First detection of the invasive protozoan Haplosporidium pinnae in the critically endangered bivalve Pinna nobilis in the Southern Mediterranean Sea (Bizerte Lagoon, Tunis) and update of its current status

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Published: Sep 6, 2023
DOI: https://doi.org/10.12681/mms.31664
Keywords:
Pinnidae pen shell Mass Mortality Haplosporidium pinnae Bizerte Lagoon Tunisia
SARRA LABIDI
University of Tunis El Manar, Faculty of Sciences of Tunis, Laboratory of Diversity, Management and Conservation of Biological Systems, LR18ES06, Tunis, Tunisia
https://orcid.org/0000-0002-5925-7893
MAITE VÁZQUEZ-LUIS
Instituto Español de Oceanografía (IEO, CSIC), Centro Oceanográfico de Baleares, 07010, Palma de Mallorca, Spain
GAETANO CATANESE
Laboratorio de Investigaciones Marinas y Acuicultura (LIMIA-IRFAP)- Balearic Government, 07157 Port d’Andratx, Spain
AMALIA GRAU
Laboratorio de Investigaciones Marinas y Acuicultura (LIMIA-IRFAP)- Balearic Government, 07157 Port d’Andratx, Spain
MARWA KHAMMASSI
University of Tunis El Manar, Faculty of Sciences of Tunis, Laboratory of Diversity, Management and Conservation of Biological Systems, LR18ES06, Tunis, Tunisia
SOUMAYA BEN YOUSSEF
University of Tunis El Manar, Faculty of Sciences of Tunis, Laboratory of Diversity, Management and Conservation of Biological Systems, LR18ES06, Tunis, Tunisia
MOHAMED SGHAIER ACHOURI
University of Tunis El Manar, Faculty of Sciences of Tunis, Laboratory of Diversity, Management and Conservation of Biological Systems, LR18ES06, Tunis, Tunisia
Abstract

Pinna nobilis (Linnaeus, 1758) populations have been severely damaged in the last few decades, and since early autumn 2016, a mass mortality event (MME) has drastically impacted populations in the Mediterranean Sea. Accordingly, the aim of the present study was to improve the knowledge on the status of P. nobilis populations in the Bizerte Lagoon (Tunisia) between 2016 and 2022. Before the MME, P. nobilis was found in the lagoon at depths from 1.5 to 6 m, with a density ranging from 2 to 30 ind/100 m². After the MME, mortality reached 100% in the monitored area, except in the eastern part of the Bizerte Lagoon near the Menzel Jemil site, where some living specimens were detected. Moreover, in 2022, successful recruitment was observed in the lagoon. Additionally, our results revealed the presence of Haplosporidium pinnae and Mycobacterium sp. in some living specimens sampled in the Bizerte Lagoon after the MME. This finding constitutes the first detection of both pathogens in Tunisia and in the entire Southern Mediterranean Sea.

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References
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, 62-70.
Afli, A., Ayari, R., Zaabi, S., 2008. Ecological Quality of Some Tunisian Coast and Lagoon Locations, by Using Benthic Community Parameters and Biotic Indices. Estuarine, Coastal and Shelf Science, 80 (2), 269-280.
Alves Martins, M.V., Helali, M.A., Zaaboub, N., Boukef-Ben- Omrane, I., Frontalini, F. et al., 2016. Organic matter quantity and quality, metals availability and foraminiferal assemblages as environmental proxy applied to the Bizerte Lagoon (Tunisia). Marine Pollution Bulletin, 105 (1), 161-179.
Andree, K.B., Carrasco, N., Carella, F., Furones, D., Prado, P., 2021. Vibrio mediterranei, a Potential Emerging Pathogen of Marine Fauna: Investigation of pathogenicity using a bacterial challenge in Pinna nobilis and development of a species-specific PCR. Journal of Applied Microbiology, 1-15.
Arzul, I., Carnegie, R.B., 2015. New perspective on the haplosporidian parasites of molluscs. Journal of Invertebrate Pathology, 131, 32-42.
Basso, L., Hendriks, I.E., Rodríguez-Navarro, A.B., Gambi, M.C., Duarte, C.M., 2015. Extreme PH Conditions at a Natural CO2 Vent System (Italy) Affect Growth, and Survival of Juvenile Pen Shells (Pinna Nobilis). Estuaries and Coasts, 38 (6), 1986-99.
Béjaoui, B., 2009. Developpement d’un modèle tridimensionnel couplé dynamique-ecologie : Application à la lagune de Bizerte. MSc Thesis. Ecole National d’Ingénieurs de Tunis, 209 pp.
