Anatomical differences among specimens of Pinctada imbricata Rí¶ding, 1798 from different South American localities
Keywords:
Bivalvia, Pteriomorphia, pearl oyster, anatomy, intraspecific variationAbstract
In the present study, we compared the internal and external anatomy of pearl oyster (Pinctada imbricata Rí¶ding, 1798) from some South American localities, including Venezuela and several regions of Brazil. The anatomical data shows non-geographical variations characterized by variable outline in adults, different degrees of posterior auricle shell development and mantle papillae ranging from normal to digitiform. The geographical variations can be divided into two major groups: the Venezuelan group presents a more folded mantle; pallial muscle grouped in anterior and median-posterior sets; poorly-developed perpendicular mantle groove; and inner lamella not extended into the anterior mantle. Brazilian group specimens present a smoother mantle, with less clear separation between anterior and posterior mantle muscle groups; externally-developed perpendicular groove; and inner lamella extension developed in anterior mantle. These differences may represent ecophenotypes or differences among isolated South American populations, which may be elucidated by subsequent phylogeographic studies.
References
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food for cultivated pearl oysters. Oceanologica Acta, 23(2): 193-210.
DAUPHIN, Y.; BALL, A.D.; COTTE, M.; CUIF, J.P.; MEIBOM, A.; SALOMÉ, M.; SUSINI, J.;WILLIAMS, T.C. 2008 Structure and composition of the nacreí prisms transition in the shell of Pinctada argaritifera (Mollusca, Bivalvia). Analytical and Bioanalytical Chemistry, 390(6): 1659-1669.
DEIDUN, A.; GIANNI, F.; CILIA, D.P.; LODOLA, A.;SAVINI, D. 2014 Morphometric analyses of a
Pinctada radiata (Leach, 1814) (Bivalvia: Pteriidae)population in the Maltese Islands. Journal of the
Black Sea/Mediterranean Environment, 20(1): 1-12.
DUVERNOY, G.L. 1853 Mémoires sur le systí¨me nerveux des mollusques acéphales lamellibranches ou bivalves. Mémoires de L'académie des Sciences de Paris, 24(1): 1-110.
FASSATOUI, C.; JENHANI, A.B.R.; ROMDHANE,M.S. 2014 Geographic pattern of shell morphology in the endemic freshwater mussel Unior avoisieri (Bivalvia: Unionidae) from northern Tunisia. Journal of Molluscan Studies,80(1): 152-160. doi: 10.1093/mollus/eyu069
FOUGEROUSE-TSING, A. and HERBAUT C. 1994 Atlas Anatomique de l'huí®tre perlií¨re: Pinctada
margaritifera. Établissement pour la valorisation des activités aquacoles et maritimes (EVAAM).
Centre Universitaire de Polynése Française, Punaauia. 68p.
FOUGEROUSE, A.; ROUSSEAU, M.; LUCAS, J.S 2008 Soft tissue anatomy, shell structure and
biomineralization. In: SOUTHGATE, P.C. and LUCAS, J.S. The Pearl Oyster. Oxford: Elsevier.
p.77-102.
GERVIS, M.H. and SIMS, N.A. 1992 The Biology and Culture of Pearl Oysters (Bivalvia, Pteriidae)
ICLARM Studies and Review, 21(1): 1-49.
HASZPRUNAR, G. 1983 Comparative analysis of the abdominal sense organs of Pteriomorpha
(Bivalvia). Journal of Molluscan Studies, 49(suppl.12A): 47-50.
HERDMAN, W.A. 1903 Observation and experiments on the life history and habits of the pearl oyster.In: HERDMAN, W.A. Report to the Government of Ceylon on the pearl oyster fisheries of the Gulf of Manaar. Part I. London: Royal Society. p.125-146.
HERDMAN, W.A. 1904 Anatomy of the pearl oyster (Margaritifera vulgaris, Schum). In: HERDMAN,
W.A. Report to the Government of Ceylon on the pearl oyster fisheries of the Gulf of Manaar. Part II.London: Royal Society. p.37-69.
