Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-29T08:54:07.929Z Has data issue: false hasContentIssue false

An improbable opportunistic predator: the functional morphology of Pinna nobilis (Bivalvia: Pterioida: Pinnidae)

Published online by Cambridge University Press:  23 April 2018

Brian Morton*
Affiliation:
School of Biological Sciences, The University of Hong Kong, Hong Kong SAR, China
Sanja Puljas
Affiliation:
Department of Biology, Faculty of Science, University of Split, Ruđera Boškovića 33, Split, Croatia
*
Correspondence should be addressed to: Brian Morton School of Biological Sciences, The University of Hong Kong, Hong Kong SAR, China email: [email protected]

Abstract

The functional morphology of Pinna nobilis is described, with special reference to the uniquely pinnid pallial organ, the similarly unique buccal (formerly pallial) gland, the stomach and its contents. The pallial gland produces sulphuric acid which as well as functioning as a shell cleaning swab may be involved in prey capture. The buccal gland discharging into the oesophagus has proteolytic digestive functions while the stomach is adapted for the reception and digestion of captured, mucous-bound, mesozooplanktonic and epi- and endo-benthic, prey items. Pinna nobilis is thus not simply either an accidental or incidental predator of such species but is opportunistic. The buccal glands and stomachs of other Pinnidae are not so specialized as in P. nobilis, possibly indicating that in the particular, oligotrophic, environment of the Mediterranean and Adriatic Seas, and in which it is endemic, P. nobilis has, in addition to being a typical ctenidial suspension feeder, become an opportunistic predator. Although the deep sea representatives of the Septibranchia (Anomalodesmata) and Propeamussidae are obligate predators, this is the first record of any bivalve functioning as an opportunistic predator with unique morphological adaptations to facilitate this.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 2018 

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

Allen, J.A. (2011) On the functional morphology of Pinna and Atrina larvae (Bivalvia: Pinnidae) from the Atlantic. Journal of the Marine Biological Association of the United Kingdom 91, 823829.Google Scholar
André, C., Jonsson, P.R. and Lindegarth, M. (1993) Predation on settling bivalve larvae by benthic suspension feeders: the role of hydrodynamics and larval behaviour. Marine Ecology Progress Series 97, 183192.Google Scholar
Ashelby, C.W., De Grave, S. and Johnson, M.L. (2015) Preliminary observations on the mandibles of palaemonoid shrimp (Crustacea: Decapoda: Caridea: Palaemonoidea). PeerJ 3, e846.Google Scholar
Atkins, D. (1938) On the ciliary mechanisms and interrelationships of lamellibranchs. Part VII. Laterofrontal cilia of the gill filaments and their phylogenetic value. Quarterly Journal of Microscopical Science 80, 346430.Google Scholar
Castellani, C. and Edwards, M. (2017) Marine plankton. A practical guide to ecology, methodology and taxonomy. Oxford: Oxford University Press.Google Scholar
Ćosović, V., Zavodnik, D., Borčić, A., Vidović, J., Deak, S. and Moro, A. (2011) A checklist of Foraminifera of the Eastern Shelf of the Adriatic Sea. Zootaxa 3035, 156.Google Scholar
