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Biodegradation of shells of the black pearl oyster, Pinctada margaritifera var. cumingii, by microborers and sponges of French Polynesia

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Abstract

The composition, distribution and infestation sequence of organisms that destroy the commercially valuable shells of the black oyster Pinctada margaritifera var. cumingii Jameson, 1901 were studied. Three ecologically different groups of boring (euendolithic) organisms were identified: (1) phototrophic boring microorganisms (cyanobacteria, Hyella caespitosa, Hyella sp., Mastigocoleus testarum, Plectonema terebrans, and green algae, Phaeophila dendroides, Ostreobium quekettii); (2) heterotrophic boring microorganisms (fungi, Ostracoblabe implexa); (3) filter-feeding boring organisms (sponges, Cliona margaritiferae, C. vastifica). The phototrophic endoliths dominate the external pristmatic region of the shell, whereas the valuable interior nacreous region is attacked mainly by heterotrophs. Boring patterns reflect in part the shape and behaviour of the organisms and in part the structural properties of the shell, and inflict different types of damage. Infestation starts with microbial borers, which prepare the conditions for later invasion by more damaging clionid sponges. The infestation begins always at the apex, the oldest part of the shells, from which the periostracum is often removed by natural attrition or by cleaning procedure. The rate of bioerosion in 1 yr-old hatchery shells is 36 times higher than in natural populations.

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References

  • Alagarswami K, Chellam A (1976) On fouling and boring organisms and mortality of pearl oysters in the farm at Veppalodai, Gulf of Mannar. Indian J Fish 23: 10–12

    Google Scholar 

  • Alderman DJ, Jones EBG (1967) Shell disease of Ostrea edulis L. Nature, Lond 216: 797–798

    Google Scholar 

  • Bevelander G, Nakahara H (1969) An electron microscope study of the formation of the nacreous layer in the shell of certain bivalve molluscs. Calcif Tissue Res 3: 84–92

    Google Scholar 

  • Bonar L (1936) An unusual ascomycete in the shells of marine animals. Univ Calif Publs Bot 19: 187–194

    Google Scholar 

  • Bornet E, Flahault C (1889) Sur quelques plantes vivant dans le test calcaire des mollusques. Bull Soc bot Fr 36: 147–176

    Google Scholar 

  • Cabral P (1989) Problems and perspecitives of the pearl oyster aquaculture in French Polynesia. Advances in Tropical aquaculture, Tahiti-Aquacop. Act Colloques, IFREMER, 9: 57–66

    Google Scholar 

  • Caseiro J (1993) Biomineralisation, paramètres et processus de croissance, effects chromatiques dans la coquille et la perle de Pinctada margaritifera. Doctoral thesis. Université de Lyon 1, France

    Google Scholar 

  • Cavaliere AR, Alberte RA (1970) Fungi in animal shell fragments J Elisha Mitchell scient Soc 86: 202–206

    Google Scholar 

  • Chazottes V, Le Campion-Alsumard T, Peyrot-Clausade M (1995) Bioerosion rates on coral reefs: interactions between macroborers, microborers and grazers (Moorea, French Polynesia). Paleogeogr Paleoclim Paleoecol 113: 189–198

    Google Scholar 

  • Cobb WR (1969) Penetration of calcium carbonate substrates by the boring sponge, Cliona. Am Zool 9: 783–790

    Google Scholar 

  • Cobb WR (1975) Fine structural features of destruction of calcareous substrata by the burrowing sponge Cliona celata. Trans Am microsc Soc 94: 197–202

    Google Scholar 

  • Cuif JP, Dauphin Y (1995) Disturbed mineralization process in shells and pearls of Pinctada margaritifera from French Polynisia (sic) Microstructural and biochemical patterns. Abstract. International workshop on shell disease in marine invertebrates: environment-host-pathogen interactions. Brest, IFREMER, Centre de Plouzané, France

    Google Scholar 

  • Dharmaraj S, Chellam A, Velayudhan TS (1987) Biofouling, boring and predation of pearl oyster. Bull cent mar Fish Res Inst (Indian Counc. agric Res) Cohin 39: 92–99

    Google Scholar 

  • Fredj G, Falconetti C (1977) Sur la présence d'algues filamenteuses perforantes dans le test des Gryphus vitreus (Born) (brachiopodes, térébratulidés) de la limite inférieure du plateau continental méditerranéen. Cr hebd Séanc Acad Sci, Paris 284: 1167–1170

    Google Scholar 

  • Gatrall M, Golubic S (1970) Comparative study on some Jurassic and recent endolithic fungi using scanning electron microscope. Geol J (Spec Iss) 3: 167–178

