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Shell morphology and relative growth variability of the invasive pearl oyster Pinctada radiata in coastal Tunisia

Published online by Cambridge University Press:  09 December 2011

Amel Bellaaj-Zouari*
Affiliation:
Institut National des Sciences et Technologies de la Mer, Centre La Goulette, Port de Pêche, 2060, Tunis, Tunisia
Souheil Dkhili
Affiliation:
Institut National des Sciences et Technologies de la Mer, Centre La Goulette, Port de Pêche, 2060, Tunis, Tunisia
Refka Gharsalli
Affiliation:
Institut National Agronomique de Tunisie, 43 Avenue Charles Nicolle, Tunis cité Marajéne, 1082, Tunisia
Abdelkrim Derbali
Affiliation:
Institut National des Sciences et Technologies de la Mer, Centre La Goulette, Port de Pêche, 2060, Tunis, Tunisia
Nejla Aloui-Bejaoui
Affiliation:
Institut National Agronomique de Tunisie, 43 Avenue Charles Nicolle, Tunis cité Marajéne, 1082, Tunisia
*
Correspondence should be addressed to: A. Bellaaj-Zouari, Institut National des Sciences et Technologies de la Mer, Centre La Goulette, Port de Pêche, 2060, Tunis, Tunisia email: [email protected]

Abstract

The variability of shell morphology and relative growth of the invasive pearl oyster Pinctada radiata was studied within and among ten populations from coastal Tunisia using discriminant tests. Therefore, 12 morphological characters were examined and 34 metric and weight ratios were defined. In addition to the classic morphological characters, populations were compared by the thickness of the nacreous layer. Results of Duncan's multiple comparison test showed that the most discriminative ratios were the width of nacreous layer of right valve to the inflation of shell, the hinge line length to the maximum width of shell and the nacre thickness to the maximum width of shell. The analysis of variance revealed an important inter-population morphological variability. Both multidimensional scaling analysis and the squared Mahalanobis distances (D2) of metric ratios divided Tunisian P. radiata populations into four biogeographical groupings: the north coast (La Marsa); harbours (Hammamet, Monastir and Zarzis); the Gulf of Gabès (Sfax, Kerkennah Island, Maharès, Skhira and Djerba) and the intertidal area (Ajim). However, the Kerkennah Island population was discriminated by the squared Mahalanobis distances (D2) of weight ratios in an isolated group suggesting particular trophic conditions in this area. The allometric study revealed high linear correlation between shell morphological characters and differences in allometric growth among P. radiata populations. Unlike the morphological discrimination, allometric differentiation shows no clear geographical distinction. This study revealed that the pearl oyster P. radiata exhibited considerable phenotypic plasticity related to differences of environmental and/or ecological conditions along Tunisian coasts and highlighted the discriminative character of the nacreous layer thickness parameter.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2011

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References

REFERENCES

Allen, E.G. (2006) New approaches to Fourier analysis of ammonoid sutures and other complex, open curves. Paleobiology 32, 299315.CrossRefGoogle Scholar