Béjaoui, B., Moussa, M., Ben Charrada, R., Ben Hamadou, R., 2005. Caractérisation hivernale de la lagune de Bizerte. Bulletin institut national des sciences et technologies de la mer de Salammbo, 32, 79-91.
Ben Hassine, O.K., Rabaoui, L., 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.
Ben Salem, F., Ben Said, O., Aissa, P., Mahmoudi, E., Duran, R. et al., 2017. Distribution of organic contamination of sediments from Ichkeul Lake and Bizerte Lagoon, Tunisia. Marine Pollution Bulletin, 123 (1-2), 329-338.
Böddinghaus, B., Rogall, T., Flohr, T., Blöcker, H., Böttger, E.C., 1990. Detection and identification of mycobacteria by amplification of rRNA. Journal of clinical microbiology, 28, 1751-1759.
Box, A., Capó, X., Tejada, S., Catanese, G., Grau, A. et al., 2020. Reduced Antioxidant Response of the Fan Mussel Pinna nobilis Related to the Presence of Haplosporidium pinnae. Pathogen, 9, 932. Buchana, J., 1984. Sediment analysis. p. 284-386. In: Methods for the Study of Marine Benthos. Holme N.A., McIntyre, A.D. (Eds). Blackwell Scientific Publications, Oxford.
Burrough, P.A., 1986. Principles of Geographical Information Systems for Land Resources Assessment. Oxford University Press, Oxford, 193 pp.
Butler, A., Vicente, N., de Gaulejac, B., 1993. Ecology of the Pterioid Bivalves Pinna Bicolor Gmelin and Pinna Nobilis L. Marine Life, 3 (1-2), 37-45.
Cabanellas-Reboredo, M., Vázquez-Luis, M., Mourre, B., Alvarez, E., Deudero. 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., Aceto, S., Pollaro, F., Miccio, A., Iaria, C. et al., 2019. A mycobacterial disease is associated with the silent mass mortality of the pen shell Pinna nobilis along the Tyrrhenian coastline of Italy. Scientific reports, 9, 1-12.
Carella, F., Antuofermo, E., Farina, S., Salati, F., Mandas. 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) Front. 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.
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 (1- 3), 339-47.
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.
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 Association of the United Kingdom, 90 (5), 885-94.
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). Invertebrate Pathology, 148, 14-19.
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), 1-14.
Deudero, S., Grau, A., Vázquez-Luis, M., Álvarez, E., Alomar, C. et al., 2017. Reproductive investment of the pen shell Pinna nobilis Linnaeus, 1758in Cabrera National Park (Spain). Mediterranean Marine Science,18, 271-284.
Donato, G., Vázquez-Luis, M., Nebot-Colomer, E., Lunetta, A., Giacobbe, S., 2021. Noble fan-shell, Pinna nobilis, in Lake Faro (Sicily, Italy): Ineluctable decline or extreme opportunity? Estuarine Coastal and Shelf Science, 261, 107536.
El Zrelli, R., Yacoubi, L., Wakkaf, T., Castet, S., Grégoire, M. et al., 2021. Surface sediment enrichment with trace metals in a heavily human-impacted lagoon (Bizerte Lagoon, Southern Mediterranean Sea): Spatial distribution, ecological risk assessment, and implications for environmental protection. Marine Pollution Bulletin, 169, 112512.
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., Pérez-Rojas, L., García-Carrascosa, A.M., 2007. 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 (2), 202-212.
García-March, J.R., Sanchís Solsona, M.Á., García-Carrascosa, A.M., 2008. Shell gaping behaviour of Pinna nobilis L., 1758: Circadian and circalunar rhythms revealed by in situ monitoring. Marine Biology, 153 (4), 689-698.
García-March, J.R., Tena-Medialdea, J., Henandis-Caballero, S., Vázquez-Luis, M., López, D., Téllez, C. et al., 2020. Can we save a marine species affected by a highly-infective- highly-lethal waterborne disease from extinction? Biological Conservation, 243, 108-498.
Grau, A., Villalba, A., Navas, J.I., Hansjosten, B., Valencia, J.M. et al., 2022.Wide-geographic and long-term analysis of the role of pathogens in the decline of Pinna nobilis to critically endangered species. Frontiers in Marine Science, 9, 666640. Gutiérrez, M., 1967. Coloración histoloógica para ovarios de peces, crustáceos ymoluscos. Investigación Pesquera, 31, 265-271.
IUCN ., 2019. The IUCN Red List of Threatened Species 2019. Gland: IUCN.
Katsanevakis, S., 2004. Population Ecology of the Endangered Fan Mussel Pinna Nobilis in a Marine Lake. Endangered Species Research, 1,51-59.
