Hostname: page-component-586b7cd67f-tf8b9 Total loading time: 0 Render date: 2024-11-24T03:40:42.742Z Has data issue: false hasContentIssue false
  • English
  • Français

Reproductive strategy of the invasive cockle Fulvia fragilis in the Bay of Tunis (Tunisia)

Published online by Cambridge University Press:  14 March 2011

Mouna Rifi ,
Gaël Le Pennec ,
Mohamed Ben Salem  and
Jamila Ben Souissi
Mouna Rifi*
Affiliation:
Département des Sciences Biologiques, Faculté des Sciences de Tunis, Campus Universitaire, Unité de Recherche Zoologie et Ecologie des Milieux Aquatiques, Campus Universitaire, 1002, le Belvédère, Tunis, Tunisia Laboratoire de Biotechnologie et Chimie Marines, Université de Bretagne Sud, BP 92116, 56321, Lorient, France
Gaël Le Pennec
Affiliation:
Laboratoire de Biotechnologie et Chimie Marines, Université de Bretagne Sud, BP 92116, 56321, Lorient, France
Mohamed Ben Salem
Affiliation:
Département des Sciences Biologiques, Faculté des Sciences de Tunis, Campus Universitaire, Unité de Recherche Zoologie et Ecologie des Milieux Aquatiques, Campus Universitaire, 1002, le Belvédère, Tunis, Tunisia
Jamila Ben Souissi
Affiliation:
Institut National Agronomique de Tunisie, 43 Avenue Charles Nicolle, Cité Mahrajène 1082, Tunis, Tunisia
*
Correspondence should be addressed to: M. Rifi, Département des Sciences Biologiques, Faculté des Sciences de Tunis, Campus Universitaire, Unité de Recherche Zoologie et Ecologie des Milieux Aquatiques, Campus Universitaire, 1002, le Belvédère, Tunis, Tunisia email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

This study is the first work on the reproductive biology of lessepsian bivalve Fulvia fragilis. Monthly and bimonthly samplings were made in the period from April 2006 to October 2007, at the Bay of Tunis (northern Tunisia). From histological preparations of gonad, a gametogenic scale was drawn up based on eight stages: sexual rest; initiation of gametogenesis; advanced gametogenesis; ripe; partial spawning; advanced spawning; restoration; and spent. After examination of gonad preparations, F. fragilis appeared to be a simultaneous hermaphrodite species. Spawning was continuous all along the year, scarce in winter and with peaks during the rest of the year. The spawning peaks were positively correlated with the rise of the sea surface temperature and the nutrient availability. Furthermore, the presence of oocytes surrounded by spermatozoa in female and male follicles and in male gonoducts was observed. Self-fertilization may occur in this species. High summer mortalities probably due to the combination of vulnerability of the bivalve in response to the reproductive effort and high temperature stress were recorded. The F. fragilis reproduction strategy explains the success of its installation on the Tunisian coast.