Al-Madfa, H., Abdel-Moati, M.A.R. and Al-Gimaly, F.H. (1998) Pinctada radiata (pearl oyster): a bioindicator for metal pollution monitoring in the Qatari waters (Arabian Gulf). Bulletin of Environmental Contamination and Toxicology 60, 245251.CrossRefGoogle ScholarPubMed
Al-Matar, S., Carpenter, K.E., Jackson, R., Al-Hazeem, S.H., AL-Saffar, A.H., Abdulghaffar, A.R. and Carpenter, C. (1993) Observations on the pearl oyster fishery of Kuwait. Journal of Shellfish Research 12, 3539.Google Scholar
Al-Sayed, H.A., Al-Rumaihi, E.M. and Al-Rumaidhm, M.J. (1993) Some morphometric measurements and population structure of the pearl oyster Pinctada radiata at two different coasts in Bahrain. Bahrain Center for Studies and Scientific Research Department (Report), 17 pp.Google Scholar
Anwar, N.A, Richardson, C.A. and Seed, R. (1990) Age determination, growth rate and population structure of the horse mussel Modiolus modiolus. Journal of the Marine Biological Association of the United Kingdom 70, 441457.CrossRefGoogle Scholar
Barash, A. and Danin, Z. (1992) Fauna Palaestina. Mollusca 1: annotated list of Mediterranean Molluscs of Israel and Sinai. Jerusalem: Israel Academy of Science and Humanities, 405 pp.Google Scholar
Batista, F.M., Ben-Hamadou, R., Fonseca, V.G., Taris, N., Ruano, F., Reis-Henriques, M.A. and Boudry, P. (2008) Comparative study of shell shape and muscle scar pigmentation in the closely related cupped oysters Crassostrea angulata, C. gigas and their reciprocal hybrids. Aquatic Living Resources 21, 3138.CrossRefGoogle Scholar
Beaumont, A. and Khamdan, S.A.A. (1991) Electrophoretic and morphometric characters in population differentiation of the pearl oyster Pinctada radiata (Leach) from around Bahrain. Journal of Molluscan Studies 57, 433441.CrossRefGoogle Scholar
Bouchon-Brandely, M. and Berthoule, A. (1891) Les pêches maritimes en Algérie et en Tunisie. Paris: Librairie Militaire de L. Baudoin, 118 pp.Google Scholar
Brake, J., Evans, F. and Langdon, C. (2004) Evidence for genetic control of pigmentation of shell and mantle edge in selected families of Pacific oysters, Crassostrea gigas. Aquaculture 229, 8998.CrossRefGoogle Scholar
Brown, J.R and Hartwick, E.B. (1988) A habitat suitability index model for suspended tray culture of the Pacific oyster Crassostrea gigas Thunberg. Aquaculture Research 19, 109126.CrossRefGoogle Scholar
Carino, M. and Monteforte, M. (1995) History of pearling in La Paz Bay, south Baja California. Gems and Gemology 2, 88105.CrossRefGoogle Scholar
Claxton, W.T., Wilson, A.B., Mackie, G.L. and Boulding, E.G. (1998) A genetic and morphological comparison of shallow- and deepwater populations of the introduced dreissenid bivalve Dreissena bugensis. Canadian Journal of Zoology 76, 12691276.CrossRefGoogle Scholar
Colgan, D.J. and Ponder, W.F. (2002) Genetic discrimination of morphologically similar sympatric species of pearl oysters (Mollusca: Bivalvia: Pinctada) in eastern Australia. Australian Journal of Marine Freshwater Research 53, 697709.CrossRefGoogle Scholar
Costa, C., Menesatti, P., Aguzzi, J., D'Andrea, S., Antonucci, F.Rimatori, V., Pallottino, F. and Mattoccia, M. (2010) External shape differences between sympatric populations of commercial clams Tapes decussatus and T. philippinarum. Food and Bioprocess Technology 3, 4348.CrossRefGoogle Scholar
De Mora, S., Fowler, S.W., Wyse, E. and Azemard, S. (2004) Distribution of heavy metals in marine bivalves, fish and coastal sediments in the Gulf and Gulf of Oman. Marine Pollution Bulletin 49, 410424.CrossRefGoogle ScholarPubMed
