Article

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

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  • Marine Explorers Society 20000 Leagues
  • Marine Explorers Society 20000 Leagues
Article

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

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Abstract

We identified areas with high individual densities of the pen shell, Pinna nobilis, in two areas along the Croatian Adriatic coast. The surveys carried out in 2018 and 2019 showed population densities of approximately 9 to 13 individuals/100 m². However, in 2019 a mass mortality event (MME) causing 36% to 100% mortality of this bivalve species was observed in the surveyed Croatian bays. The parasite Haplosporidium pinnae was identified by histological and molecular methods in all affected sampled individuals, while Mycobacterium sp. and Gram negative bacilli were detected in some affected and live bivalves. This finding constitutes the first record of these pathogens affecting P. nobilis in the middle Adriatic, confirming the continuous spread of the disease. Previously, the Adriatic water body was considered to be a natural shelter against the MME caused by pathogens in pen shell populations because of its distinct ecological features. The Adriatic Sea is a semi-closed water body with the largest continental shelf in the Mediterranean Sea, and due to its geomorphology and bathymetry, it is a sea with distinct characteristics. Monitoring plans and further studies in the Adriatic bays are now a priority for mitigating the high risk of extinction and working toward the conservation of this protected species.

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... The results of this study are in line with the results obtained by other Croatian researchers [14,15] and clearly show that MMEs have spread from the south to the middle parts of the Eastern Adriatic regions, as well as, ultimately, to the north. We first detected Haplosporidium pinnae in association with mortalities on the Croatian Adriatic coast in in- ...
... The results of this study are in line with the results obtained by other Croatian researchers [14,15] and clearly show that MMEs have spread from the south to the middle parts of the Eastern Adriatic regions, as well as, ultimately, to the north. We first detected Haplosporidium pinnae in association with mortalities on the Croatian Adriatic coast in individuals collected in mid-April 2019 on the outer side of the Mljet Island, situated on the most southern point. ...
... Then, in May, mortalities and detection of samples from Elafiti Island (which is a bit more to the north) that were positive for H. pinnae and Mycobacterium spp. were reported [14]. During the summer period, mortalities were reported at different sites along the coast and close to the islands, mostly in the southern and middle parts of the Eastern Adriatic coast [15]. ...
Article
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Noble pen shells (Pinna nobilis) along the Eastern Adriatic coast were affected by mass mortalities similarly to the populations across the Mediterranean basin. Samples of live animals and organs originating from sites on Mljet Island on the south and the Istrian peninsula on the north of the Croatian Adriatic coast were analyzed using histology and molecular techniques to detect the presence of the previously described Haplosporidium pinnae and Mycobacterium spp. as possible causes of these mortalities. To obtain more information on the pattern of the spread of the mortalities, a study was undertaken in Mljet National Park, an area with a dense population of noble pen shells. The results of the diagnostic analysis and the velocity of the spread of the mortalities showed a significant correlation between increases in water temperature and the onset of mortality. Moderate to heavy lesions of the digestive glands were observed in specimens infected with H. pinnae. A phylogenetic analysis of the detected Haplosporidium pinnae showed an identity of 99.7 to 99.8% with isolates from other Mediterranean areas, while isolated Mycobacterium spp. showed a higher heterogeneity among isolates across the Mediterranean. The presence of Mycobacterium spp. in clinically healthy animals a few months before the onset of mortality imposes the need for further clarification of its role in mortality events.
... (Carella et al., 2019). The coexistence of both pathogens in some diseased populations has been reported (García-March et al., 2020;Lattos et al., 2020;Carella et al., 2020;Č ižmek et al., 2020). Furthermore, the presence of other pathogens, such as Vibrio spp. ...
... The spread of the pathogen H. pinnae has been associated with the MMEs occurring in the Mediterranean Sea (Vázquez-Luis et al., 2017;Catanese et al., 2018;Cabanellas-Reboredo et al., 2019;Katsanevakis et al., 2019;Carella et al., 2020;Č ižmek et al., 2020). The presence of the parasite in Faro Lake was detected in 2019 by Carella et al. (2020) in a single specimen collected from the lake, whose histological analysis showed the co-occurrence of H. pinnae and Mycobacterium sp. ...
Article
The largest bivalve in the Mediterranean Sea, the fan mussel Pinna nobilis, is at risk of extinction due to mass mortality events (MMEs) caused by the spread of pathogens, Haplosporidium pinnae in particularly. In spite of being a protected area, Lake Faro (northeast Sicily, Italy) suffers from high anthropogenic pressures that affect the P. nobilis population that inhabits the lake and the two canals that connect it to the sea. In the present study, the population's long-term changes have been monitored in three distinct periods: before the MME (2010), at the beginning of the epidemic spread along the Italian coasts (2018), and after the MME (2020). The survey, carried out by visual census, showed that, relative to 2010, the population of P. nobilis halved in 2018 and disappeared from the canals in 2020; while in the lake, living specimens were only 27.69 % of the total at this time, without recruits. The disappearance of P. nobilis, allowed rapid colonization by the congeneric Pinna rudis and the invasive oyster Pinctada imbricata radiata, which had never been recorded in the Lake Faro system before 2020.
... Thereafter, severe mortalities of P. nobilis populations were reported from additional locations along the Spanish coastline, as well as France and Italy (Catanese et al., 2018;Carella et al., 2019;Panarese et al., 2019). Soon after the first reports, new MME records were reported in Greece, Cyprus, Turkey, Algeria, Tunisia, Morocco and Croatia, with mortality rates often reaching 100% (Katsanevakis et al., 2019;Kersting et al., 2019;IUCN, 2019;Čižmek et al., 2020). Due to the severe decline of its global population and its high risk of extinction, in 2019, P. nobilis was classified as Critically Endangered in the IUCN Red List of Threatened Species (Kersting et al., 2019). ...
... (Carella et al., 2019). The coexistence of both pathogens in some affected populations has been reported (Garcia-March et al., 2020, Lattos et al., 2020Carella et al., 2020;Čižmek et al., 2020). Furthermore, in some cases, increased sea temperature seems to favour the proliferation of another opportunistic pathogen in P. nobilis, namely Vibrio mediterranei (Rodriguez et al., 2018), which was recently found to intensify pathogenicity and cause increased mortality of stabled fan mussels at temperatures of about 25-26°C (Prado et al., 2020). ...
Article
Full-text available
The Mediterranean endemic fan mussel Pinna nobilis is suffering an ongoing basin-scale mass mortality event (MME) since 2016. As most Mediterranean populations have collapsed, the species has been declared as Critically Endangered in the IUCN Red List of threatened species. In an effort to track the progress of the MME and provide updated information on the status of the species in the Greek seas, we compiled data collected through dedicated surveys and opportunistic assessments during 2019 and 2020. A total of 14589 fan mussel individuals, of which 81.1% dead, were recorded in 258 site surveys. Of the remaining 2762 live individuals, 256 were juveniles. Two marine areas which still sustain living populations were identified, namely Kalloni Gulf (Lesvos Island), and Laganas Bay (Zakynthos Island). The inner part of Kalloni Gulf appears to maintain the largest surviving population of the species in the eastern Mediterranean, with an abundance estimate of 684000 individuals (95% confidence interval: 322000-1453000). Solitary, potentially resistant, scattered individuals were recorded in several sites. Other previously abundant populations that had been assessed in the past, specifically those of Lake Vouliagmeni (Korinthiakos Gulf), Souda Bay (Crete) and Gera Gulf (Lesvos Island), and which collectively summed up to ~350,000 individuals, have now been wiped out. Our results document the collapse of most P. nobilis populations throughout the Greek seas. The MME has substantially progressed between early 2019 and mid-2020, as indicated by the increase of mortality at sites consecutively monitored multiple times. This work highlights the urgent need for continuous monitoring of surviving populations and calls for the immediate implementation of an effective protection and management strategy that will ensure the persistence of surviving individuals and the production of resistant offspring.
... Recently, MME of P. nobilis have been reported, along the Croatian bays of the Adriatic Sea (part of the Mediterranean Sea) [42]. In this survey, the parasite Haplosporidium pinnae was identified by histological and molecular methods in all affected specimens, while Mycobacterium sp. was detected in some affected and live bivalves. ...
