“With the contribution of the LIFE programme, the European Union’s financial instrument supporting environmental, nature conservation and climate action projects.”
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Scientific articles from the project
The bibliography sources can be found in alphabetical order by year:
Carella, F., Prado, P., de Vico, G., Palić, D., Villari, G., García-March, J. R., Tena-Medialdea, J., Cortés Melendreras, E., Giménez-Casalduero, F., Sigovini, M., & Aceto, S. (2023). A widespread picornavirus affects the hemocytes of the noble pen shell (Pinna nobilis), leading to its immunosuppression. Frontiers in Veterinary Science, 10. https://doi.org/10.3389/fvets.2023.1273521
The widespread mass mortality of the noble pen shell (Pinna nobilis) has occurred in several Mediterranean countries in the past 7 years. Single-stranded RNA viruses affecting immune cells and leading to immune dysfunction have been widely reported in human and animal species. Here, we present data linking P. nobilis mass mortality events (MMEs) to hemocyte picornavirus (PV) infection. This study was performed on specimens from wild and captive populations. We sampled P. nobilis from two regions of Spain [Catalonia (24 animals) and Murcia (4 animals)] and one region in Italy [Venice (6 animals)]. Each of them were analyzed using transmission electron microscopy (TEM) to describe the morphology and self-assembly of virions. Illumina sequencing coupled to qPCR was performed to describe the identified virus and part of its genome. In 100% of our samples, ultrastructure revealed the presence of a virus (20 nm diameter) capable of replicating within granulocytes and hyalinocytes, leading to the accumulation of complex vesicles of different dimensions within the cytoplasm. As the PV infection progressed, dead hemocytes, infectious exosomes, and budding of extracellular vesicles were visible, along with endocytic vesicles entering other cells. The THC (total hemocyte count) values observed in both captive (eight animals) (3.5 × 104–1.60 × 105 ml−1 cells) and wild animals (14 samples) (1.90–2.42 × 105 ml−1 cells) were lower than those reported before MMEs. Sequencing of P. nobilis (6 animals) hemocyte cDNA libraries revealed the presence of two main sequences of Picornavirales, family Marnaviridae. The highest number of reads belonged to animals that exhibited active replication phases and abundant viral particles from transmission electron microscopy (TEM) observations. These sequences correspond to the genus Sogarnavirus—a picornavirus identified in the marine diatom Chaetoceros tenuissimus (named C. tenuissimus RNA virus type II). Real-time PCR performed on the two most abundant RNA viruses previously identified by in silico analysis revealed positive results only for sequences similar to the C. tenuissimus RNA virus. These results may not conclusively identify picornavirus in noble pen shell hemocytes; therefore, further study is required. Our findings suggest that picornavirus infection likely causes immunosuppression, making individuals prone to opportunistic infections, which is a potential cause for the MMEs observed in the Mediterranean.
Coupé, S., Giantsis, I. A., Vázquez Luis, M., Scarpa, F., Foulquié, M., Prévot, J. M., Casu, M., Lattos, A., Michaelidis, B., Sanna, D., García-March, J. R., Tena-Medialdea, J., Vicente, N., & Bunet, R. (2023). The characterization of toll-like receptor repertoire in Pinna nobilis after mass mortality events suggests adaptive introgression. Ecology and Evolution, 13(8). https://doi.org/10.1002/ece3.10383
Foulquie, M., Coupe, S., Vicente, N., & Bunet, R. (2023). First detection of Pinna nobilis infection by Haplosporidium pinnae in the sanctuary area of Thau lagoon, France. Mediterranean Marine Science, 24(3), 569–573. https://doi.org/10.12681/MMS.32300
The noble pen shell Pinna nobilis is an endemic and emblematic giant bivalve whose populations have been recently affected by a mass mortality event (MME), primarily due to the spread of the pathogen Haplosporidium pinnae. Since the beginning of the MME in Spain in 2016, nearly one hundred percent of monitored open sea water populations have been decimated around the Mediterranean Sea. The only refuge areas with living P. nobilis populations were found in coastal lagoons. Today, the Thau lagoon in France is home to a vitally important population of P. nobilis and was thought to be safe from the parasite. Here, we report the first molecular detection of H. pinnae (isolate PN1) in tissue samples of moribund individuals from Thau lagoon.
Hernandis, S., Ibarrola, I., Tena-Medialdea, J., Albentosa, M., Prado, P., Vázquez-Luis, M., & García-March, J. R. (2023). Physiological responses of the fan mussel Pinna nobilis to temperature: ecological and captivity implications. Mediterranean Marine Science, 24(2). https://doi.org/10.12681/mms.31050
The fan mussel Pinna nobilis is experiencing a mass mortality event throughout the Mediterranean Sea. The survival of the remaining isolated populations and the maintenance and reproduction of individuals in captivity could determine the future of the species. This paper examines the clearance rate (CR) and oxygen consumption (VO2) of fan mussel individuals measured under 5 different temperatures (8.5, 14, 18, 23 and 28ºC). The measurements of both physiological variables revealed a threshold limit of thermal tolerance at both extreme temperatures, indicating the critical situation of the remaining populations, which are located in coastal lagoons and shallow bays where these extreme temperatures usually occur. Besides, the high clearance rates observed highlight the significant ecosystem service provided by the species in terms of water filtration, especially in confined waters with low renewal rates. Routine control of the clearance rate as an early warning system is proposed for detecting ailing individuals. Such a system could also be used to improve captivity conditions.