Derbali, A., Jarboui, O. and Ghorbel, M. (2011) Distribution, abundance and population structure of Pinctada radiata (Mollusca: Bivalvia) in southern Tunisian waters (central Mediterranean). Cahiers de Biologie Marine 52, 2331.Google Scholar
Di Natale, A. (1982) Extra-Mediterranean species of Mollusca along the southern Italian coasts. Malacologia 22, 571580.Google Scholar
Eagar, R.M.C. (1978) Shape and function of the shell: a comparison of some living and fossil bivalve mussels. Biological Review 53, 169210.CrossRefGoogle Scholar
Ferson, S.F., Rohlf, F.J. and Koehn, R.K. (1985) Measuring shape variation of two-dimensional outlines. Systematic Zoology 34, 5968.CrossRefGoogle Scholar
Fisher, W., Schnneider, M. and Baichat, M.L. (1987) Fiches FAO d'identification des espèces pour les besoins de la pêche. Rome: FAO.Google Scholar
Galil, B. (2000) A sea under siege—alien species in the Mediterranean. Biological Invasions 2, 177186.CrossRefGoogle Scholar
Galil, B. and Zenetos, A. (2002) A sea change—exotics in the Eastern Mediterranean. In Leppäkoski, E., Olenin, S. and Gollasch, S. (eds) Invasive aquatic species of Europe: distributions, impacts and management. Dordrecht, The Netherlands: Kluwer Academic Publishers, pp. 325336.CrossRefGoogle Scholar
Gervis, M.H. and Sims, N.A. (1992) The biology and culture of pearl oysters (Bivalvia: Pteriidae). International Centre for Living Aquatic Resources Management (ICLARM) Studies and Reviews 21, 49 pp.Google Scholar
Harry, H.W. (1985) Synopsis of the supraspecific classification of living oysters (Bivalvia: Gryphaeidae and Ostreidae). Veliger 28, 121158.Google Scholar
Herdman, W.A. and Hornell, J. (1903) Observations and experiments on the life history and habits of the pearl oyster. Reports of the Pearl Oyster Fisheries of the Gulf of Mannar 1, 125146.Google Scholar
Hynd, J.S. (1955) A revision of the Australian pearl-shells, genus Pinctada (Lamellibranchia). Australian Journal of Marine Freshwater Research 6, 98137.CrossRefGoogle Scholar
Imai, T. and Sakai, S. (1961) Study of breeding of Japanese oyster, Crassostrea gigas. Tohoku Journal of Agricultural Research 12, 125171.Google Scholar
Innes, D. J. and Bates, A. (1999) Morphological variation of Mytilus edulis and Mytilus trossulus in eastern Newfoundland. Marine Biology 133, 691–399.CrossRefGoogle Scholar
Ktari-Chakroun, F. and Azouz, A. (1971) Les fonds chalutables de la région Sud-Est de la Tunisie (golfe de Gabès). Bulletin de l'Institut d'Océanographie et de Pêche de Salammbô 2, 547.Google Scholar
Lawrence, D.R. (1995) Diagnosis of the genus Crassostrea (Bivalvia, Ostreidae). Malacologia 36, 185202.Google Scholar
Madec, L. and Daguzan, J. (1993) Geographic variation in reproductive traits of Helix aspersa Müller studied under laboratory conditions. Malacologia 35, 99117.Google Scholar
Martinez-Fernandez, E., Acosta Salmon, H., Rangel-Davalos, C., Olivera, A., Ruiz-Rubio, H. and Romo-Pinera, A.K. (2003) Spawning and larval culture of the pearl oyster Pinctada mazatlanica (Hanley, 1856) in the laboratory. World Aquaculture 34, 3639.Google Scholar
Matlins, A.L. (1996) The pearl book: the definitive buying guide. Woodstock, VT: Gemstone Press, 198 pp.Google Scholar
Meng, Z., Li, Y. and Xing, K. (1996) Theory and techniques on pearl culture. Beijing, China: Science Press.Google Scholar