... The first description in molluscs was in 1956 by Pan [39], describing an infection caused by an unidentified species of Mycobacterium in the snail Australorbis glabratus. Since that first description, publications describing mycobacteriosis in molluscs have accumulated (Table 1); in the last few years, separate cases of mycobacteriosis have been described in the edible pen shell (Pinna nobilis) from the Mediterranean coast of Italy, Spain, Greece and Croatia [4,16,17,[40][41][42]. ...
Article
Full-text available
Mycobacteriosis is a chronic bacterial disease reported in aquatic and terrestrial animals, including humans. The disease affects a wide range of cultured and wild organisms worldwide. Mycobacteriosis is well-known in aquatic vertebrates (e.g., finfish, marine mammals), while in the last few years, reports of its presence in aquatic invertebrates have been on the rise, for both freshwater and marine species. The number of cases is likely to increase as a result of increased awareness, surveillance and availability of diagnostic methods. Domestication of wild aquatic species and the intensification of modern aquaculture are also leading to an increase in the number of reported cases. Moreover, climate changes are affecting fresh and marine aquatic ecosystems. The increasing reports of mycobacteriosis in aquatic invertebrates may also be influenced by global climate warming, which could contribute to the microbes' development and survival rates, pathogen transmission and host susceptibility. Several species of the genus Mycobacterium have been diagnosed in aquatic invertebrates; a few of them are significant due to their wide host spectrum, economic impact in aquaculture, and zoonotic potential. The impact of mycobacteriosis in aquatic invertebrates is probably underestimated, and there is currently no effective treatment other than facility disinfection. In this review, we provide an overview of the diversity of mycobacterial infections reported in molluscs, crustaceans, cnidarians, echinoderms and sponges. We highlight important issues relating to its pathological manifestation, diagnosis and zoonotic considerations.
... Since then, severe high mortality has also been observed in populations of P. nobilis from the north-western Mediterranean reaching the Aegean Sea [8,13]. Even recently, the Adriatic Sea has been affected by mass mortality events with mortalities between 36% and 100%, depending on the affected area [14]. This event involves the loss of an emblematic Mediterranean species; thus, monitoring plans, strict protection, and additional studies are a priority to mitigate the high risk of extinction and work toward the conservation of this species [34,35]. ...
... Furthermore, the presence of acid-fast bacteria, Mycobacterium sp. (confirmed by molecular analyses), had been described in both healthy [14] and sick individuals of Pinna nobilis [9,10]. Healthy adult bivalves possess efficient humoral and cellular defense mechanisms acting against foreign material, destroying or eliminating it [38]. ...
Article
Full-text available
The endemic fan mussel (Pinna nobilis) in the Mediterranean Sea is at high risk of disappearance due to massive mortality events. The aim of the study was to evaluate the antioxidant response of P. nobilis collected in the Balearic Islands (Western Mediterranean) before and after the mass mortality event. Individuals collected before (between 2011 and 2012) and after (between 2016 and 2017) the event were analyzed by histological, molecular, and biochemical methods to compare pathogenic loads and biochemical responses. All the individuals collected during 2016-2017 presented symptoms of the disease and were positive for Haplosporidium pinnae, while acid-fast bacteria or/and Gram-negative bacteria were detected in some individuals of both sampling periods. The activities of the antioxidant enzymes catalase and superoxide dismutase in the gills were significantly lower in P. nobilis affected with the parasite compared to those in the asymptomatic ones, while levels of malondialdehyde, as an indicator of lipid peroxidation, were higher in infected individuals. When analyzing the differential effects of H. pinnae and Mycobacterium sp. on P. nobilis, it was observed that significant effects on biomarkers were only observed in the presence of H. pinnae. Co-infection of P. nobilis by H. pinnae with other pathogens such as Mycobacterium sp. constitutes a serious problem due to its high mortality rate in the Balearic Island waters. This concerning situation for P. nobilis is favored by a reduction in antioxidant defenses related to H. pinnae infection that induces oxidative stress and cell damage.
... Both species are threatened by different anthropogenic pressures such as harvesting, trawling, anchoring or degradation of its natural habitat and are listed on Annex II of the Bern and Barcelona Convention. In the last few years, P. nobilis populations have undergone a significant reduction in individual number due to massive mortality events (MMEs) [4] associated to the presence of pathogens: the parasite Haplosporidium pinnae, Mycobacterium sp., Vibrio mediterranei or co-infection of them [5][6][7][8][9][10][11]. Since 2016 the mortality has spread to all the coasts of Mediterranean countries, reaching France, Italy, Greece, Cyprus and other Mediterranean countries [8,[12][13][14][15][16]. Due to its massive decline (> 99.9% mortality in most sites), P. nobilis is now listed as "critically endangered" species according to the IUCN Red List [16]. ...
... In the last few years, P. nobilis populations have undergone a significant reduction in individual number due to massive mortality events (MMEs) [4] associated to the presence of pathogens: the parasite Haplosporidium pinnae, Mycobacterium sp., Vibrio mediterranei or co-infection of them [5][6][7][8][9][10][11]. Since 2016 the mortality has spread to all the coasts of Mediterranean countries, reaching France, Italy, Greece, Cyprus and other Mediterranean countries [8,[12][13][14][15][16]. Due to its massive decline (> 99.9% mortality in most sites), P. nobilis is now listed as "critically endangered" species according to the IUCN Red List [16]. ...
Article
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Background The pen shells Pinna nobilis and Pinna rudis are large wedge-shaped bivalve molluscs. Both species are threatened by different anthropogenic pressures. In the last few years, P. nobilis populations have significantly reduced due to massive mortality events. The complete mitochondrial DNA sequences of these congeneric species have been determined and compared for the first time. Results The mitogenome sequences of P. nobilis and P. rudis were 18,919 bp and 18,264 bp in length, respectively. Each mitogenome is composed of 12 protein-coding genes, 2 ribosomal RNA, 22 transfer RNA (tRNAs) genes and non-coding regions. A putative Adenosine Triphosphate synthase subunit 8 gene could only be proposed for P. nobilis. Both newly sequenced mitogenomes present a conserved gene order between them, comparable to the closely related Atrina pectinata, but global arrangement greatly differs from other available bivalve mitochondrial sequences. Multiple copies of tRNA-Cys were identified, located in different positions probably due to mechanisms of mitochondrial genome rearrangements, and detected 2 and 3 times in P. rudis and in P. nobilis, respectively. Conclusion A close relationship was shown between Pinna species and Atrina pectinata and a consistent clustering showing a monophyletic origin of Pinnidae family sequences was evidenced. The mitochondrial genomes will provide a valuable genetic resource for further studies on population genetics and species identification.
... According to an NGO representative: "To date, we still do not know the precise extent of the problem in the Mediterranean, and we need to understand it if we want to stay ahead of the parasite's arrival and save this species." Despite now knowing more, and that more than one pathogen is involved in the MME, numerous gaps and uncertainties remain [24,45,72]. ...
... The uncertainty in knowledge status for both species concerns a whole complex, including distribution, density, age structure, growth, reproduction and recruitment, amongst others (see for example, [20,36]). But it also concerns the threats against the species; in the case of Pinna, a lack of detailed knowledge about the MMEs, Haplosporidium and the conflating factors such as pollution or rising temperatures [24,72]. In the case of red coral, the main threats come from fishing impacts, particularly illegal fishing. ...
Article
Although there is a wide range of legislative support for marine environmental policy and management, existing and emerging pressures continue to threaten biodiversity and ecosystems. Recent ambitious policies have represented a paradigm shift, moving from the traditional hands-off preservation towards more active forms of intervention through ecosystem restoration, with explicit targets for restoration of degraded ecosystems (2020/2030 EU Biodiversity Strategy). This work analyses the discourses and uncertainties in the cases of the fan mussel Pinna nobilis and the red coral Corallium rubrum in the Mediterranean, through a literature review and expert interviews. The major discourses are placed within a restoration framework based on the degree of intervention and the underlying motivations. The major discourse for both of these emblematic threatened species is ecocentric-based ‘Putting Nature First’, set around passive restoration (low-level intervention with protective measures to reduce stressor impact). Emerging discourses resulting from coastal developments and mass mortality events for the mussel and overfishing for corals, has required active restoration, with on-going small-scale actions. Both species highlight comparable shortcomings and constraints concerning restoration, particularly facing unknown baselines (what to restore to) and multiple uncertainties (population status, diseases, co-stressors, and long-term success of restoration). The top-down policy restoration targets lack detail towards implementation and most restoration efforts to-date are local-scale through bottom-up personal motivations, that have not been meeting policy targets. Lessons learned include the need to scale up passive measures and to couple with increased levels of active intervention with clear ideas on what, why, how and where to restore.