Labidi, S., Vázquez-Luis, M., Catanese, G., Grau, A., Khammassi, M., ben Youssef, S., & Sghaier Achouri, M. (2023). 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. Mediterranean Marine Science, 24(3), 470–481. https://doi.org/10.12681/MMS.31664
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.
Moro-Martínez, I., Vázquez-Luis, M., García-March, J. R., Prado, P., Mičić, M., & Catanese, G. (2023). Haplosporidium pinnae Parasite Detection in Seawater Samples. Microorganisms, 11(5). https://doi.org/10.3390/microorganisms11051146
In this study, we investigated the presence of the parasite Haplosporidium pinnae, which is a pathogen for the bivalve Pinna nobilis, in water samples from different environments. Fifteen mantle samples of P. nobilis infected by H. pinnae were used to characterize the ribosomal unit of this parasite. The obtained sequences were employed to develop a method for eDNA detection of H. pinnae. We collected 56 water samples (from aquaria, open sea and sanctuaries) for testing the methodology. In this work, we developed three different PCRs generating amplicons of different lengths to determine the level of degradation of the DNA, since the status of H. pinnae in water and, therefore, its infectious capacity are unknown. The results showed the ability of the method to detect H. pinnae in sea waters from different areas persistent in the environment but with different degrees of DNA fragmentation. This developed method offers a new tool for preventive analysis for monitoring areas and to better understand the life cycle and the spread of this parasite.
Papadakis, O., Mamoutos, I., Ramfos, A., Catanese, G., Papadimitriou, E., Theodorou A., J., Batargias, C., Papaioannou, C., Kamilari, M., Tragou, E., Zervakis, V., & Katsanevakis, S. (2023). Status, distribution, and threats of the last surviving fan mussel populations in Greece. Mediterranean Marine Science, 24(3), 679–708. https://doi.org/10.12681/mms.35384
Since the first confirmed records of mass mortality events (MME) in the Aegean Sea in 2018, Pinna nobilis populations in Greek seas have been decimated. To bolster recovery efforts, this study aimed to assess the status of fan mussel populations in the Aegean and Ionian seas and investigate potential recolonization through natural recruitment. From May 2022 to May 2023, 163 independent underwater visual surveys were conducted across various locations and depths along the Greek coastline. A total of 4348 P. nobilis individuals was recorded, of which 87.3% were found dead and 12.7% were alive. The sole surviving fan mussel populations were located in the semi-enclosed gulfs of Amvrakikos in the Ionian Sea and of Kalloni in the Aegean Sea, with estimated recent mortality rates (excluding potential poaching) of 7.7% and 6.3%, respectively. To track potential new recruitment, a network of larvae collectors was deployed in multiple locations. Additionally, an ocean circulation model (OCM) was developed to predict the export and fate of larvae from the surviving populations in the Marmara Sea towards the Aegean Sea. Beyond the MME, this study identified several other threats, which significantly endanger fan mussel survival. The findings of this study underscore the urgent need to implement protection measures and restoration actions to enhance the chances of P. nobilis survival and recovery in the Greek seas.
Zotou, M., Papadakis, O., Catanese, G., Stranga, Y., Ragkousis, M., Kampouris E., T., Naasan Aga - Spyridopoulou, R., Papadimitriou, E., Koutsoubas, D., & Katsanevakis, S. (2023). New kid in town: Pinna rudis spreads in the eastern Mediterranean. Mediterranean Marine Science, 24(3), 709–721. https://doi.org/10.12681/mms.35343
Cortés-Melendreras, E., Gomariz-Castillo, F., Alonso-Sarría, F., Giménez Martín, F. J., Murcia, J., Canales-Cáceres, R., Ramos Esplá, A. A., Barberá, C., & Giménez-Casalduero, F. (2022). The relict population of Pinna nobilis in the Mar Menor is facing an uncertain future. Marine Pollution Bulletin, 185, 114376. https://doi.org/10.1016/J.MARPOLBUL.2022.114376
Pinna nobilis is undergoing one of the most dramatic events suffered by an endangered species. An emerging disease has relegated its populations to coastal lagoons or estuaries with salinities beyond the 36.5–39.7 psu range. The Mar Menor is one of two such locations on the Spanish coastline. Poor environmental conditions and eutrophication and anoxia events, that became critical in 2016, 2019 and 2021, have reduced its population in >99 %. In this work, the spatial distribution of the species within the lagoon and the factors determining its survival along the successive crises of eutrophication are studied using a two-stage (presence/absence estimation and density modelling) Species Distribution Model. A potential area of 200.97 ha and an average density of 1.05 ind.100 m2 is estimated for 2020. The viability of the Mar Menor population depends on management actions designed both for the species and to improve the lagoon environmental state.