Milet, C., Berland, S., Lamghari, M., Mouries, L., Jolly, C., Borzeix, S., Doumenc, D. and Lopez, E. (2004) Conservation of signal molecules involved in biomineralisation control in calcifying matrices of bone and shell. Comptes Rendus Palevol 3, 493501.CrossRefGoogle Scholar
Mohammed, S.Z. and Yassien, M.H. (2003) Population parameters of the pearl oyster Pinctada radiata (Leach, 1814) in Qatari waters, Arabian Gulf. Turkish Journal of Zoology 27, 339343.Google Scholar
Monterosato, T.A. (1878) Enumerazione e sinonimia delle conchiglie Mediterranee. Giornale di Scienze Naturali ed Economiche di Palermo 13, 61113.Google Scholar
Monterosato, T.A. (1899) Coquilles marins de chypre. Journal de Conchyliologie 57, 392397.Google Scholar
Newell, C.R. and Hidou, H. (1982) The effects of sediment type on growth rate and shell allometry in the soft shelled clam Mya arenaria (L). Journal of Experimental Marine Biology and Ecology 65, 285295.CrossRefGoogle Scholar
O'Connor, W.A and Lawler, N.F. (2004) Reproductive condition of the pearl oyster, Pinctada imbricata (Roding), in Port Stephens, New South Wales (Australia). Aquaculture Research 35, 385396.CrossRefGoogle Scholar
Oliverio, M., Gerosa, G. and Cocco, M. (1992) First record of Pinctada radiata (Bivalvia: Pteriidae) epibionte on the loggerhead turtle Caretta caretta (Chelonia: Cheloniidae). Bollettino Malacologico 28, 149152.Google Scholar
Oliverio, M. (1995) The status of the living Mediterranean Strombus, or: what is a lessepsian migrant? Notiziario del CISMA 16, 3540.Google Scholar
Palmer, M., Pons, G.X. and Linde, M. (2004) Discriminating between geographical groups of a Mediterranean commercial clam [Chamelea gallina (L): Veneridae] by shape analysis. Fisheries Research 67, 9398.CrossRefGoogle Scholar
Parache, A. and Massé, H. (1987) Influence des facteurs du milieu sur le cycle biologique de Mytilus galloprovincialis (Lamarck) en élevage sur corde dans l'Anse de Carteau (côte méditerranéenne française. Haliotis 16, 137147.Google Scholar
Por, F.D. (1978) Lessepsian migration—the influx of Red Sea biota into the Mediterranean Sea by way of the Suez Canal. Ecological Studies 23, 1228.CrossRefGoogle Scholar
Por, F.D. (1990) Lessepsian migration. An appraisal and new data. Bulletin de l'Institut Océanographique, Monaco 7, 110.Google Scholar
Ranson, G. (1961) Les espèces d'huîtres perlières du genre Pinctada (Biologie de quelques unes d'entre elles). Mémoires de l'Institut des Sciences Naturelles de Belgique 2, 195.Google Scholar
Ricordi, P. (1993) Segnelazione di Pinctada radiata (Leach, 1814) per il Tirreno meridionale. Notizario SIM 11, 4142.Google Scholar
Rufino, M.M., Gaspar, M.B., Pereira, A.M. and Vasconcelos, P. (2006) Use of shape to distinguish Chamelea gallina and Chamelea striatula (Bivalvia: Veneridae): linear and geometric morphometric methods. Journal of Morphology 267, 14331440.CrossRefGoogle ScholarPubMed
Sabelli, B. (1969) Ritrovamenti malacologici a Pantellaria e nei banchi de pesca tunisini. Conchiglie 5, 311.Google Scholar
Seed, R. (1980) Shell growth and form in Bivalvia. In Rhoads, D.C. and Lutz, R.A. (eds) Skeletal growth of aquatic organisms. Biological records of environmental change. New York: Plenum, pp. 2367.CrossRefGoogle Scholar
Seurat, L.G. (1929) La petite Pintadine du Golfe de Gabes. Bulletin de la Station d'Aquaculture et de Pêche de Castiglione 1, 928.Google Scholar