Cox, L.R. and Hertlein, L.G. (1969) Superfamily Pinnacea Leach, 1819. In Moore, R.C. (ed.) Treatise on invertebrate paleontology. Part N, Mollusca 6, Bivalvia 1 (of 3). Lawrence, KS: Geological Society of America Inc. and University of Kansas Press, pp. N281N285.Google Scholar
Davenport, J., Ezgeta-Balić, D., Peharda, M., Skejić, S., Nincevi, Z., Ninčević-Gladan, Z. and Matijević, S. (2011) Size-differential feeding in Pinna nobilis L. (Mollusca: Bivalvia): exploitation of detritus, phytoplankton and zooplankton. Estuarine, Coastal and Shelf Science 92, 246254.Google Scholar
Davenport, J., Smith, R.J.J.W. and Packer, M. (2000) Mussels Mytilus edulis: significant consumers and destroyers of mesozooplankton. Marine Ecology Progress Series 198, 131137.Google Scholar
Decraemer, W., Gourbault, N. and Helléouet, M.-N. (2001) Cosmopolitanism among nematodes: examples from Epsilonematidae. Vie et Milieu 51, 1119.Google Scholar
Defossez, J.-M. and Hawkins, A.J.S. (1997) Selective feeding in shellfish: size-dependent rejection of large particles within pseudofaeces from Mytilus edulis, Ruditapes philippinarum and Tapes decussatus. Marine Biology 129, 139147.Google Scholar
Durrieu de Madron, X., Guieu, C., Sempéré, R., Conan, P., Cossa, D., D'Ortenzio, F., Estournel, C., Gazeau, F., Rabouille, C., Stemmann, L., Bonnet, S., Diaz, F., Koubbi, P., Radakovitch, O., Babin, M., Baklouti, M., Bancon-Montigny, C., Belviso, S., Bensoussan, N., Bonsang, B., Bouloubassi, I., Brunet, C., Cadiou, J.-F., Carlotti, F., Chami, M., Charmasson, S., Charrière, B., Dachs, J., Doxaran, D., Dutay, J.-C., Elbaz-Poulichet, F, Eléaume, M., Eyrolles, F., Fernandez, C., Fowler, S., Francour, P., Gaertner, J.C., Galzin, R., Gasparini, S., Ghiglione, J.-F., Gonzalez, J.-L., Goyet, C., Guidi, L., Guizien, K., Heimbürger, L.-E., Jacquet, S.H.M., Jeffrey, W.H., Joux, F., Le Hir, P., Leblanc, K., Lefèvre, D., Lejeusne, C., Lemé, R., Loÿe-Pilot, M.-D., Mallet, M., Méjanelle, L., Mélin, F., Mellon, C., Mérigot, B., Merle, P.-L., Migon, C., Miller, W.L., Mortier, L., Mostajir, B., Mousseau, L., Moutin, T., Para, J., Pérez, T., Petrenko, A., Poggiale, J.-C., Prieur, L., Pujo-Pay, M., Pulido-Villena, P., Raimbault, A.P., Rees, C., Ridame, J.-F., Rontani, D., Ruiz Pino, M.A., Sicre, V., Taillandier, C., Tamburini, T., Tanaka, I., Taupier-Letage, M, Tedetti, P., Testor, H., Thébault, B., Thouvenin, F., Touratier, J., Tronczynski, C., Ulses, F., Van Wambeke, V., Vantrepotte, S. and Vaz, R. (2011) Marine ecosystems’ responses to climatic and anthropogenic forcings in the Mediterranean. Progress in Oceanography 91, 97166.Google Scholar
Gilmour, T.H.J (1964) The structure, ciliation and function of the lip-apparatus of Lima and Pecten (Lamellibranchia). Journal of the Marine Biological Association of the United Kingdom 44, 485498.Google Scholar
Graham, A. (1988) Molluscs: prosobranch and pyramidellid gastropods. Leiden: E.J. Brill/Dr W. Backhuys.Google Scholar
Grave, B.H. (1911) Anatomy and physiology of the wing-shell, Atrina rigida. Bulletin of the Bureau of Fisheries 29, 409439 + plates XLVIII-L.Google Scholar
Hayward, P.J. and Ryland, J.S. (1990) The marine fauna of the British Isles and North-West Europe: 1. Introduction and protozoans to arthropods. Oxford: Clarendon Press.Google Scholar
