Pinna nobilis in the south Marmara Islands (Sea of Marmara); it still remains uninfected by the epidemic and acts as egg laying substratum for an alien invader

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Published: Mar 3, 2021
DOI: https://doi.org/10.12681/mms.25289
Keywords:
Fan mussel healthy individuals critically endangered species associated biota Sea of Marmara Haplosporidium pinnae.
MELIH ERTAN CINAR
1Ege University, Faculty of Fisheries, Department of Hydrobiology, 35100, Bornova, İzmir, Turke
https://orcid.org/0000-0002-1802-2801
MURAT BİLECENOĞLU
Aydın Adnan Menderes University, Science and Art Faculty, Department of Biology, Aydin, Turkey
https://orcid.org/0000-0001-5111-4997
MEHMET BAKI YOKEŞ
AMBRD Doğa Bilimleri, Hanımefendi Sokak 160/6 34384 Şişli, İstanbul, Turkey
https://orcid.org/0000-0002-9440-4561
HARUN GÜÇLÜSOY
Dokuz Eylül University, Institute of Marine Sciences and Technology, 35330, İnciraltı, İzmir, Turkey
https://orcid.org/0000-0002-4147-2587
Abstract

A total of 12 Pinna nobilis beds were found and studied at depths varying between 2 and 6 m in the south Marmara Islands (Sea of Marmara). Fan mussel individuals in the beds were healthy with a few old dead specimens, indicating that the epidemic, which has devastated P. nobilis populations in the Mediterranean Sea, has not reached the Sea of Marmara, making the region a refuge area for the species. The average density of P. nobilis in the area varied between 0.6 ind.10 m-2 and 24 ind.10 m-2. The P. nobilis shells overall provided substrata or refuge for 14 species (10 sessile and 4 motile organisms), from macroalgae to fish. Shells of juvenile and adult specimens had different species assemblages. Four distinct assemblages were detected on shells, primarily formed by the red alga Gracilaria bursa-postaris, egg cocoons of the invasive alien Rapana venosa, the gastropod Bittium reticulatum and the serpulid polychaete Spirobranchus polytrema.

 

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References
Acarli, S., Vural, P., Öktener, A., 2019. Association between the crab, Nepinnotheres pinnotheres (Linnaeus, 1758), and the endangered species fan mussel, Pinna nobilis (Linnaeus, 1758), from the Aegean Sea, Turkey. Alinteri Journal of Agriculture Science, 34, 169-174. A
carli, S., Lok, A., Yigitkurt, S., Palaz, M., 2011. Culture of fan mussel (Pinna nobilis, Linnaeus 1758) in relation to size on suspended culture system in Izmir Bay, Aegean Sea, Turkey. Kafkas Universitesi Veteriner Fakültesi Dergisi, 17 (6), 995-1002.
Acarli, S., Lok, A., Acarli, D., Kirtik, A., 2018. Reproductive cycle and biochemical composition in the adductor muscle of the endangered species fan mussel Pinna nobilis, Linnaeus 1758 from the Aegean sea, Turkey. Fresenius Environmental Bulletin, 27, 6506-6518.
Addis, P., Secci, M., Brundu, G., Manunza, A., Corrias, S. et al., 2009. Density, size structure, shell orientation and epibiontic colonization of the fan mussel Pinna nobilis L. 1758 (Mollusca: Bivalvia) in three contrasting habitats in an estuarine area of Sardinia (W Mediterranean). Scientia Marina, 73, 143-152.
Banach-Esteve, G., Vázquez Luis, M., Company, S.D., 2015. Temporal trends in sessile epibionts of the endemic bivalve Pinna nobilis variability in Lophocladia lallemandii colonization. Thalassas: An International Journal of Marine Sciences, 31, 19-29.
Becker, C., Türkay, M., 2017. Host specificity and feeding in European pea crabs (Brachyura, Pinnotheridae). Crustaceana, 90, 819-844.
Bray, J.R., Curtis, J.T., 1957. An ordination of upland forest communities of southern Wisconsin. Ecological Monographs, 27, 325-349.