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 (1), 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 Invasion, 14, 150-164.
Katsanevakis, S., Carella, F., Çinar, M., Cizmek, H., Jimenez, C. et al., 2021. The Fan Mussel Pinna nobilis on the Brink of Extinction in the Mediterranean. p. 700-709. In: the Encyclopedia of Conservation. DellaSala, D.A., Goldstein, M.I. (Eds). Elsevier, Oxford.
Kersting, D., Benabdi, M., Čižmek, H., Grau, A., Jimenez. et al., 2019. Pinna nobilis. The IUCN Red List of Threatened Species 2019. e.T160075998A160081499.
Khammassi, M., Jourde, J., Zaabar, W., Laabidi, S., Sauriau, P.G. et al., 2019. Inventory and New Records of Benthic Amphipods from Macrophytes and Fine Sand Communities of the Bizerte Lagoon (Tunisia, SW Mediterranean Sea). Marine Biodiversity Records, 12, 24.
Khammassi, M., Jourde, J., Labidi, S., Achouri, M.S. 2022. Isopod assemblages in the Bizerte lagoon (SW Mediterranean Sea): composition, structure and environmental relationships. Mediterranean Marine Science, 23 (1), 84-97.
Kjerfve, B., 1994. Coastal Lagoon Processes. Elsevier Science Publishers, Amsterdam, 577pp.
Lattos, A., Ioannis, A.G., Dimitrios, K., Basile, M., 2020. First Detection of the Invasive Haplosporidan and Mycobacteria Parasites Hosting the Endangered Bivalve Pinna Nobilis in Thermaikos Gulf , North Greece. Marine Environmental Research, 155,104889.
López-Sanmartín, M., Catanese, G., Grau, A., Valencia, J.M., Garcıía-March, J.R. et al., 2019. Real-Time PCR based test for the early diagnosis of Haplosporidium pinnae affecting fan mussel Pinna nobilis. PLoS ONE, 14 (2), 1-12.
Luna, L. G., 1968. Manual of histologic staining methods of the Armed Forces Institute of Pathology. McGraw Hill Book Company, New York, 258 pp.
Moro-Martínez, I., Vázquez-Luis, M., García-March, J.R., Prado, P., Mičić, M. et al., 2023. Haplosporidium pinnae parasite detection in seawater samples. Microorganisms, 11, 1146.
Nebot-Colomer, E., Álvarez, E., Belando, M.D., Deudero, S., Catanese, G. et al., 2021. Living under threat: Will one of the last Pinna nobilis populations be able to survive? aquatic conservation marine and freshwater ecosystems,1-13.
Newton, A., Brito, A.C., Icely, J.D., Derolez., Clara, I. et al., 2018 Assessing, quantifying and valuing the ecosystem services of coastal lagoons. Journal for Nature Conservation, 44, 50-65.
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.
Peyran, C., 2021a. Etude génétique des populations de grandes nacres, Pinna nobilis, en Occitanie : identification de priorités de conservation dans un contexte de pandémie. PhD Thesis, Sorbonne Université, 224p.
Peyran, C., Boissin, E., Morage, T., Nebot-Colomer, E., Iwankow, G. et al., 2021b. Genetic homogeneity of the critically endangered fan mussel, Pinna nobilis, throughout lagoons of the Gulf of Lion (North-Western Mediterranean Sea). Scientific reports, 11, 7805.
Prado, P., Carrasco, N., Catanese, G., Grau, A., Cabanes, P. et al., 2020. Presence of Vibrio mediterranei associated to major mortality in stabled individuals of Pinna nobilis L. Aquaculture, 519, 734899.
Prado, P., Grau, A., Catanese, G., Cabanes, P., Carella, F., et al., 2021. Pinna nobilis in suboptimal environments are more resilient to disease but more vulnerable to catastrophic events. Marine Environmental Research 163,105220.
Rabaoui, L., Tlig Zouari, S., Katsanevakis, S., Ben Hassine, O.K., 2007. Comparison of Absolute and Relative Growth Patterns among Five Pinna Nobilis Populations along the Tunisian Coastline: An Information Theory Approach. Marine Biology, 152 (3), 537-48.
Rabaoui, L., Tlig-Zouari, S., Katsanevakis, S., Ben Hassine, O.K., 2010. Modelling Population Density of Pinna Nobilis (Bivalvia) on the Eastern and Southeastern Coast of Tunisia. Journal of Molluscan Studies, 76 (4), 340-47.
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). Report Port-Cros National Park, 29, 209-222.