Keywords

Fulvia fragilislessepsian speciesgametogenesis scalehermaphroditismsuccess of installation
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 91 , Issue 7 , November 2011 , pp. 1465 - 1475
Copyright
Copyright © Marine Biological Association of the United Kingdom 2011

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aminot, A. and Chaussepied, M. (1983) Manuel des analyses chimiques en milieu marin. Brest: C.N.E.X.O.Google Scholar
Ansell, A.D. (1961) Reproduction, growth and mortality of Venus striatula (Da Costa) in Kamos Bay, Millport. Journal of the Marine Biological Association of the United Kingdom 41, 191–215.CrossRefGoogle Scholar
Ansell, A.D. (1974) Seasonal changes in the biochemical composition of the bivalve Abra abra from the Clyde Sea area. Marine Biology 25, 13–20.CrossRefGoogle Scholar
Ansell, A.D., Bodoy, A. and Massé, M. (1979) Incidence de la répartition géographique à l'échelle européenne sur la tolérance thermique de Mollusques marins. In 11é Journée de Thermo écologie, Colloque E.D.F., Nantes, pp. 1–14.Google Scholar
Araujo, R. and Ramos, M.A. (1997) Evidence of intrafollicular fertilization in Pisidium amnicum (Müller, 1774) (Mollusca: Bivalvia). Invertebrate Reproduction and Development 32, 267–272.CrossRefGoogle Scholar
Araujo, R. and Ramos, M.A. (1999) Histological description of the gonad, reproductive cycle, and fertilization of Pisidium amnicum (Müller, 1774) (Bivalvia: Spheriidae). Veliger 42, 124–131.Google Scholar
Barash, A. and Danin, Z. (1972) The Indo-Pacific species of Mollusca in the Mediterranean and notes on a collection from the Suez Canal. Israel Journal of Zoology 21, 301–371.Google Scholar
Beaumont, A.R. (1986) Genetic aspects of hatchery rearing of the scallop, Pecten maximus. Marine Biology 76, 285–289.CrossRefGoogle Scholar
Ben Charrada, R. and Moussa, M. (1997) Modélisation hydrodynamique et écologique des eaux côtières du golfe de Tunis. La Houille Blanche 6, 66–78.CrossRefGoogle Scholar
Ben Charrada, R., Moussa, M. and Zaouali, J. (1997) Analyse physico-chimique et biologique des eaux et du sédiment de la baie de Tunis. Marine Life 7, 53–66.Google Scholar
Beninger, P.G. and Le Pennec, M. (1991) Functional anatomy of scallops. In Shumway, S.E. (ed.) Scallops: biology, ecology and aquaculture. Amsterdam: Elsevier, pp. 133–224.Google Scholar
Ben Souissi, J., Rezig, M. and Zaouali, J. (2003) Appearance of invasive species in southern lake of Tunis. In Ozhan E. (ed.) Proceedings of the Sixth International Conference on the Mediterranean Coastal Environment, Ravenna, Italy, 7–11 October 2003. MEDCOAST, pp. 911–922.Google Scholar
Brey, T. (1995) Temperature and reproductive metabolism in macrobenthic populations. Marine Ecology Progress Series 125, 87–93.CrossRefGoogle Scholar
Charnov, E. (1979) Simultaneous hermaphroditism and sexual selection. Proceedings of the National Academy of Sciences of the United States of America, May 1979. Population Biology 76, 2480–2484.Google ScholarPubMed
Coe, W.R. (1941) Sexual phases in wood-boring molluscs. Biological Bulletin. Marine Biological Laboratory, Woods Hole 81, 168–176.CrossRefGoogle Scholar
Coe, W.R. (1943) Sexual differentiation in mollusks. I. Pelecypods. Quarterly Review of Biology 18, 154–164.CrossRefGoogle Scholar
Crocetta, F. (2005) Prime segnalizioni di Fulvia fragilis (Froskål in Niebuhr, 1775) (Mollusca: Bivalvia: Cardiidae) per I mari italiani. Bollettino Malacologico 41, 23–24.Google Scholar
Darriba, S., San Juan, F. and Guerra, A. (2004) Reproductive cycle of the razor clam Ensis Arcuautus (Jeffreys, 1865) in northwest Spain and its relation to environmental conditions. Journal of Experimental Marine Biology and Ecology 311, 101–115.CrossRefGoogle Scholar
