaneum from the Saguenay fjord. Canadian Journal of Fisheries and Aquatic Sciences 51, 28662872.CrossRefGoogle Scholar
Miloslavich, P. and Penchaszadeh, P.E. (1992) Reproductive biology of Vermetus sp. and Dendropoma corrodens (Orbigny, 1842): two Venezuelan gastropods from the Southern Caribbean. The Veliger 35, 7888.Google Scholar
Miloslavich, P., Penchaszadeh, P.E. and Klein, E. (2003) Reproduction of Crepidula navicula Morch, 1877 and Crepidula aplysioides Reeve, 1859 (Caenogastropoda) from Morrocoy and La Restinga Lagoon, Venezuela. The Nautilus 117, 121134.Google Scholar
Morton, J.E. (1951) The structure and adaptations of the New Zealand Vermetidae. Part I. The genus Serpulorbis. Transactions of the Royal Society of New Zealand 79, 119.Google Scholar
Morton, J.E. (1965) Form and function in the evolution of the Vermetidae. Bulletin of the British Museum (Natural History) 11, 585630.Google Scholar
Odriozola, A.L., Varela, R., Hu, C., Astor, Y., Lorenzoni, L. and Müller-Karger, F.E. (2007) On the absorption of light in the Orinoco River plume. Continental Shelf Research 27, 14471464.CrossRefGoogle Scholar
Oehlmann, J., Fioroni, P., Stroben, E. and Market, B. (1996) Tributyltin (TBT) effects on Ocinebra aciculata (Gastropoda: Muricidae): imposex development, sterilization, sex change and population decline. The Science of the Total Environment 188, 205223.CrossRefGoogle Scholar
Oliver, A.P.H. (1975) Hamlyn guide to shells of the world. London: Hamlyn.Google Scholar
Penchaszadeh, P., León, C.A., Alvarez, H., Bone, D., Castellano, P., Castillo, M.M., Díaz, Y., García, M.P., Lemus, M., Losada, F., Martín, A., Miloslavich, P., Paredes, C., Pérez, D., Sebastiani, M., Stecconi, D., Roa, V. and Villamizar, A. (2000) The coastline of Venezuela. In Sheppard, C. (ed.) Seas at the millennium. An environmental evaluation. University of Warwick, UK, Volume I: Europe, The Americas and West Africa, pp. 643661.Google Scholar
Perron, F. (1983) Growth, fecundity and mortality of Conus pennaceus in Hawaii. Ecology 64, 5362.CrossRefGoogle Scholar
Ray, G.L. (2005) Invasive marine and estuarine animals of Hawaii and other Pacific Islands. Aquatic Nuisance Species Research Program, ERDC/TN ANSRP-05-3, 19 pp.CrossRefGoogle Scholar
Ramírez-Llodra, E. (2002) Fecundity and life-history strategies in marine invertebrates. Advances in Marine Biology 43, 87170.CrossRefGoogle ScholarPubMed
Ramón, M. and Amor, M.J. (2002) Reproductive cycle of Bolinus brandaris and penis and genital duct size variations in a population affected by imposex. Journal of the Marine Biological Association of the United Kingdom 82, 435442.CrossRefGoogle Scholar
Schiaparelli, S., Albertelli, G. and Cattaneo-Vietti, R. (2006) Phenotypic plasticity of Vermetidae suspension feeding: a potential bias in their use as biological sea-level indicators. Marine Ecology 27, 4453.CrossRefGoogle Scholar
Schluker, A. (2003) State of Hawaii Aquatic Invasive Species Management Plan. The Department of Land and Natural Resources, Division of Aquatic Resources, The Nature Conservancy of Hawaii, 205 pp.Google Scholar
Strathmann, M.F. and Strathmann, R.R. (2006) A Vermetid gastropod with complex intracapsular cannibalism of nurse eggs and sibling larvae and a high potential for invasion. Pacific Science 60, 97108.CrossRefGoogle Scholar
Tello, J. (1975) Catálogo de la fauna venezolana VIII. Mollusca. Caracas, Venezuela: Arte.Google Scholar
Tetrault, F., Himmelman, J.H. and Measures, L. (2000) Impact of a castrating trematode, Neophasis sp., on the common whelk Buccinum undatum in the northern Gulf of St. Lawrence. Biological Bulletin. Marine Biological Laboratory, Woods Hole 198, 261271.CrossRefGoogle Scholar
Vega, A.J. and González, A. (2002) Moluscos del Pacífico Veraguense. Tecnociencia 4, 145.Google Scholar