Shaiek, M., Ben Amer, I., El Mokni, R., Jaziri, S., Aissi, M. et al., 2018. Genesis of Islets in Bizerte lagoon: settlement of pioneer species. Bulletin institut national des sciences et technologies de la mer de Salammbo, 45, 93-96.
Siletic, 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.
Theodorou, J.A., Ross, J., Dimitrios, T., Ioannis, Τ., Claire, H. 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, 58 (1), 63-76.
Tiscar, P.G., Rubino, F., Paoletti, B., Di Francesco, C.E., Mosca, F. et al., 2022. New insights about Haplosporidium pinnae and the pen shell Pinna nobilis mass mortality events. Journal of Invertebrate Pathology, 190, ISSN 0022-2011.
Tlig Zouari, S., 1993. Contribution à l’étude Écobiologique de Deux Espèces de Mollusques Lamellibranches Pinctada Radiata (Leach, 1814) et Pinna Nobilis, Linné 1758 Des Îles Kerkennah. PhD Thesis, Université de Tunis : Faculté des Sciences de Tunis, 215pp.
Trigos, S., García-March, J.R., Vicente, N., Tena, J., Torres, J., 2014. Utilization of Muddy Detritus as Organic Matter Source by the Fan Mussel Pinna Nobilis. Marine Science, 15 (3), 667-74.
Triki, H.Z., Daly-Yahia, O.K., Malouche, D., Komiha, Y., Deidun, A. et al., 2014. Distribution of resting cysts of the potentially toxic dinoflagellate Alexandrium pseudogonyaulax in recently deposited sediment within Bizerte Lagoon (Mediterranean coast, Tunisia). Marine Pollution Bulletin, 84, 172-181.
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), 787-96.
Vázquez-Luis, M., March, D., Alvarez, E., Alvarez-Berastegui, D., Deudero, S., 2014. Spatial distribution modelling of the endangered bivalve Pinna nobilis in a Marine Protected Area. Mediterranean Marine Science, 15 (3), 626-634.
Vázquez-Luis, M., Borg, J.A., Morell, C., Banach-Esteve, G., Deudero, S., 2015. Influence of boat anchoring on Pinna nobilis: a field experiment usingmimic units. Marine Freshwater Research, 66, 786-794.
Vázquez-Luis, M., Elvira, A.P., Barrajón, A., García-March, J.R., Grau, et al., 2017a. S.O.S. Pinna Nobilis: A Mass Mortality Event in Western Mediterranean Sea. Frontiers in Marine Science, 4, 220, (2296-7745).
Vázquez-Luis, M., Elvira, A.P., Deudero, S., 2017b. Proposal of action plan for Pinna nobilis in the Mediterranean sea in the frame of the Marine Strategy Framework Directive (MSFD). Instituto Español de Oceanografía, 53 pp.
Vicente, N., Moreteau, J.C., 1991. Statut de Pinna Nobilis L. En Mediterranee (Mollusque Eulamellibranche). p. 340- 347. In: Modelling Population Density of Pinna Nobilis (Bivalvia) on the Eastern and Southeastern Coast of Tunisia.
Rabaoui, L., Tlig-Zouari, S., Katsanevakis, S., Ben Hassine, O.K., Journal of Molluscan Studies, 76 (4).
Wakkaf, T., El Zrelli, R., Kedzierski, M., Balti, R., Shaiek, M. et al., 2020. Characterization of microplastics in the surface waters of an urban lagoon (Bizerte lagoon, Southern Mediterranean Sea): composition, density, distribution, and influence of environmental factors. Marine Pollution Bulletin, 160, 111625.
Yoshida, M., Kallali, H., Ghrabi, A., 2002. Solid Waste Landfills and Soil/Sediment Contamination around Bizerte Lagoon: Possible Pollution Sources. Study of Pollution Sources of Bizerte Lagoon (Tunisia), 55-75.
Zakhama-Sraieb, R., Sghaier, Y.R., Omrane, A., Charfi- Cheikhrouha, F., 2011. Density and population structure of Pinna nobilis (mollusca, bivalvia) in the Ghar El Melh Lagoon (N-E Tunisia). Bulletin institut national des sciences et technologies de la mer de Salammbo, 38, 65-71.
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 Especes Marines à Protégé En Méditerraneé. Boudouresque, C.F., Avon, M., Gravez, V. (Eds). GIS Posidonie publ, Marseille, France.
Zotou, M., Gkrantounis, P., Karadimou, E., Tsirintanis, K., Sini, M. et al., 2020. Pinna nobilis in the Greek Seas (NE Mediterranean): On the Brink of Extinction. Mediterranean Marine Science, 21 (3), 575-91.
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