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Related scientific publications

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Scientific articles

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Posters

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Others

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.

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Cortés Melendreras, E. (2023). Avances en acuariología y conservación de especies marinas. https://digitum.um.es/digitum/handle/10201/135944

Rapid population growth since the mid-20th century has resulted in increased pressure on ecosystems. In recent decades, an increasing deterioration of the environment has been observed, mainly due to anthropogenic factors. Conservation strategies for endangered species need multidisciplinary approaches and require a combination of in situ and ex situ actions, selected considering the specific needs of each species and the threats it faces. The present work is about the conservation of the pen shell (Pinna nobilis Linnaeus, 1758) and is divided into three chapters, the first of which is an in situ study on the diagnosis of the Mar Menor population from its entry into the lagoon to the present time. The next two are ex situ work in a closed system focusing on maintenance and breeding protocols for the species. The populations of the pen shell (Pinna nobilis) have declined progressively in recent decades because of anthropogenic activities. The species' regression increased exponentially since 2016, when a mass mortality event triggered by the parasite Haplosporidium pinnae occurred, although other pathogens may have been involved. The epidemic spread throughout the Mediterranean Sea, relegating their populations to coastal lagoons or estuaries with salinities outside the 36.5-39.7 psu range. The Mar Menor is one of the two locations with these characteristics on the Spanish coast. In the early 1980s, P. nobilis appeared in the Mar Menor lagoon and colonised it rapidly. However, the dispersion of the pen shell in the lagoon was interrupted in 2016 (in parallel to the mass mortality taking place in the Mediterranean) when the population was decimated by a crisis that affected more than 99% of the specimens as a consequence of eutrophication and anoxia events, which became critical in 2016, 2019 and 2021. In the first chapter, we estimated the variations in the potential distribution and density of P. nobilis in the different periods from the colonisation of the lagoon to the present, using two-stage species distribution models (presence/absence estimation and density modelling). The main environmental variables that determined the dispersion and colonisation of the Mar Menor by the bivalve in stages prior to 2016 have been studied, as well as the variables that have modified its distribution in the lagoon after the successive eutrophication crises. The second chapter deals with the establishment of ex situ maintenance protocols for Pinna nobilis. Appropriate recirculation systems have been designed for the maintenance of the species, the appropriate technology has been selected to reproduce the environmental conditions and their annual variations in controlled laboratory environments, and advances have been made in the development of suitable diets and pathogen control therapies to ensure their viability over time in facilities outside their natural environment. The third chapter delves into one of the key objectives to prevent the decline of Pinna nobilis and its extinction, progress in the development of ex situ reproduction protocols considering in situ and ex situ maturation procedures, as well as the fine-tuning of the methodology to ensure larval survival. The viability of the Mar Menor population depends on management actions designed both for the species and to improve the environmental status of the lagoon.

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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

The fan mussel Pinna nobilis is currently on the brink of extinction due to a multifactorial disease mainly caused to the highly pathogenic parasite Haplosporidium pinnae, meaning that the selection pressure outweighs the adaptive potential of the species. Hopefully, rare individuals have been observed somehow resistant to the parasite, stretching the need to identify the traits underlying this better fitness. Among the candidate to explore at first intention are fast-evolving immune genes, of which toll-like receptor (TLR). In this study, we examined the genetic diversity at 14 TLR loci across P. nobilisPinna rudis and P. nobilis × P. rudis hybrid genomes, collected at four physically distant regions, that were found to be either resistant or sensitive to the parasite H. pinnae. We report a high genetic diversity, mainly observed at cell surface TLRs compared with that of endosomal TLRs. However, the endosomal TLR-7 exhibited unexpected level of diversity and haplotype phylogeny. The lack of population structure, associated with a high genetic diversity and elevated dN/dS ratio, was interpreted as balancing selection, though both directional and purifying selection were detected. Interestingly, roughly 40% of the P. nobilis identified as resistant to H. pinnae were introgressed with P. rudis TLR. Specifically, they all carried a TLR-7 of P. rudis origin, whereas sensitive P. nobilis were not introgressed, at least at TLR loci. Small contributions of TLR-6 and TLR-4 single-nucleotide polymorphisms to the clustering of resistant and susceptible individuals could be detected, but their specific role in resistance remains highly speculative. This study provides new information on the diversity of TLR genes within the P. nobilis species after MME and additional insights into adaptation to H. pinnae that should contribute to the conservation of this Mediterranean endemic species.

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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.

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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.

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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

A mass mortality event that started in 2016 has put the fan mussel Pinna nobilis close to the brink of extinction, leading to the species being classified as Critically Endangered in the Red List of the International Union for Conservation of Nature. Under current circumstances, with the persistence of the disease caused by Haplosporidium pinnae in the open sea, isolated populations in coastal lagoons and estuarine bays appear to be the main chance for the survival of the species. The low resilience of those populations highlights the importance of implementing additional measures to avoid the extinction of the fan mussel. One of these measures relies on completing its reproductive cycle in captivity. The reproductive window of the remaining fan mussel population in Alfacs Bay was explored to obtain gametes and to understand possible limitations in the reproductive activity in wild populations. For this purpose, during the reproductive season, several groups of individuals were relocated for short periods (~2 weeks) into the vivarium to obtain gametes under controlled conditions. Simultaneously, controlled temperature treatments and adapted food dosage for conditioning adult fan mussels out of their reproductive season in the wild were conducted in a recirculating aquaculture system. The reproduction of natural populations was mostly restricted to May, featuring temperatures around 20°C. A low success of spawning was obtained in the vivarium, with a 0% success in 11 out of 20 of the trials (six to nine individuals each) and an overall success of 16% (25 out of 156 individuals). A 100% success (14 out of 14) was obtained with individuals conditioned for ~2 months in the recirculating aquaculture system. A second conditioning of six of those individuals was attempted after a ~3-month period, with a 33.3% success of spawning.

Vista marítima

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.

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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.

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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.

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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

In the Mediterranean Sea, the genus Pinna encompasses two large fan-shaped bivalve species, Pinna nobilis and Pinna rudis. Historically, both species coexisted in the western Mediterranean until a mass mortality event (MME) brought P. nobilis to the brink of extinction. Notably, P. rudis remained unaffected by the MME, and its recent successful recruitment and further spread have been hypothesized to be linked to the local extinction of P. nobilis. Although P. rudis has been sparsely recorded in the eastern Mediterranean Sea (with some of these records being doubtful), reports emerging in the summer of 2023 from researchers and citizens have unveiled its sudden spread in the region. This study documents the recent presence of P. rudis within Greek waters through a dedicated survey and molecularly confirmation through two distinct molecular methods. Information derived from a citizen science initiative, following photo-identification of the species was also included. Furthermore, an updated review of the distribution of P. rudis in the Mediterranean Sea, integrating data from literature and online repositories is provided. This research confirms the recent spread of P. rudis in Crete, the Greek Ionian Sea, and Cyprus (first verified records of the species in the regions), in marine areas where P. nobilis has become extinct, further strengthening the hypothesis that P. rudis has benefited from the collapse of P. nobilis populations.

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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

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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Others

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Informe Mar Balear (IEO-CSIC, 2023)

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SMBT Flyer (IOPR, 2022)

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Le Syndicat Mixte Du Bassin De Thau activity report (IOPR, 2022)

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