The last hope: the struggle for survival of fan mussels in the Gulf of Erdek, Sea of Marmara, Turkey

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Publiée : Juni 20, 2022
DOI : https://doi.org/10.12681/mms.28474
UĞUR KARADURMUŞ
Bandırma Onyedi Eylül University, Maritime Vocational School, Department of Underwater Technology, 10200, Bandırma, Balıkesir, Turkey
https://orcid.org/0000-0002-5827-0404
MUSTAFA SARI
Bandırma Onyedi Eylül University, Faculty of Maritime, Department of Maritime Business Administration, 10200, Bandırma, Balıkesir, Turkey
https://orcid.org/0000-0003-2733-3254
Résumé

This study presents the results of the first broad-scale assessment of the spatial distribution of the fan mussel (Pinna nobilis Linnaeus, 1758) population in the Gulf of Erdek (Sea of Marmara, Turkey), based on underwater surveys. The population density and structure of mussels were estimated by diving along strip transects between the shoreline and a depth of 15.8 m, in a study area of 9080 km2. A total of 2164 mussels were counted, of which 78.8% were alive, and 21.2% were dead in 29 sites. The mean density was calculated as 18.3 ± 3.3 ind·100 m-2, and recorded densities reached 71.2 ind·100 m-2 among the studied sites. Although mussel density was very high (>15 ind·100 m-2) in nine sites, dead mussels were also recorded in the gulf. Benthic habitats, depth range, and exposure levels seem to play a crucial role in the spatial distribution and survival of fan mussels. The average height (± SE) was calculated as 19.5 ± 0.35 cm and 24.9 ± 0.37 cm for alive and dead mussels, respectively. The percentage of juveniles (≤20 cm) was 57% in the population, and they dominated in seagrass meadow beds and shallow waters. Despite many deaths due to uncertain causes, the results indicate a partially promising scenario for the fan mussel population in the Gulf of Erdek and highlight the existence of many alive juveniles that could play a primary role in the sustainability of the population. This situation is not static, as anthropogenic changes and human activities could affect population welfare in the future. These high-density sites need to be protected, and protection measures in these locations should include all effects that may cause incidental mortality.

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Références
Acarlı, S., Lök, A., Yiğitkurt, 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. Journal of the Faculty of Veterinary Medicine, Kafkas University, 17 (6), 995-1002.
Acarlı, S., Acarlı, D., Kale, S., 2021. Current status of critically endangered fan mussel Pinna nobilis (Linnaeus 1758) population in Çanakkale Strait, Turkey. Marine Science and Technology Bulletin, 10 (1), 62-70.
Basso, L., Vázquez-Luis, M., García-March, J.R., Deudero, S., Alvarez, E. et al., 2015. The pen shell, Pinna nobilis: A review of population status and recommended research priorities in the Mediterranean Sea. Advances in Marine Biology, 71, 109-160.
Butler, A., Vicente, N., Gaulejac, B., 1993. Ecology of the pterioid bivalves Pinna bicolor Gmelin and Pinna nobilis L. Marine Life, 3, 37-45.
Cabanellas-Reboredo, M., Vázquez-Luis, M., Mourre, B., Álvarez, E., Deudero, S. et al., 2019. Tracking the mass mortality outbreak of pen shell Pinna nobilis populations: a collaborative effort of scientists and citizens. Scientific Reports, 9, 13355.
Carella, F., Aceto, S., Pollaro, G., Micccio, A., Carrasco, N. et al., 2019. An emerging mycobacterial disease is associated with the silent mass mortality of the Pen shell Pinna nobilis along Tyrrhenian coastline of Italy. Scientific Reports, 9, 2725.
Catanese, G., Grau, A., Valencia, J.M., García-March, J.R., Vázquez-Luis, M. et al., 2018. Haplosporidium pinnae sp. nov., a haplosporidian parasite associated with mass mortalities of the fan mussel, Pinna nobilis in the Western Mediterranean Sea. Journal of Invertebrate Pathology, 157, 9-24.
Čelebičić, M., Gradaščević, N., Viteškić, V., 2020. Is Pinna nobilis l. critically endangered in Neum bay, Bosnia and Herzegovina? Veterinaria, 69 (3), 221-227.