Derbali, A., Jarboui, O. and Ghorbel, M. (2009) Reproductive biology of the cockle Cerastoderma glaucum (Mollusca: Bivalvia) from the north coast of Sfax (Gulf of Gabès, Tunisia). Ciencias Marinas 35, 141–152.CrossRefGoogle Scholar
Enríquez-Díaz, M., Pouvreau, S., Chávez-Villaba, J. and Le Pennec, M. (2009) Gametogenesis, reproductive investment, and spawning behaviour of the Pacific giant oyster Crassostrea gigas: evidence of an environment-dependent strategy. Aquaculture International 17, 491–506.CrossRefGoogle Scholar
Fisher-Piette, E. (1977) Révision des Cardiidae (Mollusques Lamellibranches). Mémoires du Muséum National d'Histoire Naturelle 101, 76–82.Google Scholar
Gabe, M. (1968) Techniques histologiques. Paris: Masson et Cie.Google Scholar
Gallucci, V.F. and Gallucci, B.B. (1982) Reproduction and ecology of the hermaphroditic cockle Clinocardium nuttalli (Bivalvia: Cardiidae) in Garrison Bay. Marine Ecology 7, 137–145.CrossRefGoogle Scholar
Gaspar, M.B., Ferreira, R. and Monteiro, C.C. (1999) Growth and reproductive cycle of Donax trunculus L., (Mollusca: Bivalvia) off Faro, southern Portugal. Fisheries Research 41, 309–316.CrossRefGoogle Scholar
Ghiselin, M.T. (1969) The evolution of hermaphroditism among animals. Quarterly Review of Biology 44, 189–208.CrossRefGoogle ScholarPubMed
Golani, D. (2002) The Indo-Pacific striped eel catfish, Plotosuslineatus (Thunberg, 1787), (Osteichtyes: Siluriformes) a new record from the Mediterranean. Scientia Marina 3, 321–323.CrossRefGoogle Scholar
Goudand, J. and Mifsud, C. (2009) Fulvia fragilis (Forsskål in Niebuhr, 1775) (Bivalvia: Cardiidae), an alien species new to the Maltese malacofauna. Aquatic Invasions 4, 389–391.CrossRefGoogle Scholar
Guillou, J., Bachelet, G., Desprez, M., Ducotoy, J.P., Madani, I., Rybarczyk, H., Sauriau, P.G., Sylvand, B., Elkaim, B. and Glemarc, M. (1990) Les modalités de la reproduction de la coque (Cerastoderma edule) sur le littoral français de la Manche et de l'Atlantique. Aquatic Living Resources 3, 29–41.CrossRefGoogle Scholar
Guillou, J., Bachelet, G., Rybarczyk, H. and Glemarc, M. (1992) Influence des fluctuations de la température sur la reproduction et le recrutement de la coque Cerastoderma edule (L.). Colloque du Programme National sur le Déterminisme du Recrutement, Nantes 68, 65–74.Google Scholar
Heath, D.J. (1977) Simultaneous hermaphroditism; cost and benefit. Journal of Theoretical Biology 64, 363–373.CrossRefGoogle ScholarPubMed
Heller, J. (1993) Hermaphroditism in molluscs. Biological Journal of the Linnean Society 48, 19–42.CrossRefGoogle Scholar
Hermann, M., Alfaya, J.E.F., Lepore, M.L., Penchaszadech, P.E. and Laudien, J. (2009) Reproductive cycle and gonad development of the Northern Argentinean Mesodesma mactroides (Bivalvia: Mesodesmatidae). Helgoland Marine Research 63, 207–218.CrossRefGoogle Scholar
Ibarra, A.M., Cruz, P. and Romero, B.A. (1995) Effects of inbreeding on growth and survival of self-fertilized catarina scallop larvae, Argopecten circularis. Aquaculture 134, 37–47.CrossRefGoogle Scholar
Ketata, I., Guermazi, F., Rebai, T. and Hamza-Chaffai, A. (2007) Variation of steroid concentrations during the reproductive cycle of the clam Ruditapes decussatus: a one year study in the Gulf of Gabès area. Comparative Biochemistry and Physiology Part A 147, 424–431.CrossRefGoogle ScholarPubMed
Le Pennec, M., Dorange, G., Beninger, P., Donval, A. and Widowati, I. (1992) Les relations trophiques anse intestinale-gonade chez Pecten maximus (Mollusque Bivalve). Société Française de Malacologie. Aspects Récents de la Biologie des Mollusques. Ifremer, Actes des Colloques 13, 57–70.Google Scholar