HORNBACH, D.J.; MCLEOD, M.J.; GUTTMAN, S.I.;SEILKOP, S.K. 1980 Genetic and morphological
variation in the freshwater clam, Sphaerium (Bivalvia: Sphaeriidae). Journal of Molluscan
Studies, 46(2): 158-170.
HUBER, M. 2010 Compendium of bivalves. A full-color guide to 3,300 of the World’s Marine Bivalves. A status on Bivalvia after 250 years of research. Hackenheim: Conchbooks. 901p.
HYND, J.S. 1955 A revision of the Australian pearl shells, genus Pinctada (Lamelli-branchia). Marine and Freshwater Research, 6(1): 98-138.
HYND, J.S. 1960 An analysis of variation in Australian specimens of Pinctada albina (Lamarck)
(Lamellibranchia). Marine and Freshwater Research,11(3): 326-364.
KíÅ“HNELT, W. 1938 Der Anpassungstypus der Hammermuschel. Palaeobiologica, 6(1): 230í 241.
LODOLA, A.; NICOLINI, L.; SAVINI, D.; DEIDUN, A.; OCCHIPINTI-AMBROGI, A. 2013 Range
expansion and biometric features of Pinctada imbricata radiata (Bivalvia: Pteriidae) around
Linosa Island, Central Mediterranean Sea (Italy). Italian Journal of Zoology, 80(2): 303-312.
MAMANGKEY, N. 2009 Improving the quality of pearls from Pinctada maxima. Townsville
(Australia). 167p. (PhD Dissertation. James Cook University). Available at: <http://
researchonline.jcu.edu.au/11722/>
MASAOKA, T. and KOBAYASHI, T. 2002 Phylogenetic relationships in pearl oysters (Genus: Pinctada) based on nuclear rRNA sequences. DNA Polymorphism, 10(1): 100-104.
MASAOKA, T. and KOBAYASHI, T. 2005 Species identification of Pinctada imbricata using intergenic spacer of nuclear ribosomal RNA genes and mitochondrial 16S ribosomal RNA gene regions. Fisheries Science, 71(4): 837-846.
PELSENEER, P. 1911 Les lamellibranches de l’expédition Du Siboga. Partie Anatomique. E.J. Brill, Leiden. 353p.
OWEN, G. and STEEDMAN, H.F. 1958 Preservation of molluscs. Journal of Molluscan Studies, 3(3):
101-103.
POUVREAU, S.; GANGNERY, A.; TIAPARI, J.;LAGARDE, F.; GARNIER, M.; BODOY, A. 2000 Gametogenic cycle and reproductive effort of the tropical blacklip pearl oyster, Pinctada
margaritifera (Bivalvia: Pteriidae), cultivated in Takapoto atoll (French Polynesia). Aquatic Living
Resources, 13(1): 37-48.
RAJAEI, M.; POORBAGHER, H.; FARAHMAND, H.; MORTAZAVI, M.S..; EAGDERI, S. 2014 Interpopulation differences in shell forms of the pearl oyster Pinctada imbricata radiata Bivalvia:
Pterioida), in the northern Persian Gulf inferred from principal component analysis and elliptic
Fourier analysis. Turkish Journal of Zoology, 38(1):42-48.
RANSON, G. 1961 Les especes d'huitres perliéres du genre Pinctada (biologie de quelques-unes
d'entre elles). In: BELGIQUE, I.R.D.S.N.D. Mémoires, deuxií¨me série, 67(2): 3-95.
SHIRAI, S. 1994 Pearls and pearl oysters of the world. Okinawa: Marine Planning. 108p.
SIMONE, L.R.L. and GONí"¡ALVES, E.P. 2006 Anatomical study on Myoforceps aristatus, an
invasive boring bivalve in SE Brazilian coast (Mytilidae). Papéis Avulsos de Zoologia, 46(6): 57-65.
STANLEY, S.M. 1970 Relation of shell form to life habits of the Bivalvia (Mollusca). Geological
Society of America Memoirs, 125(1): 1-296.