    Google Scholar 

  • Golubic S, Brent G, Le Campion-Alsumard T (1970) Scanning electron microscopy of endolithic algae and fungi using a multipurpose casting-embedding technique. Lethaia 3: 203–209

    Google Scholar 

  • Golubic S, Cambell SE, Drobne K, Cameron B, Balsam WL, Cimerman F, Dubois L (1984) Microbial endoliths: a benthic cross-reference with foraminifera. J Paleont 58: 351–361

    Google Scholar 

  • Golubic S, Friedmann I, Schneider J (1981) The lithobiontic ecological niche, with special reference to microorganisms. J sedim Petrol 51: 475–478

    Google Scholar 

  • Golubic S, Perkins RD, Lukas KJ (1975) Boring microorganisms and microborings in carbonate substrates. In: Frey RW (ed) The study of trace fossils. Springer-Verlag, Berlin Heidelberg New York, pp 229–259

    Google Scholar 

  • Goreau TF, Hartman WD (1963) Boring sponges as controlling factors in the formation and maintenance of coral reefs. Publs Am Ass Advmnt Sci 75: 25–54

    Google Scholar 

  • Hatch WI (1980) The implication of carbonic anhydrase in the physiological mechanisms of penetration of carbonate substrate by the marine burrowing sponge Cliona celata (Demospongiae). Biol Bull mar biol Lab, Woods, Hole 59: 135–147

    Google Scholar 

  • Herrera-Duvault Y, Roux M (1986) Modalités et vitesse de dissolution de la coquille des modioles du site hydrothermal de 13°N sur la dorsale du Pacifique oriental. Cr hebl Séanc Acad Sci, Paris 302: 251–256

    Google Scholar 

  • Hook JE, Golubic S (1993) Microbial shell destruction in deep-sea mussels, Florida Escarpment. Pubbl Staz zool Napolia (I: Mar Ecol) 14: 81–89

    Google Scholar 

  • Hutchings PA (1986) Biological destruction of coral reefs. A review. Coral Reefs 4: 239–252

    Google Scholar 

  • Johnson TW, Anderson WR (1962) A fungus in Amonia simplex shell. J Elisha Mitchell scient Soc 78: 42–47

    Google Scholar 

  • Kiene WE, Radtke G, Gektidis M, Golubic S, Vogël K (1995) Factors controlling the distribution of microborers in Bahamian reef environment. Facies 32: 176–184

    Google Scholar 

  • Kobluk DR, Risk MJ (1977) Rate and nature of infestation of a carbonate substratum by a boring alga Ostreobium sp. J exp mar Biol Ecol 27: 107–115

    Google Scholar 

  • Kohlmeyer J (1969) The role of marine fungi in the penetration of calcareous substances. Am Zool 9: 741–746

    Google Scholar 

  • Le Campion-Alsumard T (1970) Cyanophycées marines endolithes colonisant les surfaces rocheuses dénudées (Etages Supralittoral et Médiolittoral de la région de Marseille). Arch Hydrobiol (Suppl) 82: 552–558

    Google Scholar 

  • Le Campior-Alsumard T (1975) Etude expérimentale de la colonisation d'éclats de calcite par les cyanophycées endolithes marines. Cah Biol mar 16: 177–185

    Google Scholar 

  • Le Campion-Alsumard T, Golubic S (1985) Hyella caespitosa Bornet et Flahault and Hyella balani Lehman (Pleurocapsales, Cyanophyta): a comparative study. Arch Hydrobiol (Suppl) 71: 119–148

    Google Scholar 

  • Le Campion-Alsumard T, Golubic S, Hutchings PA (1995) Microbial endoliths in skeletons of live and dead corals: Porites lobata (Moorea, French Polynesia). Mar Ecol Prog Ser 117: 149–157

    Google Scholar 

  • McCloskey LR (1970) The dynamic of community associated with a scleractinian coral marine. Int Rev ges Hydrobiol Hydrogr 55: 13–81

    Google Scholar 

  • Nakahara H, Bevelander G (1971) The formation and growth of the prismatic layer of Pinctada radiata. Calcif Tissue Res 7: 31–45

    Google Scholar 

  • Neumann AC (1966) Observations on coastal erosion in Bermuda and measurements of the boring rate of the sponge, Cliona lampa. Limnol Oceanogr 11: 92–108

    Google Scholar 

  • Nielsen R (1972) A study of the shell-boring marine algae around the Danish Island Laeso. Bot Tidsskr 67: 245–269

    Google Scholar 

  • Nielsen R (1987) Marine algae within calcareous shell from New Zealand. NZ JL Bot 25: 425–438