Huys, R. (2001) Copepoda – Harpacticoida. In Costello, M.J., Emblow, C.S. and White, R. (eds) European register of marine species: a check-list of the marine species in Europe and a bibliography of guides to their identification. Collection Patrimoines Naturels, pp. 268280.Google Scholar
Katsanevakis, S. (2006) Population ecology of the endangered fan mussel Pinna nobilis in a marine lake. Endangered Species Research 1, 5159.Google Scholar
Katsares, V., Tsiora, A., Galinou-Mitsoudi, S. and Imsiridou, A. (2008) Genetic structure of the endangered species Pinna nobilis (Mollusca: Bivalvia) inferred from mtDNA sequences. Biologia 63, 412417.Google Scholar
Kennedy, H., Richardson, C.A., Duarte, C.M. and Kennedy, D.P. (2001) Diet and association of Pontonia pinnophylax occurring in Pinna nobilis: insights from stable isotope analysis. Journal of the Marine Biological Association of the United Kingdom 81, 177178.Google Scholar
Kršinić, F. (2007) Zooplankton population structure in the lower reach of the Krka estuary. In Marguš, D. (ed.) Simpozij rijeka Krka i Nacionalni park Krka. Šibenik: Prirodna i kulturna baština, zaštita i održivi razvitak, pp. 469480. [In Croatian]Google Scholar
Kršinić, F. (2010) Tintinnids (Tintinnida, Choreotrichia, Ciliata) in the Adriatic Sea, Mediterranean. Part I. Taxonomy. Split, Croatia: Institute of Oceanography and Fisheries, 186 pp.Google Scholar
Lehane, C. and Davenport, J. (2002) Ingestion of mesozooplankton by three species of bivalve; Mytilus edulis, Cerastoderma edule and Aequipecten opercularis. Journal of the Marine Biological Association of the United Kingdom 82, 615619.Google Scholar
Lemer, S., Buge, B., Bemis, A. and Giribet, G. (2014) First molecular phylogeny of the circumtropical family Pinnidae (Mollusca: Bivalvia): evidence for high levels of cryptic species diversity. Molecular Phylogenetics and Evolution 75, 1123.Google Scholar
Lemer, S., Combosch, D., Sotto, F., Giribet, G. and Dumale, D. (2016) The family Pinnidae (Bivalvia) in the Philippine archipelago: observations on its distribution and phylogeography. The Nautilus 130, 137145.Google Scholar
Liang, X.Y and Morton, B. (1988) The pallial organ of Atrina pectinata (Bivalvia: Pinnidae): its structure and function. Journal of Zoology, London 216, 469.Google Scholar
Machado, F.M., Morton, B. and Passos, F.D. (2017) Functional morphology of Cardiomya cleryana (d'Orbigny, 1842) (Bivalvia: Anomalodesmata: Cuspidariidae) from Brazilian waters: new insights into the lifestyle of carnivorous bivalves. Journal of the Marine Biological Association of the United Kingdom 97, 447462.Google Scholar
Maeder, F. (2002) The project sea-silk – rediscovering an ancient textile material. Archaeological Textiles Newsletter 35, 811.Google Scholar
Mikulich, L.V. and Tsikhno-Lukanina, Y.A. (1981) Food of the scallop. Oceanology 21, 633635.Google Scholar
Morton, B. (1995) The evolutionary history of the Bivalvia. In Taylor, J.D. (ed.) The origin and evolutionary radiation of the Mollusca. Oxford: Oxford University Press, pp. 337359.Google Scholar
Morton, B. (2016) The biology and functional morphology of the predatory septibranch Cardiomya costellata (Bivalvia: Anomalodesmata: Cuspidariidae) from the Mid-Atlantic Ridge at the Açores. Survival at the edge. Journal of the Marine Biological Association of the United Kingdom 96, 13471361.Google Scholar