Tí"¹MKIN, I. 2006 Morphological perspective on the classification and evolution of Recent Pterioidea (Mollusca: Bivalvia). Zoological Journal of the Linnean Society, 148(3): 253-312.
THIELE, J. 1886 Die Mundlappen der Lamellibranchiaten. Zeitschriftfür Wissenschaftliche
Zoologie, 44(1): 239í 272.
THOMAS, S.D.K. 1976 Constraints of ligament growth, form and function on evolution in the
Arcoida (Mollusca: Bivalvia). Paleobiology, 2(1):64-83.
THURSTON, E. 1890 Notes on the Pearl and Chank Fisheries and Marine Fauna of the Gulf of Manaar.British India: Madras. 10p.
TRUEMAN, E.R.; BRAND, A.R; DAVIS, P. 1966 The dynamics of burrowing of some common littoral
bivalves. Journal of Experimental Biology, 44(3):469-492.
URBAN, H. 2000 Culture potential of the pearl oyster (Pinctada imbricata) from the Caribbean: II. Spat collection, and growth and mortality in culture systems. Aquaculture, 189(3): 375-388.
UBUKATA, T. 2003 A morphometric study on morphological plasticity of shell form in creviceâ€Â
dwelling Pterioida (Bivalvia). Biological Journal of the Linnean Society, 79(2): 285-297.
VELAYUDHAN, T.S. and GANDHI, A.D. 1987 Morphology and anatomy of Indian pearl oyster. CMFRI Bulletin-Pearl Culture, 39(1): 4-12.
YONGE, C.M. 1962 On the primitive significance of the byssus in the Bivalvia and its effects in
evolution. Journal of the Marine Biological Association of the United Kingdom, 42(1): 113-125.
YONGE, C.M. 1968 Form and habit in species of Malleus (including the" hammer oysters") with
comparative observations on Isognomon isognomon. Biological Bulletin, 135(3): 378-405.
YONGE, C.M. 1979 Cementation in bivalves. In: VAN DER SPOEL, S.; VAN BRUGGEN, A.C.; LEVER, J. Pathways in Malacology. Utrecht: Bohn, Scheltema, Holkema and Jong. 83p.
YUKIHIRA, H.; LUCAS, J.S.; KLUMPP, D.W. 2006 The pearl oysters, Pinctada maxima and P.
margaritifera, respond in different ways to culture in dissimilar environments. Aquaculture,
252(2): 208-224.
WADA, K. and Tí"¹MKIN, I. 2008 Taxonomy and Phylogeny. In: SOUTHGATE, P.C. and LUCAS,
J.S. The Pearl Oyster. Oxford: Elsevier. p.37-75.
food for cultivated pearl oysters. Oceanologica Acta, 23(2): 193-210.
DAUPHIN, Y.; BALL, A.D.; COTTE, M.; CUIF, J.P.; MEIBOM, A.; SALOMÉ, M.; SUSINI, J.;WILLIAMS, T.C. 2008 Structure and composition of the nacreí prisms transition in the shell of Pinctada argaritifera (Mollusca, Bivalvia). Analytical and Bioanalytical Chemistry, 390(6): 1659-1669.
DEIDUN, A.; GIANNI, F.; CILIA, D.P.; LODOLA, A.;SAVINI, D. 2014 Morphometric analyses of a
Pinctada radiata (Leach, 1814) (Bivalvia: Pteriidae)population in the Maltese Islands. Journal of the
Black Sea/Mediterranean Environment, 20(1): 1-12.
DUVERNOY, G.L. 1853 Mémoires sur le systí¨me nerveux des mollusques acéphales lamellibranches ou bivalves. Mémoires de L'académie des Sciences de Paris, 24(1): 1-110.
FASSATOUI, C.; JENHANI, A.B.R.; ROMDHANE,M.S. 2014 Geographic pattern of shell morphology in the endemic freshwater mussel Unior avoisieri (Bivalvia: Unionidae) from northern Tunisia. Journal of Molluscan Studies,80(1): 152-160. doi: 10.1093/mollus/eyu069
FOUGEROUSE-TSING, A. and HERBAUT C. 1994 Atlas Anatomique de l'huí®tre perlií¨re: Pinctada
margaritifera. Établissement pour la valorisation des activités aquacoles et maritimes (EVAAM).