Centoducati, G., Tarsitano, E., Bottalico, A., Marvulli, M., Lai, O.R. et al., 2007. Monitoring of the endangered Pinna nobilis Linné,1758 in the Mar Grande of Taranto (Ionian Sea, Italy). Environmental Monitoring and Assessment, 131, 339-347.
Čižmek, H., Čolić, 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., de Lucia, G.A., Magni, P., Domenici, P., Antognarelli, F. et al., 2013. The effect of hydrodynamics on shell orientation and population density of Pinna nobilis in the Gulf of Oristano (Sardinia, Italy). Journal of Sea Research, 76, 201-210.
Çınar, M., Bilecenoğlu, M., Yokeş, M., Güçlüsoy, H., 2021a. 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. Mediterranean Marine Science, 22 (1), 161-168.
Çınar, M., Bilecenoğlu, M., Yokeş, M., Güçlüsoy, H., 2021b. The last fortress fell: mass mortality of Pinna nobilis in the Sea of Marmara. Mediterranean Marine Science, 22 (3), 669-676.
Darriba, S., 2017. First haplosporidan parasite reported infecting a member of the Superfamily Pinnoidea (Pinna nobilis) during a mortality event in Alicante (Spain, Western Mediterranean). Journal of Invertebrate Pathology, 148, 14-19.
Davenport, J., Ezgeta-Balić, D., Peharda, M., Skejić, S., Ninčević-Gladan, Ž. et al., 2011. Size-differential feeding in Pinna nobilis L. (Mollusca: Bivalvia): exploitation of detritus, phytoplankton and zooplankton. Estuarine, Coastal and Shelf Science, 92 (2), 246-254.
Deudero, S., Vázquez-Luis, M., Álvarez, E., 2015. Human stressors are driving coastal benthic long-lived sessile fan mussel Pinna nobilis population structure more than environmental stressors. PLoS ONE, 10 (7), e0134530.
Duarte, C.M., Benavent, E., Sánchez, M.C., 1999. The microcosm of particles within seagrass (Posidonia oceanica) canopies. Marine Ecology Progress Series, 181, 289-295.
Galinou-Mitsoudi, S., Vlahavas, G., Papoutsi, O., 2006. Population study of the protected bivalve Pinna nobilis (Linnaeus, 1758) in Thermaikos Gulf (North Aegean Sea). Journal of Biological Research, 5, 47-53.
García-March, J.R., García-Carrascosa, A.M., Luís Peña, Á., 2002. In situ measurement of Pinna nobilis shells for age and growth studies: a new device. Marine Ecology, 23 (3), 207-217.
García-March, J.R., Kersting, D.K., 2006. Preliminary data on the distribution and density of Pinna nobilis and Pinna rudis in the Columbretes Islands Marine Reserve (Western Mediterranean, Spain). Organism Diversity and Evolution, 6, 6-16.
García-March, J.R., Pérez-Rojas, L., García-Carrascosa, A.M., 2007a. Influence of hydrodynamic forces on population structure of Pinna nobilis L., 1758 (Mollusca: Bivalvia): the critical combination of drag force, water depth, shell size and orientation. Journal of Experimental Marine Biology and Ecology, 342, 202-212.
García-March, J.R., García-Carrascosa, A.M., Peña Cantero, A.L., Wang, Y.G., 2007b. Population structure, mortality and growth of Pinna nobilis Linnaeus, 1758 (Mollusca, Bivalvia) at different depths in Moraira bay (Alicante, Western Mediterranean). Marine Biology, 150 (5), 861-871.
García-March, J.R., Tena, J., Henandis, S., Vázquez-Luis, M., López, D. et al., 2020. Can we save a marine species affected by a highly infective, highly lethal, waterborne disease from extinction?. Biological Conservation, 243, 108498.
Hastie, T.J., Tibshirani, R.J., 1990. Generalized additive models (monographs on statistics and applied probability). Chapman & Hall, London, 352 pp.
Hendriks, I.E., Cabanellas-Reboredo, M., Bouma, T.J., Deudero, S., Duarte, C.M., 2011. Seagrass meadows modify drag forces on the shell of the fan mussel Pinna nobilis. Estuaries and Coasts, 34, 60-67.