Le Pennec, G. and Le Pennec, M. (2002) Molecular analysis of the seasonal expression of genes coding for different functional markers of the digestive gland of the bivalve mollusc Pecten maximus (L.) Comparative Biochemistry and Physiology 133, 417–426.CrossRefGoogle Scholar
Limpanont, Y., Yang, H.S., Won, S.H., Han, S.J., Lee, J. B., Lee, B. G. and Choi, K.S. (2010) First report on the annual reproductive cycle of Burchardi's cockle Acrosterigma (=Vastricardium) burchardi Dunker 1877 (Bivalvia: Cardiidae) on a subtidal sand flat off southern Jeju Island, Korea. Invertebrate Reproduction and Development 54, 27–34.CrossRefGoogle Scholar
Lindner, G. (1988) Laevicardium (Fulvia) papyraceum (Bruguière, 1987)-von der sudturkishen Mittelmeerkuste (leg. Familie Schmidt, Feldkrichen). Club Conchylia Informationen 20, 35–37.Google Scholar
Liu, W., Li, Q., Yuan, Y. and Zhang, S. (2008) Seasonal variations in reproductive activity and biochemical composition of the cockle Fulvia mutica (Reeve) from the eastern coast of China. Journal of Shellfish Research 27, 405–411.CrossRefGoogle Scholar
Lubet, P. (1959) Recherches sur le cycle sexuel et l'émission des gamètes chez les mytilidés et les pectinidés (Mollusques bivalves). Revue des Travaux de l'Institut des Pêches Maritimes 23, 387–548.Google Scholar
Lubet, P. (1981) Action de la température sur le cycle de reproduction des lamellibranches. Bulletin de la Société Zoologique de France 106, 283–292.Google Scholar
Lubet, P. and Mann, R. (1987) Les différentes modalités de la reproduction chez les mollusques bivalves. Haliotis 16, 181–195Google Scholar
Mackie, G.L. (1984) Bivalves. In Wilbur, K. (ed.) The Mollusca. Reproduction. Volume 7. New York: Academic Press, pp. 351–418.Google Scholar
Mahmoud, N., Dellali, M., El Bour, M., Aissa, P. and Mahmoud, E. (2010) The use of Fulvia fragilis (Mollusca: Cardiidae) in the biomonitoring of Bizerta lagoon: a multimarkers approach. Ecological Indicators 10, 696–702.CrossRefGoogle Scholar
Mann, R. (1979) The effect of temperature on growth, physiology, and gametogenesis in the Manila clam Tapes philippinarum (Adams & Reeve, 1850). Journal of Experimental Marine Biology and Ecology 38, 121–133.CrossRefGoogle Scholar
Mansour, S., Rifi, M., Ben Souissi, J. and Zaouali, J. (2007) Contribution à l'étude de quelques aspects écobiologiques de Fulvia fragilis (Bivalve, Cardiidae) de la lagune de Bizerte (Tunisie Septentrionale, Méditerranée centrale). In VII éme Congrès Maghrébin des Sciences de la Mer et Premier Congrès Franco-Maghrébin de Zoologie et d'Ichtyologie. El Jadida (Maroc), p. 193.Google Scholar
Martínez, G., Mettifogo, L., Pérez, M.A. and Callejas, C. (2007) A method to eliminate self-fertilization in a simultaneous hermaphrodite scallop.1. Effects on growth and survival of larvae and juveniles. Aquaculture 273, 459–469.CrossRefGoogle Scholar
Meier-Brook, C. (1970) Untersuchungen zur Biologie einiger Pisidium-Arten (Mollusca: Eulamellibranchiata: Sphaeridae). Archiv für Hydrobiologie Supplement 38, 73–150.Google Scholar
Mohammad, S.H., Mohallal, M.E., Mohammed, S.Z. and Attia, M.N. (2006) Age and growth of the cockles Cerastoderma glaucum and Papyridea papyracea in Lake Timsah, Suez Canal. In Proceedings of the First International Conference on Conservation and management on Natural Resources, Ismailia, Egypt, 18–19 June 2006. Catrina, pp 25–32.Google Scholar
Occhipinti-Amborgi, A. and Galil, B. (2004) A uniform terminology on bioinvasions: a chimera or an operative tool? Marine Pollution Bulletin 49, 688–694.CrossRefGoogle Scholar