... Recently, H. pinnae has been frequently recorded in association with other bacterial pathogens, making the MME scenario more complex than initially thought and far from being fully understood (Carella et al., 2020;Prado et al., 2020;Scarpa et al., 2020). In the Western Mediterranean, North Tyrrhenian Sea, Adriatic Sea and Aegean Sea, up to 100% mortality levels were recorded within monitored P. nobilis populations (Vázquez-Luis et al., 2017;Kersting et al., 2019;Acarli et al., 2020;Čižmek et al., 2020;Acarli et al., 2021;Betti et al., 2021;Katsanevakis et al., 2021), in contrast with P. rudis populations, which are not affected by H. pinnae (Catanese et al., 2018). ...
... In testimony of the ongoing P. nobilis MME (IUCN, 2021;Carella et al., 2020;Cabanellas-Reboredo et al., 2019;), we here provide the first instance of this phenomenon recorded in Maltese waters, in line with other Mediterranean national observations (Katsanevakis et al., 2019;Acarli et al., 2020Acarli et al., , 2021Čižmek et al., 2020;Zotou et al., 2020). The average P. nobilis individual density registered during the first monitoring survey conducted in 2006 was that of 1.8 individuals/100 m 2 (max. ...
Article
Full-text available
The genus Pinna includes two species in the Mediterranean Sea: Pinna nobilis and Pinna rudis. Both these species are under threat from multiple stressors. Pinna nobilis, in particular, has been exhibiting mass mortality events (MMEs) since 2016. The population and distribution of these species have never been comprehensively explored in the Maltese archipelago, and in this work, we collate information collected between 2006 and 2019 through a number of SCUBA underwater visual census monitoring programs. The logistical barriers surrounding SCUBA-based sampling techniques and the low-density distribution of these species constitute significant obstacles to an extensive conventional population assessment. Citizen science was thus also deployed in this study to supplement the data collected through SCUBA surveys: recreational SCUBA divers worked as citizen scientists, providing data on the distribution of these two endangered species from areas never explored before. This information can be used for assessing the conservation status of P. nobilis and P. rudis in Maltese waters, whilst contributing to the next generation of ocean-literate citizens.
... Signalée pour la première fois dans la région d'Alicante en Espagne (Darriba, 2017), l'épizootie s'est rapidement propagée vers l'est, touchant l'ensemble des côtes espagnoles, françaises et italiennes. Aujourd'hui, le bassin oriental est à son tour largement concerné au niveau de la côte est de l'Adriatique (Cizmek et al. 2020), de la Grèce Lattos et al. 2020 (Catanese et al. 2018 ;Vázquez-Luis et al. 2017 ;Cadene et al. 2018 ;Vicente 2020). ...
Article
Full-text available
Since 2016, the fan shell Pinna nobilis (L.1758) endemic species to the Méditerranean, is victim of an epizootic (parsitosis linked to an Haplosporidium), generalised to the whole Mediterraean basin. Protected at European level since 1992 (Directive 92/43/EEC), the species has recently been recognized as critically endangered on the world Red list of threatened Species of IUCN.In Occitania, the first cases of mortality were reported in 2018, in the area of Banyuls-sur-Mer. At present, some individuals resistant to epizzootic disease are observed in some Mediterranean lagoons. At the level of the Occitania region, well-known populations of the Thau lagoon have been monitored for several years. In this context of mass mortality, and in order to find out of these supposed « refuges » areas are also affected, observations campaingns have therefore carried out in May and June 2020 in the populations already identified. These new investigations show that the populations are healthy, with reduced mortality that seems natural, and regular renewal of these populations.
... Published data about P. nobilis population in Adriatic Sea offer only limited information about population ecology and genetics, and a recent study on animal health status are available [11][12][13][14][15][16][17]. Fisheries data and marine ecosystem surveys suggest that P. nobilis populations in the Adriatic Sea have been in decline, likely due to various anthropogenic and environmental influences such as habitat destruction (reduction of Posidonia oceanica meadow areas), illegal fishing, pollution, anchoring damage, invasive species, and climate change [18][19][20]. ...
Article
Full-text available
From May to October 2019, multiple mass mortality events (MMEs) of Pinna nobilis were observed along Croatian coastline starting from the south-east and rapidly progressing in north-western direction. Time dynamics of the MMEs closely followed general speed and direction patterns of surface sea-currents, advancing approximately 350 km in less than 3 months. Surveillance, clinical evaluation, and sample collection were performed on multiple sites with various degrees of mortality rates. Moribund P. nobilis individuals were collected and subjected to pathological, molecular, and microscopical investigation. Affected animals were positive for Mycobacterium in 70% of the individuals, and Haplosporidium pinnae was present in 58% of the cases. Observed pathological lesions were most severe where concurrent presence of both pathogens was confirmed (in 45.8% of moribund individuals). Moderate to strong lesions were observed in animals positive for Mycobacterium only (25% of cases), and lesions were absent or minor to moderate when only H. pinnae was confirmed (16% of cases). Considering the rapid and severe spread of the MMEs, the areas less exposed to major sea currents appeared to be at lower risk of pathogen transmission. Surveillance activities along the Croatian coastline identified several P. nobilis populations in such “lower risk” areas without apparent mortality or clinical symptoms. Such areas are of particular interest as source of potentially healthy individuals to support active recovery actions
... The implications of the presence of different pathogens in the development of the disease has still to be clarified. Most known and studied P. nobilis populations in the Western Mediterranean Sea have almost completely disappeared, with mortality rates exceeding 90% Panarese et al., 2019;García-March et al., 2020) and populations in the Eastern Mediterranean and Adriatic Sea are suffering the same fate Kersting et al., 2019;Cižmek et al., 2020;Öndes et al., 2020;Özalp and Kersting, 2020). There is the exception, however, of several sites with very specific environmental settings where P. nobilis populations remain unaffected to date: Fangar Bay (Delta del Ebro, Spain), Mar Menor (Spain), Rhône Delta (France), Etang de Thau (France), Diana and Urbino pools (Corsica, France), Venice lagoon (Italy), inner Kalloni Gulf (Greece) (Catanese et al., 2018;Cabanellas-Reboredo et al., 2019;Kersting et al., 2019;Simide et al., 2019;Prado et al., 2019;Foulquie et al., 2020;Zotou et al., 2020). ...
Article
Full-text available
A devastating mass mortality event (MME) very likely caused by the protozoan Haplosporidium pinnae first detected in 2016 in the Western Mediterranean Sea, is pushing the endemic bivalve Pinna nobilis to near extinction. Populations recovery, if possible, will rely on larval dispersal from unaffected sites and potential recolonization through recruitment of resistant juveniles. To assess the impact of the MME on the species’ larval recruitment, an unprecedented network of larval collector stations was implemented over several thousands of kilometers along the Western Mediterranean coasts during the 3 years after the onset of the MME. The findings of this network showed a generalized disruption in recruitment with dramatic consequences for the recovery of the species. However, there were exceptions to this pattern and recruits were recorded in a few sites where the resident population had been decimated. This hints to the importance of unaffected populations as larval exporting sources and the role of oceanographic currents in larval transport in the area, representing a beacon of hope in the current extremely worrying scenario for this emblematic species.
... This phenomenon has been investigated since the first mass mortality event occurred in the south-western Mediterranean coast of Spain, which caused mortalities in the local populations of fan mussel, whereas populations in the northern coasts seemed to be unaffected [29,30]. As causative agent for those mortalities is considered the protozoan parasite Haplosporidium pinnae which continued to devastate populations of fan mussel, P. nobilis in France, Italy, Tunisia, Turkey, Greece, reaching out one of the last safe shelters for the fan mussel in Croatia [22,[31][32][33][34][35][36]. Strong inflammatory responses were observed in all infestation cases caused by H. pinnae, leading to infiltrations in the digestive gland. ...