Other scientific articles related
Hernandis, S., Prado, P., García-March, J. R., Gairin, I., Vázquez-Luis, M., & Tena-Medialdea, J. (2023). Reproduction of the endangered fan mussel Pinna nobilis under natural and captivity conditions. Aquatic Conservation: Marine and Freshwater Ecosystems, 33(12), 1501–1513. https://doi.org/10.1002/aqc.4009
Catanese, G., Tena-Medialdea, J., Bel Dajković, M. A., Mičić, M., García-March, J. R. (2022). An incubation water eDNA method for a non-destructive rapid molecular identification of Pinna nobilis and Pinna rudis bivalve juveniles. MethodsX, 9, 101708. https://doi.org/10.1016/j.mex.2022.101708
Grau, A., Villalba, A., Navas, J. I., Hansjosten, B., Valencia, J. M., García-March, J. R., Prado, P., Follana-Berná, G., Morage, T., Vázquez-Luis, M., Álvarez, E., Katharios, P., Pavloudi, C., Nebot-Colomer, E., Tena-Medialdea, J., Lopez-Sanmartín, M., Peyran, C., Čižmek, H., Sarafidou, G., … Catanese, G. (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. https://doi.org/10.3389/FMARS.2022.666640/FULL
Prado, P., Grau, A., Catanese, G., Cabanes, P., Carella, F., Fernández-Tejedor, M., Andree, K. B., Añón, T., Hernandis, S., Tena, J., & García-March, J. R. (2021). Pinna nobilis in suboptimal environments are more tolerant to disease but more vulnerable to severe weather phenomena. Marine Environmental Research, 163. https://doi.org/10.1016/J.MARENVRES.2020.105220
Giménez-Casalduero, F., Gomariz-Castillo, F., Alonso-Sarría, F., Cortés, E., Izquierdo-Muñoz, A., & Ramos-Esplá, A. A. (2020). Pinna nobilis in the Mar Menor coastal lagoon: a story of colonization and uncertainty. Marine Ecology Progress Series, 652, 77–94. https://doi.org/10.3354/MEPS13468
Prado, P., Andree, K.B., Trigos, S., Carrasco, N., Caiola, N., García-March, J. R., Tena, J., Fernández-Tejedor, M. & Carella, F. (2020). Breeding, planktonic and settlement factors shape recruitment patterns of one of the last remaining major population of Pinna nobilis within Spanish waters. Hydrobiologia 847, 771–786. https://doi.org/10.1007/s10750-019-04137-5
Prado, P., Carrasco, N., Catanese, G., Grau, A., Cabanes, P., Carella, F., García-March, J. R., Tena, J., Roque, A., Bertomeu, E., Gras, N., Caiola, N., Furones, M. D., & Andree, K. B. (2020). Presence of Vibrio mediterranei associated to major mortality in stabled individuals of Pinna nobilis L. Aquaculture, 519, 734899. https://doi.org/10.1016/J.AQUACULTURE.2019.734899
Posters
Current status and perspectives of the pen shell (Pinna nobilis) in the western Mediterranean Sea; a species highly threatened with extinction
The poster was showcased at the Annual Meeting of the British Ecological Society (BES Meeting 2023), held in Belfast, the capital of Northern Ireland, from December 12 to 15, 2023.
In the last decade, Pinna nobilis has suffered a drastic population decline due to an infectious disease, likely caused by the protozoan parasite Haplosporidium pinnae and the bacteria Mycobacterium spp., among others. Consequently, only a few isolated surviving populations persist scattered along its original habitat. Since 2016, when a mass mortality event occurred, substantial efforts have been made by the scientific community to preserve the species. In this sense, the current situation of the species presented here, centered in the Ebro Delta population and the NE Iberian Peninsula, is being studied as part of the LIFE project (LIFE PINNARCA NAT/ES/001265), focused on improving our understanding of key aspects of pen shell biology, ecology, and populations status, an essential information to develop conservation and management strategies for preserving the species.
With this poster, we aimed to raise awareness on a global scale, given the participation of over 1,500 delegates from more than 50 countries across six continents attending the meeting in person or online. Additionally, we sought to encourage broad public collaboration and provided a more informed background to other countries planning mitigation and recovery actions on the topic.
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Pinna nobilis, in search for the surviving fan mussel population in Greece
The poster was presented in the 15th International Congress of Zoogeography and Ecology of Greece and Adjacent Regions (15th ICZEGAR), hosted by the University of the Aegean, Department of Marine Sciences from 12 to 15 October 2022 in Mytilini.
To track the progress of the Pinna nobilis mass mortality event in Greece by September 2022, the present study attempted to assess the status of fan mussel populations in the Aegean and Ionian Seas by means of underwater visual surveys.
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