Okada, K. (1935) Some notes on Musculium heterodon (Pilsbry), a fresh water bivalve. III. Fertilization and segmentation. Science Reports of the Tohoku University 10, 467–483.Google Scholar
Oliver, P.G. (1992) The bivalve seashells of the Red Sea. An identification guide. Verlag Christa Hemmen and The National Museum of Wales, Cardiff.Google Scholar
Ozturk, B. and Poutiers, J.M. (2005) Fulvia fragilis (Bivalvia: Cardidae): a lessepsian mollusc species from Izmir Bay (Aegean Sea). Journal of the Marine Biological Association of the United Kingdom 85, 351–356.CrossRefGoogle Scholar
Park, G.M. and Chung, E.Y. (2004) Histological studies on hermaphroditism, gametogenesis and cyclic changes in the structures of marsupial gills of the introduced Asiatic clam, Corbicula fluminea, and the Korean clam, Corbicula leana. Journal of Shellfish Research 23, 179–184.Google Scholar
Passamonti, M. (1996) Nuova Segnalazione Per Le Coste Tunisine Di Papyridea papyracea (Gmelin, 1971) (Bivalvia: Cardiidae). Bollettino Malacologico 32, 153–156.Google Scholar
Pérès, J.M. (1967) The Mediterranean benthos. Oceanography and Marine Biology: an Annual Review 5, 449–533.Google Scholar
Pettinelli, R. and Bicchierai, M.C. (2009) Life cycle of Pisidium henslowanum (Sheppard, 1823) (Bivalvie, Veneroida, Sphaeriidae) from Piediluco Lake (Umbria, Italy). Fundamental and Applied Limnology 175, 79–92.CrossRefGoogle Scholar
Ruiz, C., Abad, M., Sedano, F., Garcia-Martin, L.O. and López Sández, J.L. (1992) Influence of seasonal environmental changes on the gamete production and biochemical composition of Crassostrea gigas (Thunberg) in suspended culture in El Grove, Galicia, Spain. Journal of Experimental Marine Biology and Ecology 155, 249–262.CrossRefGoogle Scholar
Stepanoff, P. (1865) Uber die Geschlechtsorgane und die Entwicklung von Cyclas cornea. Archiv für Naturgeschichte 31, 1–32.Google Scholar
Streftaris, N., Zenetos, A. and Papathanassiou, E. (2005) Globalisation in marine ecosystems: the story of non-indigenous marine species across European seas. Oceanography and Marine Biology: an Annual Review 43, 419–453.Google Scholar
Tirado, C., Salas, C. and Márquez, I. (2003) Reproduction of Venus verrucosa L., 1758 (Bivalvia: Veneridae) in the littoral of Malaga. Fisheries Research 63, 437–445.CrossRefGoogle Scholar
Tomlinson, J. (1966) The advantages of hermaphroditism and parthenogenesis. Journal of Theoretical Biology 11, 54–58.CrossRefGoogle ScholarPubMed
Vardala-Theodorou, G.E. (1999) The occurrence of the Indo-Pacific molluscan species Fulvia fragilis (Forsskål, 1775) and Bulla ampulla L., 1758 in Elefsis Bay. Newletter of the Hellenic Zoological Society 31, 10–11.Google Scholar
Vidal, J. (1994) A review of the genus Fulvia Gray, 1853 (Mollusca, Cardiidae). Apex 9, 93–118.Google Scholar
Woods, F.H. (1931) History of the germ cells in Sphaerium striatinum (Lam.). Journal of Morphology and Physiology 51, 545–595.CrossRefGoogle Scholar
Zaouali, J. (1974) Les peuplements malacologiques dans les biocoenoses lagunaires tunisiennes. Etude de la biologie de l'espèce pionnière Cerastoderma glaucum Poiret. PhD thesis. University of Caen, France.Google Scholar
Zaouali, J. (2008) Méditerranée: mixité ethnique et coexistence pacifique? Cas du Golfe de Tunis. In CIESM Workshop Monographs 35, Helgoland, Germany, 27–31 May 2008. Climate Warming and Changes in Mediterranean Marine Biota, pp. 89–98.Google Scholar
Zenetos, A., Gofas, S., Russo, G. and Templado, J. (2003) Atlas of exotic species in the Mediterranean. Volume 3. Molluscs. Monaco: CIESM.Google Scholar
Zenetos, A., Koutsoubas, D. and Vardala-Theodorou, E. (2005) Origin and vectors of introduction of exotic molluscs in Greek waters. Belgian Journal of Zoology 135, 279–286.Google Scholar