Article
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Mass mortality events due to disease outbreaks have recently affected almost every healthy population of fan mussel, Pinna nobilis in Mediterranean Sea. The devastating mortality of the species has turned the interest of the research towards the causes of these events. After the haplosporidan infestation and the infection by Mycobacterium sp., new emerging pathogens have arisen based on the latest research. In the present study, a metagenomic approach of 16S rRNA next generation sequencing (NGS) was applied in order to assess the bacterial diversity within the digestive gland of diseased individuals as well as to carry out geographical correlations among the biodiversity of microbiome in the endangered species Pinna nobilis. The specimens originated from the mortalities occurred in 2019 in the region of Greece. Together with other bacterial genera, the results confirmed the presence of Vibrio spp., assuming synergistic effects in the mortality events of the species. Alongside with the presence of Vibrio spp., numerous bacterial genera were detected as well, including Aliivibrio spp., Photobacterium spp., Pseudoalteromonas spp., Psychrilyobacter spp. and Mycoplasma spp. Bacteria of the genus Mycoplasma were in high abundance particularly in the sample originated from Limnos island representing the first time recorded in Pinna nobilis. In conclusion, apart from exclusively the Haplosporidan and the Mycobacterium parasites, the presence of potentially pathogenic bacterial taxa detected, such as Vibrio spp., Photobactrium spp. and Alivibrio spp. lead us to assume that mortality events in the endangered Fan mussel, Pinna nobilis, may be attributed to synergistic effects of more pathogens.
... Meanwhile, the detection of H. pinnae persisted in mortalities in the Ionian and Aegean Sea, having a great negative impact on populations of fan mussels and causing the change of the ranking of the species in the Mediterranean Sea to Critically Endangered according to the IUCN red list [15][16][17][18][19][20][21]. Both aforementioned pathogens have been detected in P. nobilis populations suffering from mortalities on Croatian coastlines, thus invading the last safe shelter of the species from the mortalities that occurred in the rest of Mediterranean Sea [22,23]. The only parasite-free area is the Sea of Marmara, which was recently referred as unaffected from the epidemic [24]. ...
Article
Full-text available
Pinna nobilis populations, constituting the largest bivalve mollusk endemic to the Mediterranean, is characterized as critically endangered, threatened by extinction. Among the various factors proposed as etiological agents are the Haplosporidium pinnae and Mycobacterium sp. parasites. Nevertheless, devastation of the fan mussel populations is still far from clear. The current work is undertaken under a broader study aiming to evaluate the health status of Pinna nobilis population in Aegean Sea, after the mass mortalities that occurred in 2019. A significant objective was also (a) the investigation of the etiological agents of small-scale winter mortalities in the remaining populations after the devastating results of Haplosporidium pinnae and Mycobacterium sp. infections, as well as (b) the examination of the susceptibility of the identified bacterial strains in antibiotics for future laboratory experiments. Microbiological assays were used in order to detect the presence of potential bacterial pathogens in moribund animals in combination with molecular tools for their identification. Our results provide evidence that Vibrio bacterial species are directly implicated in the winter mortalities, particularly in cases where the haplosporidian parasite was absent. Additionally, this is the first report of Vibrio mediterranei and V. splendidus hosted by any bivalve on the Greek coastline.
... Recently, many young individuals of P. rudis have been observed thanks to the strong recruitment event that occurred in summer 2017 Kersting et al., 2020b;the present work). This greater availability of P. rudis juveniles, has turned the species into the best model to conduct manipulative experiments on Mediterranean pinnids given the mass mortality events associated to a parasitic disease affecting exclusively P. nobilis (Catanese, 2020;Panarese et al., 2019). Using P. rudis to assay methodologies prior to their application to P. nobilis, a species that is presently endangered with extinction Kersting et al., 2020a), could help reducing fan mussel mortality during experimentation. ...
Article
A two-year growth study of 80 Pinna rudis individuals was conducted in offshore cages in the western Mediterranean Sea. A Von Bertalanffy growth model was fitted to monthly measured data of 40 individuals (Group 1), whereas length-dry weight relationship was established with the other 40 individuals (Group 2). Oceanographic data were sampled bimonthly. The individuals showed the fastest growth reported for a bivalve (1.32 mm/day). Temperature acted as the main factor controlling growth, which showed strong seasonality, but phytoplankton availability acted as a limiting factor during the warmest periods of year. These data will be useful to understand P. rudis ecology. Furthermore, the length-dry weight regression is proposed as a tool for captivity diet confection of the critically endangered species P. nobilis. Natural mortality was 0% during the study period.
... Since 2016, the population is under the thread of a parasite Haplosporidium pinnae which caused many mass mortalities recorded along the Mediterranean (Vázquez-Luis et al., 2017). Greece, Italy, Croatia, Turkey, Tunisia, France and Morocco are the Mediterranean countries that have reported mass mortality (Acarli et al., 2020a;Čižmek et al., 2020;Šarić et al., 2020;Öndes et al., 2020;Zotou et al., 2020;Betti et al., 2021;Acarli et al., 2022a). International Union for Conservation of Nature (IUCN) has changed the status of P. nobilis as Critically Endangered Species (Kersting et al., ). ...
Article
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In August 2020, a total area of 38000 m 2 around Gökçeada has been scanned to determine the current population status of Pinna nobilis. 9 stations (Yıldızkoy, Manastır, Marmaros, Gizli Liman, Laz Koyu, Kapıkaya, Karaçavuş, Karaçavuş shore and Kefalos) have been detected by means of SCUBA and ABC diving techniques. All specimens were found dead (total mass mortality of 100%). The total length range of P. nobilis was between 30.8-38.3 cm.
... Published data about P. nobilis population in Adriatic Sea offer only limited information about population ecology and genetics, and a recent study on animal health status are available [11][12][13][14][15][16][17]. Fisheries data and marine ecosystem surveys suggest that P. nobilis populations in the Adriatic Sea have been in decline, likely due to various anthropogenic and environmental influences such as habitat destruction (reduction of Posidonia oceanica meadow areas), illegal fishing, pollution, anchoring damage, invasive species, and climate change [18][19][20]. ...
... The pen shell Pinna nobilis, endemic to the Mediterranean Sea, has been suffering from a highly infective and lethal water-borne disease, caused primarily by the sporozoan parasite Haplosporidium pinnae and several pathogenic bacteria, since late 2016 (Vázquez-Luis et al., 2017;Catanese et al., 2018;Cabanellas-Reboredo et al., 2019;Katsanevakis et al., 2019;Panarese et al., 2019;Carella et al., 2020;Scarpa et al., 2020). The majority (>90%) of Mediterranean populations of P. nobilis have been affected by the disease, with mass mortality events reported in both the western and eastern parts of the Mediterranean Sea (Vázquez-Luis et al., 2017;Katsanevakis et al., 2019;Kersting et al., 2019;Öndes et al., 2020;Čižmek et al., 2020). This disease has devastated the P. nobilis populations in the region, leading IUCN to categorize it as a critically endangered species (Kersting et al., 2019). ...
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A spring 2021 cruise to the south Marmara Islands revealed a mass mortality event of Pinna nobilis, which had been reported to be healthy just seven months ago. The cause of death might be associated with an epidemic disease or a catastrophic mucilage event seen after November 2020 in the Sea of Marmara. A total of 191 Pinna nobilis individuals were found at seven stations, of which 88% were dead. The population density (including dead and alive individuals) of P. nobilis was found to be between 0.3 ind.100 m-2 and 12 ind.100 m-2 in the area. A total of three live and four dead juvenile individuals were observed in the area, indicating low recent recruitment. The largest number of dead Pinna nobilis individuals was encountered in shallow waters (0-4 m depth). A total of 34 species, belonging to six taxonomic groups (Sipuncula, Oligochaeta, Polychaeta, Crustacea, Mollusca and Pisces), were found within the dead shells of four P. nobilis individuals. The mass mortality of Pinna nobilis in the Sea of Mar-mara, the last remaining disease-free sea, indicates the necessity of establishing and implementing emergency action plans for this species, including ex-situ conservation.
... Limiting factors for this emerging 'Enhancing Pinna' governance arrangement are scientific understanding of the MME and impacts on suitable areas and last refugia, breeding, settlement and abiotic factors (Čižmek et al., 2020;Prado et al., 2020;Šari c et al., 2020;Zotou et al., 2020), nursery know-how, but also public support (although support from diver citizen scientists has been reported; Cabanellas- ...