IUCN, 2021. International Union for Conservation of Nature: Habitats Classification Scheme (Version 3.1). https://www. iucnredlist.org/resources/habitat-classification-scheme (Accessed 15 September 2021).
Karadurmuş, U., Sarı, M., 2022. Marine mucilage in the Sea of Marmara and its effects on the marine ecosystem: mass deaths. Turkish Journal of Zoology, 46 (1), 93-102.
Katsanevakis, S., 2006. Population ecology of the endangered fan mussel Pinna nobilis in a marine lake. Endangered Species Research, 1, 51-59.
Katsanevakis, S., 2007. Growth and mortality rates of the fan mussel Pinna nobilis in Lake Vouliagmeni (Korinthiakos Gulf, Greece): a generalized additive modelling approach. Marine Biology, 152 (6), 1319-1331.
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., 2019. The cryptogenic parasite Haplosporidium pinnae invades the Aegean Sea and causes the collapse of Pinna nobilis populations. Aquatic Invasions, 14 (2), 150-164.
Katsanevakis, S., Carella, F., Çınar, M.E., Čižmek, H., Jimenez, C. et al., 2021. The fan mussel Pinna nobilis on the brink of extinction in the Mediterranean. Reference Module in Earth Systems and Environmental Sciences.
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. https://dx.doi.org/10.2305/IUCN.UK.2019-3.RLTS. T160075998A160081499.en. (Accessed 5 October 2021).
Kersting, D., 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.
Keskin, C., 2007. Temporal variation of fish assemblages in different shallow-water habitats in Erdek Bay, Marmara Sea, Turkey. Journal of the Black Sea/Mediterranean Environment, 13, 215-234.
Kurihara, T., Nakano, S., Matsuyama, Y., Hashimoto, K., Yamada, K. et al., 2018. Survival time of juvenile pen shell Atrina pectinata (Bivalvia: Pinnidae) in hyposaline water. International Aquatic Research, 10, 1-11.
Künili, İ.E., Gürkan, S.E., Aksu, A., Turgay, E., Çakir, F. et al., 2021. Mass mortality in endangered fan mussels Pinna nobilis (Linnaeus 1758) caused by co-infection of Haplosporidium pinnae and multiple Vibrio infection in Çanakkale Strait, Turkey. Biomarkers, 26 (5), 450-461.
Maeno, Y., Yurimoto, T., Nasu, H., Ito, S., Aishima, N. et al., 2006. Virus-like particles associated with mass mortalities of the pen shell Atrina pectinata in Japan. Diseases of Aquatic Organisms, 71 (2), 169-173.
Maeno, Y., Suzuki, K., Yurimoto, T., Kiyomoto, S., Fuseya, R. et al., 2012. Laboratory and field studies on gill and kidney associated virus in the pen shell Atrina lischkeana (Mollusca: Bivalvia). Bulletin of the European Association of Fish Pathologists, 32 (3), 78-86.
Marbá, N., Díaz-Almela, E., Duarte, C.M., 2014. Mediterranean seagrass (Posidonia oceanica) loss between 1842 and 2009. Biological Conservation, 176, 183-190.
Öndes, F., Alan, V., Akçalı, B., Güçlüsoy, H., 2020a. Mass mortality of the fan mussel, Pinna nobilis in Turkey (eastern Mediterranean). Marine Ecology, 41 (5), e12607.
Öndes, F., Kaiser, M.J., Güçlüsoy, H., 2020b. Human impacts on the endangered fan mussel, Pinna nobilis. Aquatic Conservation: Marine and Freshwater Ecosystems, 30, 31-41.
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.
Özalp, H.B., 2021. First massive mucilage event observed in deep waters of Çanakkale Strait (Dardanelles), Turkey. Journal of the Black Sea/Mediterranean Environment, 27 (1), 49-66.
Perçin-Paçal, F., Altınsaçlı, S., Arısal, S.B., Balkıs, H., 2019. Assessment of the spatio-temporal distribution and habitat preferences of Ostracoda (Crustacea) related to certain environmental factors in Kapıdağ Peninsula (The Sea of Marmara, Turkey). Hacettepe Journal of Biology and Chemistry, 47 (4), 347-365.
Prado, P., Caiola, N., Ibáñez, C., 2014. Habitat use by a large population of Pinna nobilis in shallow waters. Scientia Marina, 78 (4), 555-565.