Butler, A., Vicente, N., De Gaulejac, B., 1993. Ecology of de pterioid bivalves Pinna bicolor Gmelin and Pinna nobilis L. Life, 3, 37-45.
Cabanellas-Reboredo, M., Blanco, A., Deudero, S., Tejada, S., 2010. Effects of the invasive macroalga Lophocladia lallemandii on the diet and trophism of Pinna nobilis (Mollusca: Bivalvia) and its guests Pontonia pinnophylax and Nepinnotheres pinnotheres (Crustacea: Decapoda). Scientia Marina, 74, 101-110.
Cabanellas-Reboredo, M., Vázquez-Luis, M., Mourre, B., Álvarez, E., Deudero, S. et al., 2019. Tracking a mass mortality outbreak of pen shell Pinna nobilis populations: A collaborative effort of scientists and citizens. Scientific Reports, 9, 13355.
Carella, F., Antuofermo, E., Farina, S., Salati, F., Mandas, D. et al., 2020. In the wake of the ongoing mass mortality events: co-occurrence of Mycobacterium, Haplosporidium and other pathogens in Pinna nobilis collected in Italy and Spain (Mediterranean Sea). Frontiers in Marine Science, 7, 48.
Catanese, G., Grau, A., Valencia, J. M., Garcia-March, J. R., Vázquez-Luis, M. et al., 2018. Haplosporidium pinnae sp. nov., a haplosporidan parasite associated with mass mortalities of the fan mussel, Pinna nobilis, in the Western Mediterranean Sea. Journal of Invertebrate Pathology, 157, 9-24.
Çinar, M.E., 2003. Ecological features of Syllidae (Polychaeta) from shallow-water benthic environments of the Aegean Sea, eastern Mediterranean. Journal of the Marine Biological Associations of the United Kingdom, 83, 737-745.
Çinar, M.E., 2006. Serpulid species (Polychaeta: Serpulidae) from the Levantine coast of Turkey (eastern Mediterranean), with special emphasis on alien species. Aquatic Invasions, 1, 223-240.
Çinar, M.E., Ergen, Z., 2001. On the ecology of the Nereididae (Polychaeta: Annelida) in the Bay of İzmir, Aegean Sea. Zoology in the Middle East, 22, 113-122.
Çinar, M.E., Dağli, E., Çağlar, S., Albayrak, S., 2015. Polychaetes from the northern part of the Sea of Marmara with the description of a new species of Polydora (Annelida: Polychaeta: Spionidae). Mediterranean Marine Science, 16 (3), 524-532.
Çinar, M.E., Bakir, K., Öztürk, B., Doğan, A., Açık, Ş. et al., 2020. Spatial distribution pattern of macroinvertebrates associated with the black mussel Mytilus galloprovincialis (Mollusca: Bivalvia) in the Sea of Marmara. Journal of Marine Systems, 211, 103402.
Čižmek, H., Čolic, B., Gračan, R., Grau, A., Catanese, G., 2020. An emergency situation for pen shells in the Mediterranean: The Adriatic Sea, one of the last Pinna nobilis shelters, is now affected by a mass mortality event. Journal of Invertebrate Pathology, 173, 107388.
Coppa, S., Guala, I., de Lucia, G.A., Massaro, G., Bressan, M., 2010. Density and distribution patterns of the endangered species Pinna nobilis within a Posidonia oceanica meadow in the Gulf of Oristano (Italy). Journal of the Marine Biological Associations of the United Kingdom, 90, 885-894.
Cosentino, A., Giacobbe, S., 2007. Aspects of epizoobiontic mollusc assemblages on Pinna shells. I. composition and structure. Cahiers de Biologie Marine, 48, 187-197.
Demirci, A., Acarli, S., 2019. Estimation growth parameters of endangered the fan mussel species (Pinna nobilis L.) by using different growth models from Izmir Bay, Aegean Sea, Turkey. Fresenius Environmental Bulletin, 28, 7368-7374.
Forsskål, P., 1775. Descriptiones animalium avium, amphibiorum, piscium, insectorum, vermium; quae in itinere orientali observavit Petrus Forskal. Post mortem auctoris edidit Carsten Niebuhr Adjuncta est materia medica Kahirina atqus tabula maris rubri geographica. Copenhagen, 164 p.