Morton, B., Machado, F.M. and Passos, F.D. (2015) The smallest carnivorous bivalve? Biology, morphology and behaviour of Grippina coronata (Anomalodesmata: Cuspidarioidea: Spheniopsidae) preying on epipsammic micro-crustaceans in the southwestern Atlantic off Brazil. Journal of Molluscan Studies 82, 244258.Google Scholar
Morton, B., Machado, F.M. and Passos, F.D. (2016) The organs of prey capture and digestion in the miniature predatory bivalve Spheniopsis brasiliensis (Anomalodesmata: Cuspidarioidea: Spheniopsidae) expose a novel life history trait. Journal of Natural History 50, 17251748.Google Scholar
Morton, B., Peharda, M. and Petrić, M. (2011) Functional morphology of Rocellaria dubia (Bivalvia: Gastrochaenidae) with new interpretations of crypt formation and adventitious tube construction, and a discussion of evolution within the family. Biological Journal of the Linnean Society 104, 786804.Google Scholar
Morton, B. and Thurston, M.H. (1989) The functional morphology of Propeamussium lucidum (Bivalvia: Pectinacea), a deep sea predatory scallop. Journal of Zoology, London 218, 471496.Google Scholar
Musco, L. and Giangrande, A. (2005) Mediterranean Syllidae (Annelida: Polychaeta) revisited: biogeography, diversity and species fidelity to environmental features. Marine Ecology Progress Series 304, 143153.Google Scholar
Ockelmann, K.W. and Dinesen, G.E. (2011) Life on wood – the carnivorous deep-sea mussel Idas argenteus (Bathymodiolinae, Mytilidae, Bivalvia). Marine Biology Research 7, 7184.Google Scholar
Palaz, M. and Selcuk, B. (2005) The bivalve species of the Dardanelles. Journal of the Marine Biological Association of the United Kingdom 85, 357358.Google Scholar
Pelseneer, P. (1911) Les lamellibranches de l’ expédition du Siboga. Partie anatomique. Siboga Expedetion Monograph 53a, 1125.Google Scholar
Pešić, V., Sezgin, M., Karaçuha, M.E. and Ürkmez, D. (2013) New records of marine water mites (Acari: Hydrachnidia, Pontarachnidae) from the southern Black Sea (Sinop Bay, Turkey). Mediterranean Marine Science 14, 4547.Google Scholar
Poppe, G.T. and Goto, Y. (1993) European seashells. Volume 2 (Scaphopoda, Bivalvia, Cephalopoda). Wiesbaden: Verlag Christa Hemmen.Google Scholar
Purchon, R.D. (1957) The stomach in the Filibranchia and Pseudolamellibranchia. Proceedings of the Zoological Society of London 129, 2760.Google Scholar
Ridewood, W.G. (1903) On the structure of the gill of the Lamellibranchia. Philosophical Transactions of the Royal Society, Series B 195, 147284.Google Scholar
Shumway, S.E., Selvin, R. and Schick, D.F. (1987) Food resources related to habitat in the scallop Placopecten magellanicus (Gmelin 1791): a qualitative study. Journal of Shellfish Research 6, 8995.Google Scholar
Šiletić, T. (2006) Marine fauna of Mljet National Park (Adriatic Sea, Croatia). 5. Mollusca: Bivalvia. Natura Croatica 15, 109169.Google Scholar
Šiletić, T. and Peharda, M. (2003) Population study of the fan shell Pinna nobilis L. in Malo and Veliko Jezero of the Mljet National Park (Adriatic Sea). Scientia Marina 67, 9198.Google Scholar
Siokou, I., Ates, A.S., Ayas, D., Ben Souissi, J., Chatterjee, T., Dimiza, M., Durgham, H., Dogrammatzi, K., Erguden, D., Gerakaris, V., Grego, M., Issaris, Y., Kadis, K., Katagan, T., Kapiris, K., Katsanevakis, S., Kerckhof, F., Papastergiadou, E., Pesic, V., Polychronidis, L., Rifi, M., Salomidi, M., Sezgin, M., Triantaphyllou, M., Tsiamis, K., Turan, C., Tziortzis, I., D'Udekem D'Acoz, C., Yaglioglu, D., Zaouali, J. and Zenetos, A. (2013) New Mediterranean marine biodiversity records (June 2013). Mediterranean Marine Science 14, 238249.Google Scholar