    Google Scholar 

  • Philippon J, Plaziat J (1975) Rôles respectifs de la corrosion et des cryptogames perforantes dans la destruction des coquilles de mollusques des mangroves. Conséquences sur la fossilisation. Cr hebd Séanc Acad Sci, Paris 281: 617–620

    Google Scholar 

  • Pomponi SA (1980) Cytological mechanisms of calcium carbonate excavation by boring sponges. Int Rev Cytol 65: 301–319

    Google Scholar 

  • Poulicek MF, Jaspar-Versali MF, Goffinet G (1981) Etude expérimentale de la dégradation des coquilles de mollusques an niveau des sédiments marins. Bull Soc r Sci Liège 11–12: 513–518

    Google Scholar 

  • Raghukumar C, Pathak S, Chandramohan D (1988) Biodegradation of calcareous shells of the window pane oyster by shell-boring cyanobacteria. In: Thompson MF, Sarojini R, Nagabhushanam R (eds) Marine biodeterioration. Oxford IBH New Delhi, pp 692–701

    Google Scholar 

  • Rützler K, Rieger G (1973) Sponge burrowing: fine structure of Cliona lampa penetrating calcareous substrata. Mar Biol 21: 144–162

    Google Scholar 

  • Smyth MJ (1990) Incidence of boring organisms in gastropod shells on reefs around Guam. Bull mar Sci 46: 432–449

    Google Scholar 

  • Thangavelu R, Sanjeevaraj PJ (1988) Boring and fouling organisms of the edible oyster Crassostrea madrasensis (Preston) from the Pulicat lake, South India. J mar biol Ass India 30: 47–53

    Google Scholar 

  • Thivy F (1943) New records of some marine Chaetophoraceae and Chaetosphaeridiacea for North America. Biol Bull mar biol Lab, Woods Hole 85: 244–264

    Google Scholar 

  • Thomas PA (1979) Boring sponges destructive to economically important molluscan beds and coral reefs in Indian seas. Indian J Fish 26: 163–200

    Google Scholar 

  • Velayudhan TS (1983) On the occurrence of shell boring polychaetes and sponges on pearl oyster Pinctada fucata and control of boring organisms. Symp Ser mar biol Ass India 2: 614–618

    Google Scholar 

  • Wada K (1961) Crystal growth of molluscan shells. Bull natn Pearl Res Lab 36: 703–869

    Google Scholar 

  • Warburton FE (1958a) Control of the boring sponge on oyster beds. Prog Rep Atlant Cst Stns 69: 7–11

    Google Scholar 

  • Warburton FE (1958b) The manner in which the sponge Cliona bores in calcareous objects. Can J Zool 36: 555–562

    Google Scholar 

  • Weibel ER, Kistler GS, Scherle WF (1966) Practical stereological methods for morphometric cytology. J Cell Biol 30: 23–38

    Google Scholar 

  • Wilkinson M (1974) Investigations on the autoecology of Eugomontia sacculata Kornm., a shell-boring alga. J exp mar Biol Ecol 16: 19–27

    Google Scholar 

  • Wilkinson M, Burrows EM (1972) The distribution of marine shellboring green algae. J mar biol Ass UK 52: 59–65

    Google Scholar 

Download references

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Authors and Affiliations

  1. Laboratorire d'Ecologie Marine, Université Française du Pacifique, Faaa Aéroport, BP 6570, Papeete, Tahiti, French Polynesia, France

    L. Mao Che

  2. Etablissement pour la Valorisation des Activités Aquacoles et Maritimes (EVAAM), BP 20, Papeete, Tahiti, French Polynesia, France

    L. Mao Che & C. Payri

  3. Centre d'Océanologie de Marseille, Université de la Méditerranée, URA CNRS 41, Rue de la Batterie des Lions, F-13007, Marseille, France

    T. Le Campion-Alsumard, N. Boury-Esnault & C. Bézac

  4. Department of Biology, Boston University, 2 Cummington Street, 02215, Boston, Massachusetts, USA

    S. Golubic

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  1. L. Mao Che
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  2. T. Le Campion-Alsumard
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  3. N. Boury-Esnault
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  4. C. Payri
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  5. S. Golubic
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  6. C. Bézac
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Communicated by A. Rodríguez, Puerto Real

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Mao Che, L., Le Campion-Alsumard, T., Boury-Esnault, N. et al. Biodegradation of shells of the black pearl oyster, Pinctada margaritifera var. cumingii, by microborers and sponges of French Polynesia. Marine Biology 126, 509–519 (1996). https://doi.org/10.1007/BF00354633

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  • DOI: https://doi.org/10.1007/BF00354633

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