Article
A new motivation for marine restoration has been observed, associated with the dissatisfaction with current marine restoration governance arrangements (MRGAs). An MRGA consists of alliances of public and private actors (coalitions) who, through their common conceptualisation of the problem (discourses), try to influence and design marine restoration activities while considering the rules of decision-making, and the management of limited resources. Emerging MRGAs rise in parallel to existing ones and aim to contribute to the same goals or show another way of reaching those goals. This phenomenon raises questions of legitimacy both for the emerging and the existing arrangement. Building on existing literature, this paper proposes an analytical framework to simultaneously explore input, throughput and output legitimacy as three essential pre-conditions of legitimacy for MRGAs. The framework is tested in three European cases of MRGAs that were part of the European Union MERCES project (http://www.merces-project.eu/). Analysis showed that actors who are influential in achieving restoration goals, and also those who are impacted by restoration actions, should be involved in the MRGAs (input legitimacy); actors within MRGAs should establish and follow procedures for decision-making that are both transparent and clear (throughput legitimacy); and actors within MRGAs need to establish a common understanding of restoration, of the goal to reach and of the related uncertainties (output legitimacy). Awareness of these pre-conditions allows actors internal and external to MRGAs to address aspects that give legitimacy to restoration actions. It also creates a language that allows actors to engage in discussion on legitimacy that goes beyond the mere application of the rule of law.
... lithophaga, P. nobilis, P. rudis and P. dactylus) are included in Annex II of the Barcelona Convention as endangered or threatened species (Barcelona Convention, 1976). Since 2016, P. nobilis has been undergoing mass mortality, an event documented in whole Mediterranean, due to infection caused by the haplosporidan parasite Haplosporidium pinnae (Cabanellas-Reboredo et al., 2019;Čižmek et al., 2020). Species mortality rates often reach 100% across the Mediterranean (Vázquez-Luis et al., 2017;Catanese et al., 2018;Katsanevakis et al., 2019;García-March et al., 2020). ...
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This paper presents an updated inventory of marine bivalves of Montenegro. The checklist based on published literature and recent research includes 165 taxa. Eleven taxa are recorded here for the first time in Montenegrin coastal waters. Six species are non-indigenous, while one is crytogenic. Two species (Lithophaga lithophaga and Pinna nobilis) are additionally listed in Annex IV of the Habitat Directive and are therefore protected fauna species in Montenegro. Three species are strictly protected according to the Bern Convention (Appendix II), while four species are endangered or threatened according to the Barcelona Convention (1976, Annex II). Pinna nobilis is considered to be Critically Endangered due to mass mortality. Finaly, as Thyasira orahovaziana is a questionable taxon as its validity is uncertain (taxon inquirendum) it is excluded from the checklist, as well as the taxa Spaniorinus reconditus which is extinct and Mytilus edulis, whose occurrence in Montenegrin coastal waters is uncertain.
... The species is now included as "critically endangered" in the IUCN Red List [4] and as endangered with extinction in Spanish coasts (Orden TEC/596/2019, de 8 de abril). The MME has been mainly associated to the presence of pathogens such as: the parasite Haplosporidium pinnae [5][6][7] , Mycobacterium sp . [ 8 , 9 ], Vibrio spp . ...
Article
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The pen shell Pinna nobilis is critically endangered due to a disease that has affected all open water populations since late 2016. Collection of early spats is considered a fundamental step for pen shell conservation. However, the identification between P. nobilis and P. rudis juveniles by morphology is a very difficult task. Furthermore, due to the small size of juveniles and high sensitivity to handling, the sampling for this purpose must not damage individuals. As a consequence, the application of molecular techniques for conservation strategies to identify threatened and endangered bivalve species is every day more and more necessary. In this study, we present the development of a multiplex-PCR procedure for the rapid identification of two Pinna species from eDNA water samples. Using species-specific primers, designed in the rRNA16S and rRNA12S mitochondrial genes, identification of species was obtained by cellular or extracellular DNA dissolved in water and differentiated based on the size of the amplified DNA fragments. • Development of a molecular multiplex-PCR procedure for the rapid identification of two Pinna species from eDNA water samples • Using specie-specific primers, the different species can be differentiated basing on the size of the amplified DNA fragments • This technique removes many of the limitations commonly associated with sampling of threatened and endangered juvenile bivalves for conservation strategies (sampling does not damage individuals).
... Mass mortalities of the P. nobilis populations reaching up to 100% occurred along the Mediter- Katsanevakis, 2019), Dardanelles Strait (Öndes et al., 2020b;Özalp & Kersting, 2020;Acarlı et al., 2021), Bosnia and Herzegovina (Čelebičić et al., 2020), and even the Sea of Marmara (Öndes et al., 2020b; Çınar et al., 2021a; Çınar et al., 2021b). The findings indicated that mass deaths were commonly caused by H. pinnae (Darriba, 2017;Vázquez-Luis et al., 2017;Catanese et al., 2018;Čižmek et al., 2020). According to recent research, deaths also seem to occur due to co-infection of the protozoa with bacteria such as Mycobacterium sp. or Vibrio sp. ...
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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 regions, 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.
Chapter
The fan mussel (or pen shell), Pinna nobilis, is an emblematic large bivalve, endemic to the Mediterranean Sea. Due to various anthropogenic impacts, its populations had substantially decreased the last century, which led to its strict protection by international and national legislative instruments since the 1990s. Since 2016, P. nobilis has been suffering from mass mortality due to a pathogen infection, which devastated its populations. Currently, the species has become locally extinct in most of its previous range and has therefore been flagged as Critically Endangered by IUCN's Red List in 2019. Surviving populations persist only in a few scattered lagoons or enclosed bays and in the Sea of Marmara, which is still unaffected. Substantial efforts have been made since 2016 by the scientific community for the in situ and ex situ conservation of the species. Although, these have not yet proven fully successful, there has been substantial progress in efforts to breed the species in captivity and to understand the dynamics of the pandemic, as well as in disentangling the role of unaffected populations for potential recovery. The following years seem to be critical for the survival of the species. By further strengthening collective efforts there is still hope that the species can be saved from extinction.
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Pinna nobilis is a large bivalve endemic to the Mediterranean Sea that lives in shallow coastal areas. Due to its size and relatively fast shell growth rates, it is an interesting taxon for high-resolution study of nitrogen isotopes of carbonate bound organic matter (δ ¹⁵ N CBOM ). In this study we tested if P. nobilis shells can be used as an indicator of the nitrogen isotope baseline of the system, if it can provide high-resolution data on environmental δ ¹⁵ N variability, and if the chemical properties of the shell and biomineralization process change in response to mass mortality events spreading in the Mediterranean. Shells were opportunistically collected during 2019 and 2020 by skin diving, as a part of a project on mortality monitoring, from four shallow coastal localities in the eastern Adriatic. Shell powder for δ ¹⁵ N CBOM analysis was collected by milling sample swaths from the internal (low-resolution) and external (high resolution) shell surface. Significant differences in δ ¹⁵ N CBOM , obtained from the internal shell surface, were observed between sampling localities with different anthropogenic influences, with lowest values (∼3–4‰) recorded for shells obtained from Pag Bay, and highest (∼6–8‰) for shells sampled in Lim and Kaštela Bays. High-resolution samples from the external shell surface of Pinna nobilis showed spatial and temporal variations in δ ¹⁵ N CBOM values, with temporal resolution of 1–3 weeks. High-resolution δ ¹⁵ N CBOM data obtained from the shell Kas1 corresponded to a time interval from spring 2018 to summer 2019 and had a pronounced increase of δ ¹⁵ N CBOM values closest to the shell margin coupled with a decrease in δ ¹³ C shell values, indicating that this animal was experiencing stressful conditions several months prior to its death. According to our findings, δ ¹⁵ N CBOM values from P. nobilis shells can serve as an indicator of the isotopic baseline of the ecosystem potentially as a powerful tool to study bivalve physiology.
Chapter
In this study, the comparative results of the fan mussel Pinna nobilis larvae collection during 3 years (2016–2019) on the sites of the Montenegrin Adriatic coast and the Western Mediterranean, France are presented. In both countries, growth studies of collected fan mussel juveniles were carried out as well. After 1 year growth measurement of P. nobilis recruits in their natural habitat on the site Dobrota, Montenegro, mean shell length was 198.58 ± 17.77 mm for the recruits from Sv. Nedjelja and 206.73 ± 16.40 mm for the recruits collected from Ljuta. The growth study carried out in a laboratory tank in France indicated that the mean shell length of P. nobilis recruits after a 9 month period was 100.50 ± 7.59 mm for the recruits from Bomasse, 96.33 ± 11.06 mm from Basse Renette 1, and 95.75 ± 8.45 mm for recruits from Basse Renette 2, respectively. In spite of much larger mean shell lengths obtained in Montenegro, mean monthly growth rate of P. nobilis recruits bred in France was higher due to more stable conditions and access to food within the tank in contrast to variations of environmental parameters in their natural habitat. We have presented first data on P. nobilis recruitment and growth in Montenegro and showed higher growth rate in comparison with the other sites in the Adriatic Sea and Mediterranean. It was shown that the temperature is of high importance for the growth rate of P. nobilis juveniles in their natural habitat due to lower growth during winter. Anthropogenic pressure was the main obstacle for development of P. nobilis populations during the study period, while biological pollution as the main threat for P. nobilis survival will be the subject of further studies in the Montenegrin Adriatic coast.