Centre Universitaire de Polynése Française, Punaauia. 68p.
FOUGEROUSE, A.; ROUSSEAU, M.; LUCAS, J.S 2008 Soft tissue anatomy, shell structure and
biomineralization. In: SOUTHGATE, P.C. and LUCAS, J.S. The Pearl Oyster. Oxford: Elsevier.
p.77-102.
GERVIS, M.H. and SIMS, N.A. 1992 The Biology and Culture of Pearl Oysters (Bivalvia, Pteriidae)
ICLARM Studies and Review, 21(1): 1-49.
HASZPRUNAR, G. 1983 Comparative analysis of the abdominal sense organs of Pteriomorpha
(Bivalvia). Journal of Molluscan Studies, 49(suppl.12A): 47-50.
HERDMAN, W.A. 1903 Observation and experiments on the life history and habits of the pearl oyster.In: HERDMAN, W.A. Report to the Government of Ceylon on the pearl oyster fisheries of the Gulf of Manaar. Part I. London: Royal Society. p.125-146.
HERDMAN, W.A. 1904 Anatomy of the pearl oyster (Margaritifera vulgaris, Schum). In: HERDMAN,
W.A. Report to the Government of Ceylon on the pearl oyster fisheries of the Gulf of Manaar. Part II.London: Royal Society. p.37-69.
HORNBACH, D.J.; MCLEOD, M.J.; GUTTMAN, S.I.;SEILKOP, S.K. 1980 Genetic and morphological
variation in the freshwater clam, Sphaerium (Bivalvia: Sphaeriidae). Journal of Molluscan
Studies, 46(2): 158-170.
HUBER, M. 2010 Compendium of bivalves. A full-color guide to 3,300 of the World’s Marine Bivalves. A status on Bivalvia after 250 years of research. Hackenheim: Conchbooks. 901p.
HYND, J.S. 1955 A revision of the Australian pearl shells, genus Pinctada (Lamelli-branchia). Marine and Freshwater Research, 6(1): 98-138.
HYND, J.S. 1960 An analysis of variation in Australian specimens of Pinctada albina (Lamarck)
(Lamellibranchia). Marine and Freshwater Research,11(3): 326-364.
KíÅ“HNELT, W. 1938 Der Anpassungstypus der Hammermuschel. Palaeobiologica, 6(1): 230í 241.
LODOLA, A.; NICOLINI, L.; SAVINI, D.; DEIDUN, A.; OCCHIPINTI-AMBROGI, A. 2013 Range
expansion and biometric features of Pinctada imbricata radiata (Bivalvia: Pteriidae) around
Linosa Island, Central Mediterranean Sea (Italy). Italian Journal of Zoology, 80(2): 303-312.
MAMANGKEY, N. 2009 Improving the quality of pearls from Pinctada maxima. Townsville
(Australia). 167p. (PhD Dissertation. James Cook University). Available at: <http://
researchonline.jcu.edu.au/11722/>
MASAOKA, T. and KOBAYASHI, T. 2002 Phylogenetic relationships in pearl oysters (Genus: Pinctada) based on nuclear rRNA sequences. DNA Polymorphism, 10(1): 100-104.
MASAOKA, T. and KOBAYASHI, T. 2005 Species identification of Pinctada imbricata using intergenic spacer of nuclear ribosomal RNA genes and mitochondrial 16S ribosomal RNA gene regions. Fisheries Science, 71(4): 837-846.
PELSENEER, P. 1911 Les lamellibranches de l’expédition Du Siboga. Partie Anatomique. E.J. Brill, Leiden. 353p.
OWEN, G. and STEEDMAN, H.F. 1958 Preservation of molluscs. Journal of Molluscan Studies, 3(3):
101-103.
POUVREAU, S.; GANGNERY, A.; TIAPARI, J.;LAGARDE, F.; GARNIER, M.; BODOY, A. 2000 Gametogenic cycle and reproductive effort of the tropical blacklip pearl oyster, Pinctada
margaritifera (Bivalvia: Pteriidae), cultivated in Takapoto atoll (French Polynesia). Aquatic Living
Resources, 13(1): 37-48.