Geldiay, R., Kocataş, A., 1972. İzmir Körfezi‘nin bentosu üzerine preliminer bir araştırma. Ege Universitesi Fen Fakültesi Monograflar Serisi, 12, 1-34.
Gönülal, O., Güreşen, S.O., 2014. A list of macrofauna on the continental shelf of Gökçeada Island (northern Aegean Sea) with a new record (Gryphus vitreus Born, 1778) (Brachiopoda, Rhynchonellata) for the Turkish seas. Journal of Black Sea/Mediterranean Environment, 20, 228-252.
Hendriks, I.E., Tenan, S., Tavecchia, G., Marbà, N., Jordà, G. et al., 2013. Boat anchoring impacts coastal populations of the pen shell, the largest bivalve in the Mediterranean. Biological Conservation, 160, 105-113.
Katsanevakis, S., 2006. Population ecology of the endangered fan mussel Pinna nobilis in a marine lake. Endangered Species Research, 1, 1-9.
Katsanevakis, S., Thessalou-Legaki, M., 2009. Spatial distribution, abundance and habitat use of the protected fan mussel Pinna nobilis in Souda Bay, Crete. Aquatic Biology, 8, 45-54.
Katsanevakis, S., Tsirintanis, K., Tsaparis, D., Doukas, D., Sini, M. et al., 2019. The cryptogenic parasite Haplosporidium pinnae invades the Aegean Sea and causes the collapse of Pinna nobilis populations. Aquatic Invasions, 14, 150–164.
Kersting, D.K., García-March, J.R., 2017. Long-term assessment of recruitment, early stages and population dynamics of the endangered Mediterranean fan mussel Pinna nobilis in the Columbretes Islands (NW Mediterranean). Marine Environmental Research, 130, 282-292.
Kersting, D., Benabdi, M., Čižmek, H., Grau, A., Jimenez, C. et al., 2019. Pinna nobilis. The IUCN Red List of Threatened Species 2019: e.T160075998A160081499.
Kersting, D.K., Vázquez-Luis, M., Mourre, B., Belkhamssa, F.Z., Álvarez, E. et al., 2020. Recruitment disruption and the role of unaffected populations for potential recovery after the Pinna nobilis mass mortality event. Frontiers in Marine Science, 7, 594378.
Lattos, A., Giantsis, I.A., Karagiannis, D., Michaelidis, B., 2020. First detection of the invasive haplosporidian and mycobacteria parasites hosting the endangered bivalve Pinna nobilis in Thermaikos Gulf, North Greece. Marine Environmental Research, 155, 104889.
Marion, A.F., 1898. Notes sur la faune des Dardanelles et du Bosphore. Annales du Musée d̓’Histoire Naturelle de Marseille. Série II. Bulletin notes zoologiques, géologiques, paléontologiques, 1, 163-182.
Okuş, E., Yüksek, A., Noyan Yılmaz, I., Aslan Yılmaz, A., Karhan, S.Ü. et al., 2007. Marine Biodiversity of Datça-Bozburun Specially Protected Area (Southeastern Aegean Sea, Turkey). Journal of Black Sea/Mediterranean Environment, 13, 7-17.
Öndes, F., Kaiser, M.J., Güçlüsoy, H., 2020a. Human impacts on the endangered fan mussel, Pinna nobilis. Aquatic Conservation: Marine Freshwater Ecosystems, 30, 31-41.
Öndes, F., Alan, V., Akçalı, B., Güçlüsoy, H., 2020b. Mass mortality of the fan mussel Pinna nobilis in Turkey (eastern Mediterranean). Marine Ecology, e12607.
Özalp, H.B., Kersting, D.K., 2020. A pan-Mediterranean extinction? Pinna nobilis mass mortality has reached the Turkish Straits System. Marine Biodiversity, 50, 81.
Özsoy, E., Altiok, H., 2016. A review of hydrography of the Turkish Straits System. In: Özsoy, E., Çağatay, M.N., Balkıs, N., Balkıs, N., Öztürk, B. (Eds.), The Sea of Marmara; Marine Biodiversity, Fisheries, Conservation and Governance. Turkish Marine Research Foundation (TUDAV), Publication No: 42, Istanbul, pp. 13-42.