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A total of 12 Pinna nobilis beds were found and studied at depths 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), 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.
Conference Paper
The aim of the paper is to present preliminary shellfish community data on shellfish larvae mesh bag collectors placed at three locations in the ecological network – Natura 2000 Cetina estuary (HR3000126) with several replicas at different depths at 2, 4, 6, 8 and 10 m. Larvae mesh bag collectors were set up to collect long-lived, strictly protected and critically endangered, Mediterranean endemic bivalve Pinna nobilis Linnaeus 1758. The experiment was set up in June 2020 and after five months of immersion the presence of 11 families with 16 bivalve species was established with one juvenile individual of Pinna nobilis total of 12mm in length.
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After the mass mortality events of Pinna nobilis L. occurred in the neighboring Croatia, and conservation status of this species was changed in the IUCN Red List to critically endangered (CE), a survey was conducted to determine whether this emerging disease had spread to Bosnia and Herzegovina (B&H). A site of 1.4 HA, located at the north side of the Neum bay, was investigated. All populations found had 100% mortality rate. Furthermore, there was absence of juveniles and younger individuas. Irregularities in the age structure and density of dead populations found are the signs of certain environmental pressures on this species for a long time. The results indicate that the situation is serious and requires a systematic approach of all competent institutions for the conservation of this species.
Article
Since early autumn 2016, Mass Mortality Events (MME) have drastically impacted the population of the fan mussel Pinna nobilis in the Mediterranean Sea. Haplosporidium pinnae, a newly described Haplosporidian species, has been considered the causative agent of the mortality outbreaks in association to opportunistic bacterial pathogens. In the present study, we first reported a cytological description of H. pinnae in moribund specimens of P. nobilis which were collected in the Gulf of Taranto (Ionian Sea, Italy) during summer 2018. Different life-cycle stages of the parasite, including uni- and binucleate cells, small plasmodia, big multinucleate plasmodia and sporocysts with spores, were detected in all the examined animals and most of the parasite cells were present in gills, mantle and digestive gland, while the spores were found only in the latter organ. Histology and molecular biology were also performed, confirming the nature of the infectious agent, as already reported in the area. Additionally, molecular study revealed the presence of the Mycobacterium ulcerans - M. marinum complex but no evident macroscopical or microscopical lesions, just as no bacteria referred to Mycobacterium were observed. In conclusion, the present study aimed to provide further contributions to the understanding of the mortality of P. nobilis, pointing on the role of the cytological method of investigation both for diagnostic and epidemiological purposes, and discussing about the current epidemic situation in the Adriatic sea.
Preprint
The dramatic Mass Mortality Event, MME, of Pinna nobilis populations initially detected in 2016 in the western Mediterranean basin, has also spread rapidly to the central and eastern basin. Unfortunately, there is still a significant lack of information on the status and health of P. nobilis , since only a fragmentary picture of the mortality rate affecting these populations is available. Regarding the Italian coast, several surveys have given only localized or point-like views on the distribution of species and the effect of the MME. Therefore, for the first time, this study investigated P. nobilis densities, distribution and mortality in 164 surveys covering a total of 800 km along the southeast coast of Italy (Apulia region). The geographical scale of this investigation made it the largest ever conducted in Italy, and this was achieved through a rapid and standardized protocol. No live individuals were observed along the 92 km linear transects, allowing us to assess that the P. nobilis populations had totally collapsed, with a mortality rate of 100% in Apulia. The distributional pattern of the species showed a strong overlap with seagrass meadows on meso and macro geographical scale, however this was not the case on a micro scale. This result indicates that although there is a relationship between P. nobilis and seagrass meadows, it is not limited to the habitat patch but crosses the boundaries of seagrass. This observation led us to the conclusion that the distribution of P. nobilis shows a trophic link through the cross-boundary subsidy occurring from seagrass meadows to the nearby habitat, by means of the refractory detrital pathway.
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A mass mortality event (MME) affecting the fan mussel Pinna nobilis was first detected in Spain in autumn 2016 and spread north-and eastward through the Mediterranean Sea. Various pathogens have been blamed for contributing to the MME, with emphasis in Haplosporidium pinnae, Mycobacterium sp. and Vibrio spp. In this study, samples from 762 fan mussels (necropsies from 263 individuals, mantle biopsies from 499) of various health conditions, with wide geographic and age range, taken before and during the MME spread from various environments along Mediterranean Sea, were used to assess the role of pathogens in the MME. The number of samples processed by both histological and molecular methods was 83. The most important factor playing a main role on the onset of the mass mortality of P. nobilis throughout the Mediterranean Sea
Thesis
Les systèmes marins côtiers sont généralement discontinus et constitués d’une mosaïque de paysages sous-marins différents, créant ainsi des distributions parfois très fragmentées chez les espèces qui les colonisent. Les espèces marines côtières sont donc structurées en réseaux de populations connectées entre elles via la dispersion larvaire. Comprendre le fonctionnement et la connectivité entre les populations d’une espèce est indispensable pour adapter les stratégies de conservation. La grande nacre, Pinna nobilis, est une espèce endémique de la mer Méditerranée qui fait aujourd’hui face à une crise majeure qui menace sa survie. Depuis Octobre 2016, des mortalités de masse sont signalées sur ses populations, à travers toutes la mer Méditerranée, causées par un protozoaire parasite, Haplosporidium pinnae. Il s’agit d’un évènement sans précédent, que ce soit par le taux de mortalité (près de 100 %) ou la vitesse de propagation, et qui pourrait conduire à l’extinction de l’espèce. En se focalisant sur le littoral Occitan, cette thèse apporte des connaissances sur la biologie et l’écologie de l’espèce mais aussi sur son fonctionnement et les processus qui permettent le maintien de ses populations afin de proposer des priorités de conservation. Ainsi, nous avons mis en évidence la diversité d’habitats colonisés par l’espèce ainsi que l’importance des lagunes car elles abritent près de 90 % des grandes nacres, sur le littoral Occitan, et semblent servir d’habitat refuge à l’espèce en limitant l’infestation par le parasite. A l’aide de marqueurs microsatellites nouvellement développés, nous avons montré une structure génétique très homogène sur toute la côte, ce qui implique un certain niveau de connectivité et laisse penser qu’une grande partie de la diversité génétique de l’espèce reste préservée dans les lagunes. En se focalisant sur la population de la baie de Peyrefite, dans la Réserve Naturelle Marine de Cerbère-Banyuls, et grâce à une analyse de parenté, nous avons apporté des connaissances sur la dynamique démographique et les processus de repeuplement de l’espèce. L’ensemble de cette thèse permet de définir des recommandations qui seront utiles à la mise en place de mesures de conservation adaptées, indispensables pour la survie de l’espèce.
Article
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A non-invasive laser fiber-optic method based on infrared sensors for heart rate (Hr) recording was applied to assess the physiological condition of Pinna nobilis. During 2017, the specimens of P. nobilis were sampled at three sites within the Boka Kotorska Bay, Montenegro and used for ex situ experiments with short-term reduction/restoration of ambient salinity to evaluate their physiological adaptive capacity based on heart rate recovery time (Trec). Mean Trec for specimens from Sv. Nedjelja (reference site), Dobrota and Sv. Stasije were 72 ± 3, 91 ± 7 and 117 ± 15 min, while the coefficients of variation (CV) were 0.12, 0.13 and 0.17, respectively. Resting heart rate (Hrrest) and Trec showed statistically significant differences between the groups of mussels from Dobrota and Sv. Stasije in comparison to the reference site. Statistically significant correlations were observed between Trec and shell length/width, which was not the case in comparison between Hrrest and shell length/width. The lower adaptive capacity within the P. nobilis specimens from Dobrota and Sv. Stasije in comparison to the reference site could occur due to stress induced by deterioration of environmental conditions, which could have led to impairment of the physiological state of the mussels evaluated by Hr. All the specimens of P. nobilis survived the experimental treatments; afterwards, they were successfully transplanted at the Dobrota site. The experimental unit with sensor technology applied in this study can provide Hr recording in real time and could have an application in monitoring the physiological/health state of P. nobilis individuals maintained in aquaria.