Stasek, C.R. (1963) Synopsis and discussion of the association of ctenidia and labial palps in the bivalved Mollusca. The Veliger 6, 9197.Google Scholar
Stenta, M. (1906) Über ein drüsiges, organ der Pinna. Arbeiten aus des Zoologischen Instituten der Universität Wien 16, 407436.Google Scholar
Theodorou, J.A., James, R., Tagalis, D., Τzοvenis, I., Hellio, C. and Katselis, G. (2017) Density and size structure of the endangered fan mussel Pinna nobilis (Linnaeus 1758), in the shallow water zone of Maliakos Gulf, Greece. Acta Adriatica 58, 6376.Google Scholar
Thompson, T.E. (1983) Detection of epithelial acid secretions in marine molluscs: a review of techniques and new analytical methods. Comparative Biochemistry and Physiology (A) 74, 615621.Google Scholar
Thubaut, J., Corbari, L., Gros, O., Duperron, S., Couloux, A. and Samadi, S. (2013) Integrative biology of Idas iwaotakii (Habe, 1958), a ‘model species’ associated with sunken organic substrates. PLoS ONE 8, e69680.Google Scholar
Travizi, A. and Vidaković, J. (1997) Nematofauna in the Adriatic Sea: review and check-list of free-living nematode species. Helgolander Meeresuntersuchungen 51, 503519.Google Scholar
Vidjak, O., Bojanić, N., Kušpilić, G., Grbec, B., Ninčević Gladan, Ž., Matijević, S. and Brautović, I. (2009) Population structure and abundance of zooplankton along the Krka River estuary in spring 2006. Acta Adriatica 50, 4558.Google Scholar
Vidjak, O., Bojanić, N., Kušpilić, G., Grbec, B., Ninčević Gladan, Ž. and Tičina, V. (2007) Zooplankton community and hydrographical properties of the Neretva Channel (eastern Adriatic Sea). Helgoland Marine Research 61, 267282.Google Scholar
Vidjak, O., Bojanić, N., Kušpilić, G., Marasović, I., Ninčević Gladan, Ž. and Brautović, I. (2006) Annual variability and trophic relations of the mesozooplankton community in the eutrophicated coastal area (Vranjic Basin, eastern Adriatic Sea). Journal of the Marine Biological Association of the United Kingdom 86, 1926.Google Scholar
Viličić, D. (2014) Specifična oceanološka svojstva Hrvatskog dijela Jadrana. Hrvatske Vode 22, 297314. [In Croatian]Google Scholar
White, K.M. (1937) Mytilus. In L.M.B.C. Memoirs on typical British marine plants and animals. Volume 31. Liverpool: The University Press of Liverpool, pp. 1117 +plates 1–10.Google Scholar
White, K.M. (1942) The pericardial cavity and the pericardial gland of the Lamellibranchia. Proceedings of the Malacological Society of London 25, 3788.Google Scholar
Yonge, C.M. (1953) Form and habit in Pinna carnea Gmelin. Philosophical Transactions of the Royal Society Series B 237, 335374.Google Scholar
Zavodnik, D. (1967) Contribution to the ecology of Pinna nobilis L. (Mollusca, Bivalvia) in the Northern Adriatic Sea. Thalassia Yugoslavica 3, 93103.Google Scholar
Zavodnik, D., Hrs-Brenko, M. and Legac, M. (1991) Synopsis on the fan shell Pinna nobilis L. in the eastern Adriatic Sea. In Boudouresque, C.F., Avon, M. and Gravez, V. (eds) Les Espèces Marines à Protéger en Méditerranée. Marseille: Gis Posidonie Publication, pp. 169178.Google Scholar