RAJAEI, M.; POORBAGHER, H.; FARAHMAND, H.; MORTAZAVI, M.S..; EAGDERI, S. 2014 Interpopulation differences in shell forms of the pearl oyster Pinctada imbricata radiata Bivalvia:
Pterioida), in the northern Persian Gulf inferred from principal component analysis and elliptic
Fourier analysis. Turkish Journal of Zoology, 38(1):42-48.
RANSON, G. 1961 Les especes d'huitres perliéres du genre Pinctada (biologie de quelques-unes
d'entre elles). In: BELGIQUE, I.R.D.S.N.D. Mémoires, deuxií¨me série, 67(2): 3-95.
SHIRAI, S. 1994 Pearls and pearl oysters of the world. Okinawa: Marine Planning. 108p.
SIMONE, L.R.L. and GONí"¡ALVES, E.P. 2006 Anatomical study on Myoforceps aristatus, an
invasive boring bivalve in SE Brazilian coast (Mytilidae). Papéis Avulsos de Zoologia, 46(6): 57-65.
STANLEY, S.M. 1970 Relation of shell form to life habits of the Bivalvia (Mollusca). Geological
Society of America Memoirs, 125(1): 1-296.
Tí"¹MKIN, I. 2006 Morphological perspective on the classification and evolution of Recent Pterioidea (Mollusca: Bivalvia). Zoological Journal of the Linnean Society, 148(3): 253-312.
THIELE, J. 1886 Die Mundlappen der Lamellibranchiaten. Zeitschriftfür Wissenschaftliche
Zoologie, 44(1): 239í 272.
THOMAS, S.D.K. 1976 Constraints of ligament growth, form and function on evolution in the
Arcoida (Mollusca: Bivalvia). Paleobiology, 2(1):64-83.
THURSTON, E. 1890 Notes on the Pearl and Chank Fisheries and Marine Fauna of the Gulf of Manaar.British India: Madras. 10p.
TRUEMAN, E.R.; BRAND, A.R; DAVIS, P. 1966 The dynamics of burrowing of some common littoral
bivalves. Journal of Experimental Biology, 44(3):469-492.
URBAN, H. 2000 Culture potential of the pearl oyster (Pinctada imbricata) from the Caribbean: II. Spat collection, and growth and mortality in culture systems. Aquaculture, 189(3): 375-388.
UBUKATA, T. 2003 A morphometric study on morphological plasticity of shell form in creviceâ€Â
dwelling Pterioida (Bivalvia). Biological Journal of the Linnean Society, 79(2): 285-297.
VELAYUDHAN, T.S. and GANDHI, A.D. 1987 Morphology and anatomy of Indian pearl oyster. CMFRI Bulletin-Pearl Culture, 39(1): 4-12.
YONGE, C.M. 1962 On the primitive significance of the byssus in the Bivalvia and its effects in
evolution. Journal of the Marine Biological Association of the United Kingdom, 42(1): 113-125.
YONGE, C.M. 1968 Form and habit in species of Malleus (including the" hammer oysters") with
comparative observations on Isognomon isognomon. Biological Bulletin, 135(3): 378-405.
YONGE, C.M. 1979 Cementation in bivalves. In: VAN DER SPOEL, S.; VAN BRUGGEN, A.C.; LEVER, J. Pathways in Malacology. Utrecht: Bohn, Scheltema, Holkema and Jong. 83p.
YUKIHIRA, H.; LUCAS, J.S.; KLUMPP, D.W. 2006 The pearl oysters, Pinctada maxima and P.
margaritifera, respond in different ways to culture in dissimilar environments. Aquaculture,
252(2): 208-224.
WADA, K. and Tí"¹MKIN, I. 2008 Taxonomy and Phylogeny. In: SOUTHGATE, P.C. and LUCAS,
J.S. The Pearl Oyster. Oxford: Elsevier. p.37-75.
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