Article
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Following the Mass Mortality Events (MMEs) of the pen shell P. nobilis in Campania region and Sicily, a survey of moribund P. nobilis specimens was also conducted in other Italian regions (Campania, Tuscany, Sardinia, and Apulia) and Spain (Catalunya). Histopathological and molecular examination of 27 specimens of P. nobils revealed different types of pathogens associated with tissue lesions, morbidity and mortality. Presence of Mycobacterium, Vibrio species, Haplosporidium pinnae and Perkinsus sp. were detected, differently distributed into the areas. The Mycobacterium sp., previously reported in Campania and Sicily samples, was observed in all the analyzed areas and individuals, associated to systemic inflammatory lesions. In Spain, H. pinnae was observed in 36% of cases, always associated to the Mycobacterium sp. Molecular study using hsp65 genes and Internal Transcriber Spacer ITS support that a new species of Mycobacteria is infecting P. nobilis, close to M. triplex and belonging to the group of M. simiae complex with M. sherrisi. Presence of Perkinsus spp. resembling P. mediterraneus was observed in 2 out of 13 Italian individuals whose presence should be addressed as potential risk for shellfish aquaculture of the area. Vibrio spp. were also detected in some case. The preliminary results of this study suggest that Mycobacterium sp., Vibrio spp., H. pinnae and Perkinsus sp. cooperate to disease pathogenesis, being Mycobacterium and Haplosporidium most of the time involved. Vigilant inspection of those areas where MME is now starting, along with continuous systematic surveys, are crucial to define the spatiotemporal progress of mortality and the role of every single pathogen in the disease outcome.
Article
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A major epizootic event attributed to Haplosporidium pinnae leading to 100% mortality of Pinna nobilis L. populations along Mediterranean coastlines started in the fall of 2016. As a result, a project to rescue 221 adult individuals of the endangered pen shell, Pinna nobilis was conducted in November 2017 in the two areas of the Spanish coast where the species was still abundant and apparently free from infection by H. pinnae: Port Lligat in the Costa Brava, and the Alfacs Bay in the Ebro Delta. For biosecurity reasons, the 106 individuals from the Ebro Delta were stabled at the IRTA facilities located next to Alfacs Bay, whereas the 115 individuals from Port Lligat were stabled in different institutions throughout the Spanish territory. Initial biopsies showed that individuals from the Ebro Delta were free of the parasite, whereas most individuals from Port Lligat were already parasitized and died in the following months. Individuals at IRTA were hold in five tanks and fed ca. 4% of their dry weight with a mix of three species of phytoplankton and fine riverine sediments (13% OM). Seawater was filtered through 10, 5 and 1 μm to ensure the absence of the parasite and disinfected with UV light. No individuals died during the 4 initial months of captivity, but two died in April–May at temperatures from 17 to 19 °C. A peak of mortalities occurred during the summer months and early fall (53%) with maximums coinciding with temperatures above 25 °C. Individuals were again analyzed by PCR and histology for the presence of H. pinnae, Mycobacteria sp., and other locally important pathogens of commercial bivalves (Vibrio splendidus, V. aestuarianus and Herpesvirus OsHV-1 microVar), and therefore considered as potential pathogens of pen shells. However, with the exception of 3 individuals that were positive for Mycobacteria sp., results were all negative for the studied pathogens. Microbiological culture and isolation of bacteria from three moribund individuals, sacrificed for study purposes, showed V. mediterranei as the dominant species, and further PCR analyses confirmed the presence of the bacterium in ten deceased individuals. Overall, our results suggest the V. mediterranei is an opportunistic pathogen of stabled individuals possibly subjected to stress from captivity, and that antibiotic treatment (Florfenicol) combined with vitamins and mineral supplementation and reduction of water temperature (15 to 18 °C), can be used to mitigate (not to eradicate) the disease. Further research is needed to determine diets and stabling conditions that minimize captivity stress and prevent the emergence of the disease.
Article
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The pen shell, Pinna nobilis L., is a critically endangered bivalve threatened by mass mortality events throughout the Mediterranean, but the Alfacs Bay (Ebro Delta) still hosts many healthy individuals. Herein, we study the main factors controlling recruitment patterns in this locality, including gonadal development and abundance of critical life-stages, as well as the effect of environmental factors. Growth records from empty shells suggested a single major peak of recruitment during a period of 11 years, although many juveniles were found in two very shallow sand bars possibly acting as a barrier for water circulation and as a trap for larvae. Collectors deployed outside these sand bar areas showed zero settlers, and the availability of planktonic larvae was very low. Gonadal examination evidenced breeding throughout the summer period with successive hermaphroditism, but 20% of individuals were simultaneous hermaphrodites, a condition that has been associated with environmental stress and that could lead to in-breeding depression and potentially reduced fertility. Yet, given the large size of the population and the wide breeding period observed, planktonic processes causing larval mortality such as freshwater discharges from rice locally important rice agriculture are also proposed as possible impacts accounting for patterns of low larval availability.
Article
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A mass mortality event is devastating the populations of the endemic bivalve Pinna nobilis in the Mediterranean Sea from early autumn 2016. A newly described Haplosporidian endoparasite (Haplosporidium pinnae) is the most probable cause of this ecological catastrophe placing one of the largest bivalves of the world on the brink of extinction. As a pivotal step towards Pinna nobilis conservation, this contribution combines scientists and citizens’ data to address the fast- and vast-dispersion and prevalence outbreaks of the pathogen. Therefore, the potential role of currents on parasite expansion was addressed by means of drift simulations of virtual particles in a high-resolution regional currents model. A generalized additive model was implemented to test if environmental factors could modulate the infection of Pinna nobilis populations. The results strongly suggest that the parasite has probably dispersed regionally by surface currents, and that the disease expression seems to be closely related to temperatures above 13.5 °C and to a salinity range between 36.5–39.7 psu. The most likely spread of the disease along the Mediterranean basin associated with scattered survival spots and very few survivors (potentially resistant individuals), point to a challenging scenario for conservation of the emblematic Pinna nobilis, which will require fast and strategic management measures and should make use of the essential role citizen science projects can play.
Article
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Disease is an increasing threat for marine bivalves worldwide. Recently, a mass mortality event (MME) impacting the bivalve Pinna nobilis was detected across a wide geographical area of the Spanish Mediterranean Sea and linked to a haplosporidian parasite. In 2017–2018, mass mortality events affecting the pen shell Pinna nobilis were recorded in two different regions of Italy, Campania and Sicily, in the Tyrrhenian Sea (Mediterranean Sea). Histopathological and molecular examinations of specimens showed the presence of Haplosporidium sp. in only one specimen in one area. Conversely, in all of the surveyed moribund animals, strong inflammatory lesions at the level of connective tissue surrounding the digestive system and gonads and linked to the presence of intracellular Zhiel-Neelsen-positive bacteria were observed. Molecular analysis of all of the diseased specimens (13) confirmed the presence of a Mycobacterium. Blast analysis of the sequences from all of the areas revealed that they were grouped together with the human mycobacterium M. sherrisii close to the group including M. shigaense, M. lentiflavum and M. simiae. Based on pathological and molecular findings, it is proposed that a mycobacterial disease is associated with the mortality episodes of Pinna nobilis, indicating that, at this time, Haplosporidium sp. is not responsible for these events in Campanian and Sicilian waters.