Shirai, S. (1994) Pearls and pearl oysters of the world. Marine Planning Company, Okinawa, Japan, 108 pp.Google Scholar
Stenzel, H.B. (1971) Oysters. In Moore, K.C. (ed.) Treatise on invertebrate paleontology. Part N. Volume 3. Mollusca 6. Geological Society of America Inc, Boulder, Colorado and the University of Kansas, Lawrence, pp. N935N1224.Google Scholar
Tlig Zouari, S. and Zaouali, J. (1994) Reproduction de Pinctada radiata (Leach, 1814, Mollusque, Bivalve) dans les îles Kerkennah (Tunisie). Marine Life 4, 4145.Google Scholar
Tlig Zouari, S. and Zaouali, J. (1998) Etude de quelques caractères biométriques de Pinctada radiata des îles Kerkenah (Tunisie). Annales de l'Institut Océanographique, Paris 2, 217224.Google Scholar
Tlig-Zouari, S., Rabaoui, L., Irathni, I. and Ben Hassine, O.K. (2009) Distribution, habitat and poulation densities of the invasive species Pinctada radiata (Mollusca: Bivalvia) along the Northern and Eastern coasts of Tunisia. Cahiers de Biologie Marine 50, 131142.Google Scholar
Tomlin, J.R. (1927) Report on the Mollusca (Amphineura, Gastropoda, Scaphopoda, Pelecypoda). Transactions of the Zoological Society of London 22, 291320.CrossRefGoogle Scholar
Vassel, E. (1899) La Pintadine de Vaillant et l'acclimatation de la mère perle sur le littoral tunisien. Journal de Conchyliologie 57, 416419.Google Scholar
Wada, K.T. (1994) Genetics of pearl oyster in relation to aquaculture. Japan Agricultural Research Quarterly 28, 276282.Google Scholar
White, J.N.C., Englar, J.R. and Carswell, B.L. (1990) Biochemical composition and energy reserves in Crassostrea gigas exposed to different levels of nutrition. Aquaculture 90, 157172.CrossRefGoogle Scholar
Yassien, M.H. (1998) Biological and ecological studies on the pearl oyster Pinctada radiata (Mollusca, Lamellibranchia) from the Red Sea with special reference to its tolerance to water pollution. PhD thesis. Faculty of Science, Ain Shams University.Google Scholar
Yassien, M.H., Abdel-Razek, F.A. and Kilada, R.W. (2000) Growth estimates of the pearl oyster Pinctada radiata from the Eastern Mediterranean. Egyptian Journal of Aquatic Biology and Fisheries 4, 105118.Google Scholar
Yu, D.H. and Chu, K.H. (2006) Low genetic differentiation among widely separated populations of the pearl oyster Pinctada fucata as revealed by AFLP. Journal of Experimental Marine Biology and Ecology 333, 140146.CrossRefGoogle Scholar
Zanette, Y. and Deslous-Paoli, J.M. (1983) Intérêt du préélevage de l'huître Crassostrea gigas en claire. Sciences et Pêches. Bulletin de l'Institut des Pêches Maritimes 333, 1115.Google Scholar
Zaouali, J. (1978) Les peuplements malacologiques de la mer de Bou Grara. Bulletin de l'Institut d'Océanographie et de Pêche de Salammbô 3, 107142.Google Scholar
Zaouali, J. and Beaten, S. (1985) Etude des peuplements macrobentiques de la zone centrale et du bassin oriental de la mer des Bibans (Tunisie méridionale) par la méthode de l'analyse factorielle des correspondances. Rapport de la Commission Internationale de la Mer Méditerranée 29, 199203.Google Scholar
Zenetos, A., Koutsoubas, D. and Vardala-Theodorou, E. (2004) Origin and vectors of introduction of exotic molluscs in Greek waters. Belgian Journal of Zoology 134, 161168.Google Scholar
Zibrowius, H. (1992) Ongoing modifications on the Mediterranean marine fauna and flora by the establishment of exotic species. Mesogée 51, 83107.Google Scholar