Rabaoui, L., Tlig-Zouari, S., Ben Hassine, O.K., 2008. Distribution and habitat of the fan mussel Pinna nobilis Linnaeus, 1758 (Mollusca: Bivalvia) along the northern and eastern Tunisian coasts. Cahiers de Biologie Marine, 49 (1), 67-78.
Rabaoui, L., Tlig-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 (1), 129-141.
Richardson, C.A., Kennedy, H., Duarte, C.M., Kennedy, D.P., Proud, S.V., 1999. Age and growth of the fan mussel Pinna nobilis from south–east Spanish Mediterranean seagrass (Posidonia oceanica) meadows. Marine Biology, 133, 205- 212.
Riva, A., 2002. Approche méthodologique de quelques paramètres bioénergétiques chez Pinna nobilis. p. 91-102. In: Premier séminaire international sur la grande nacre de Méditerranée: Pinna nobilis. Vicente, N. (Ed). Mémoires de l’Institut Océanographique Paul Ricard, Nice.
Rouanet, E., Trigos, S., Vicente, 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.
Ruitton, S., Lefebvre, C., 2021. Toward a recovery of the pen shell Pinna nobilis in the French Mediterranean open sea? Scientific Reports of the Port-Cros National Park, 35, 429- 434.
Russo, P., 2012. Segnalazione di una grande colonia di Pinna nobilis (Linnaeus, 1758) nella Laguna di Venezia. Notiziario della Società Italiana di Malacologia, 30 (1), 31-34.
Russo, P., 2017. Lagoon malacofauna: results of malacological research in the Venice Lagoon. Bollettino Malacologico, 53 (1), 49-62.
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 (10), 776.
Scarpa, F., Sanna, D., Azzena, I., Cossu, P., Casu, M., 2021. From dark to light and back again: is Pinna nobilis, the largest Mediterranean shellfish, on the brink of extinction?. Veterinaria, 70 (1), 1-14.
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 (1), 91-98.
Sokal, R.R., Rohlf, F.J., 1969. Introduction to biostatistics. W.H. Freeman and Company, New York.
Theodorou, H.A., James, R., Tagalis, D., Tzovenis, I., Hellio, C. et al., 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: International Journal of Marine Sciences, 58 (1), 63-76.
Topçu, N.E., Öztürk, B., 2021. The impact of the massive mucilage outbreak in the Sea of Marmara on gorgonians of Prince Islands: A qualitative assessment. Journal of the Black Sea/Mediterranean Environment, 27 (2), 270-278.
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 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 Association of the United Kingdom, 94 (4), 787-796.
Vázquez-Luis, M., Banach-Esteve, G., Álvarez, E., Deudero, S., 2014. Colonization on Pinna nobilis at a marine protected area: Extent of the spread of two invasive seaweeds. Journal of the Marine Biological Association of the United Kingdom, 94 (5), 857-864.
Vázquez-Luis, M., Borg, J.A., Morell, C., Banach-Esteve, G., Deudero, S., 2015. Influence of boat anchoring on Pinna nobilis: a field experiment using mimic units. Marine and Freshwater Research, 66 (9), 786-794.
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.
Vicente, N., 1990. Estudio ecológico y protección del molusco lamelibranquio Pinna nobilis L., 1758 en la costa mediterránea. Iberus, 9 (1-2), 269-279.
Vicente, N., Moreteau, J.C., 1991. Statut de Pinna nobilis L. en Méditerranée (mollusque eulamellibranche). p. 159- 168. In: Les espèces marines à protèger en Mèditerranèe. Boudouresque, C.F., Avon, M., Gravez, V. (Eds). GIS Posidonie Publications, Marseille.
Zavodnik, D., 1967. Contribution to the ecology of P. nobilis L. (Moll., Bivalvia) in the northern Adriatic. Thalassia Jugoslavica, 3, 93-103.
Zavodnik, D., Hrs-Brenko, M., Legac, M., 1991. Synopsis on the fan shell Pinna nobilis L. in the eastern Adriatic Sea. p. 169-178. In: Les espèces marines à protèger en Mèditerranèe. Boudouresque, C.F., Avon, M., Gravez, V. (Eds). GIS Posidonie Publications, Marseille.