Panarese, R., Tedesco, P., Chimienti, G., Latrofa, M.S., Quaglio, F. et al., 2019. Haplosporidium pinnae associated with mass mortality in endangered Pinna nobilis (Linnaeus 1758) fan mussels. Journal of Invertebrate Pathology, 164, 32-37.
Pergent, G., Pergent, C., 1985. Cartographie de l’herbier a Posidonia oceanica de la Baie d’Urla-Iskele (Turquie). Rapports et Procès-Verbaux des Internationale pour l’Exploration Scientifique de la Mer Méditerranée, 29, 6.
Plećaš, D., 2017. Epibionti na plemenitoj periski (Pinna nobilis Linnaeus, 1758; Mollusca: Bivalvia). MSc Thesis, University of Zagreb, Faculty of Science, 37 pp.
Rabaoui, L., Tlih-Zouari, Ben Hassine, O.K., 2008. Two species of Crustacea (Decapoda) associated with the fan mussel, Pinna nobilis Linnaeus, 1758 (Mollusca, Bivalvia). Crustaceana, 81, 433-446.
Rabaoui, L., Tlih-Zouari, S., Cosentino, A., Ben Hassine, O.K., 2009. Associated fauna of the fan shell Pinna nobilis (Mollusca: Bivalvia) in the northern and eastern Tunisian coasts. Scientia Marina, 73, 129-141.
Riley, K., Ballerstedt, S., 2005. Spirobranchus triqueter A tubeworm. In: Tyler-Walters H. and Hiscock K. (eds) Marine Life Information Network: Biology and Sensitivity Key Information Reviews, [on-line]. Plymouth: Marine Biological Associations of the United Kingdom. 1794.2.
Rouanet, E., Trigos, S., Vicenti, N., 2015. From youth to death of old age: the 50-year story of a Pinna nobilis fan mussel population at Port-Cros Island (Port-Cros National Park, Provence, Mediterranean Sea). Scientific reports of the Port-Cros national Park, 29, 209-222.
Šarić, T., Župan, I., Aceto, S., Villari, G., Palić, D. et al., 2020. Epidemiology of Noble Pen Shell (Pinna nobilis L. 1758) mass mortality events in Adriatic Sea Is characterised with rapid spreading and acute disease progression. Pathogens, 9, 776.
Scarpa, F., Sanna, D., Azzena, I., Mugetti, D., Cerruti, F. et al., 2020. Multiple non-species-specific pathogens possibly triggered the mass mortality in Pinna nobilis. Life, 10, 238.
Šiletić, T., 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, 91-98.
Torgerson, W.S., 1958. Theory and methods of scaling. New York: Wiley.
Trigos, S., García-March, J., Vicente, N., Tena, J., Torres, J., 2014. Utilization of muddy detritus as organic matter source by the fan mussel Pinna nobilis. Mediterrannean Marine Science, 15 (3), 667-674.
Trygonis, V., Sini, M., 2012. photoQuad: A dedicated seabed image processing software, and a comparative error analysis of four photoquadrat methods. Journal of Experimental Marine Biology and Ecology, 425, 99-108.
Tsatiris, A., Papadopoulos, V., Makri, D., Topouzelis, K., Manoutsoglou, E. et al., 2018. Spatial distribution, abundance and habitat use of the endemic Mediterranean fan mussel Pinna nobilis in the Gera Gulf, Lesvos (Greece): comparison of design- based and model-based approaches. Mediterranean Marine Science, 19 (3), 642-655.
Vafidis, D., Antoniadou, C., Voultsiadou, E., Chintiroglou, C., 2014. Population structure of the protected fan mussel Pinna nobilis in the south Aegean Sea (eastern Mediterranean). Journal of the Marine Biological Associations of the United Kingdom, 94, 787-796.
Vázquez-Luis, M., Álvarez, E., Barrajón, A., García-March, J.R., Grau, A. et al., 2017. S.O.S. Pinna nobilis: A mass mortality event in Western Mediterranean Sea. Frontiers in Marine Science, 4, 220.
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