Article
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Noble pen shell or fan mussel, Pinna nobilis Linnaeus (1758), protected since 1992, was incorporated into the Spanish Catalogue of Threatened Species (Category: Vulnerable, Royal Decree 139/2011). The status is presently in the process of being catalogued as critically endangered, pending approval by Spanish Government (https://www.mapama.gob.es/es/biodiversidad/participacion-publica/Borrador_OM_situacion_critica.aspx). The International Union for the Conservation of Nature (IUCN) alerted the countries of the Mediterranean basin to the “emergent situation” due to serious mortality events suffered by the fan mussel, putting it in serious risk of extinction. Thus, emergency actions have been implemented by Spanish authorities in which several research institutes from all over the country are involved. The parasite, Haplosporidium pinnae, was recently characterized by histology, TEM, SEM and molecular biology techniques and it was considered responsible for the mass mortality of P. nobilis in the Mediterranean Sea. In this context, the aim of this study has been to develop species-specific quantitative PCR (qPCR) protocol carrying out a fast, specific and effective molecular diagnose of H. pinnae. In this sense, the detection limit for qPCR was equal to 30 copies of SSU rDNA / ng of DNA using plasmid alone and when 100ng DNA of non-infected oyster were added. The qPCR assay revealed that 94% of the 32 analysed mantle tissues of fan mussel were infected by H. pinnae, showing a high sensitivity and specificity for its detection (100% if we don't consider negative and too much degraded samples). This technique will allow us to make quicker follow-ups of the disease, allowing us to get a better understanding of its evolution in order to help in the rescue of P. nobilis populations
Article
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The cryptogenic parasite Haplosporidium pinnae has caused mass mortality of the protected endemic Mediterranean bivalve Pinna nobilis in the western Mediterranean, since the autumn of 2016. Herein, we confirm the spread of the parasite in the eastern Mediterranean, and report a mass mortality event, with > 93% average mortalities, in the coastal waters of Lesvos Island (Greece, Aegean Sea). Histopathological study of collected specimens revealed the presence of a haplosporian-like protozoon in different life cycle stages, mainly within the digestive gland of the infected Pinna nobilis, with many uni- and bi-nucleate parasite cells, plasmodia and sporocysts in the wide lumen of digestive tubules causing the collapse of epithelial cells, and apparently low host haemocyte reaction. The parasite was identified as H. pinnae by molecular methods (PCR amplification and sequencing of a part of small subunit ribosomal DNA gene, and comparison with available records in Genbank). In many sites, 100% mortality was recorded, whereas in a single site (among 13 surveyed sites) mortality was relatively low (36%), successful recruitment was observed and the parasite was not detected. The latter observation stresses the importance of possible parasite-free refugia sites. We call for continuous monitoring of the spread of the parasite and its impacts, and for urgent targeted research and actions to identify the factors affecting the parasite’s virulence, investigate biotic and abiotic conditions that characterize refugia sites, and strictly protect the remaining P. nobilis populations to increase the chances for the survival of the species.
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The Adriatic Sea differs sharply from the Tyrrhenian Sea and the rest of the Mediterranean in its hydrographic and hydrobiological characteristics. Three different areas can be distinguished: the Northern, the Central and the Southern Adriatic. The first shows the most accentuated peculiarities: maximum depth does not exceed 40 meters, temperature may fluctuate between 5°C and 28°C during the year, salinity is highly variable, and tides may rise higher than 1 m. Organic matter input from rivers, and the resulting nutrient enrichment, leads to elevated primary productivity, particularly in the Northern and the Central Adriatic. Both the circulation and distribution of water masses in the Adriatic Sea are strongly influenced not only by the morphology of the three basins but also by the fresh water inflow of continental origin. In the Tyrrhenian Sea the continental shelf extends only for a relatively short distance. The depth exceeds 2000 m throughout virtually the whole of the basin, with a maximum depth of 3840 m. Input from the continental waters is minimal so salinity remains constant at roughly 38 PSU. In winter the Tyrrhenian Sea maintains a constant temperature of about 13°C, while in summer the temperature is around 23-24°C. The mean value of primary productivity is much lower than in the Adriatic. The surface Atlantic current feeds a cyclonic gyre with a southern branch entering between Sardinia and Sicily and moving in a northeasterly direction, and the other towards the southwest. Levantine intermediate waters penetrate mainly through the strait of Sicily at a depth ranging between 300 and 400 m. A clear distinction between coastal and off-shore habitats is found only in the Southern Adriatic where the bottom drops to considerable depths. Particularly significant is the beachrocks habitat enclosed within the surrounding soft bottom. Bathial fauna are found only in the Southern Adriatic. The extensive coastal lagoons are of considerable ecological and biogeographic interest. Several endemisms are known, some of sarmatic origin. Only the Central and Southern Adriatic are characterised off-shore by an oceanic planktonic community. The Northern Adriatic is characterised by neritic plankton throughout its extension. Production of nanoplankton is dominant. In the Tyrrhenian Sea the hard bottom communities are amongst the most important of the whole Mediterranean. Of particular interest are the 'trottoir' and the coralligenous formations typical of the Tyrrhenian Sea which can develop on rocky and sandy bottoms at depths ranging between 20 and 1230 m. Zooplankton shows some characteristics that distinguish it from other areas of the Western Mediterranean. Abyssal fauna is present in the centre of the basin although it is considerably poorer than that of the Atlantic. Along the coast of both seas there are important ports and numerous large urban centres whose population is substantially increased during the tourist season. The numerous industrial complexes co-exist with intense agriculture and animal-rearing activities. Maritime traffic is intense. The most important fishing ports are in the Central and Southern Adriatic and aquaculture is highly developed. In the Adriatic natural gas reserves and oil fields lie along the Italian coast: there are 70 off-shore platforms, and oil or gas flows to the mainland through pipelines. Water quality is impaired by a number of factors, particularly the excessive quantity of nitrogen and phosphorus. On the Tyrrhenian sea floor, several areas of interest for mineral extraction have been identified. The presence of cinnabar mines in Tuscany has increased the levels of mercury in the water and sediment in the Northern Tyrrhenian. Other metals are also present in considerable concentration in the waters of the Southern Tyrrhenian due to underwater volcanic activity. Both the Adriatic and Tyrrhenian have been included within the framework of protective measures set up on the basis of international conventions. Considerable progress has been made in designing waste purification technology and measures designed to establish protected marine areas are already in place. Interdisciplinary research developed in the universities and in various research centres has long been a driving force and has made a crucial contribution to knowledge of oceanography and marine biology. Proposals based on data concerning the current ecological situation have also been put forward, aimed at water clean-up and improving fishery production.
Article
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The pen shell Pinna nobilis (also known as the fan mussel) is an endemic bivalve of the Mediterranean Sea. Threatened by human activities, it has been listed as an endangered and protected species under the European Council Directive 92/43/EEC since 1992. The ecological role of this species is of importance because it filters and retains large amounts of organic matter from suspended detritus contributing to water clarity. In addition, as a hard substrate in the soft-bottom seafloor, it provides a surface that can be colonized by other (floral and faunal) benthic species. Here, we provide an overview of all available published studies on the pen shell, compiling available data and summarizing current knowledge on the conservation status and viability of populations over the full range of the Mediterranean Basin. Additionally, we discuss the different practices in applied methodology and identify gaps and new research areas in order to render conservation programmes of the species more effective. © 2015 Elsevier Ltd. All rights reserved.
Article
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A population of the fan mussel Pinna nobilis Linnaeus, 1758 (molluscan, Bivalvia) has been studied since 1969 at Port-Cros Island (Port-Cros National Park, Provence, France, Mediterranean Sea). This population dwelt on a substrate constituted of dead rhizomes of the seagrass Posidonia oceanica (“dead matte”) covered by coarse sand, between 10 and 38 m depth. 122 individuals were studied (census and biometry) within the framework of a long term monitoring programme. The population probably originated in a single cohort that settled ~ 5 years before 1969. Since the first survey, no juvenile was observed in the studied area. The mortality rate peaked between 1978 and 1984, when individuals were 15-20 years old. In 2009, the two last living individuals were observed. They died between 2009 and 2014, at an age between ~45 and 50 years. The putative longevity of the species is therefore far above the 10-20 years previously assumed. The total shell length of the last two survivors was 73 cm and 75 cm, respectively. ISSN: 0241-8231
Article
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We investigated the habitat use and size structure of the fan mussel, Pinna nobilis L. in the Alfacs Bay (Ebro Delta, Spain, NW Mediterranean). Shore-parallel transects were conducted to assess the abundance, size, and orientation of individuals and to record habitat features along the Banya Sandspit, at depths of 20 to 130 cm. Results showed two distinctive areas in terms of population density, marked by the end of local salt pan dikes that we named Good Habitat (GH) and Bad Habitat (BH). To extrapolate these results to the full area of BH and GH, perpendicular transects were conducted to determine the local bathymetry. Then, the underestimation of individuals due to the effects of distance, depth and seagrass cover (Distance 6 computer package) was added to raw abundances to obtain a corrected population of 90303 individuals (12085 in the BH and 782018 in the GH), the largest so far reported at such low depths. Most recorded individuals were adults (40 to 60 cm shell length), with no occurrence of sizes <20 cm, and with a strong association with Cymodocea nodosa seagrass beds. Given the shallow distribution of the population, the absence of small sizes during the study period, and the presence of human activities that may damage P. nobilis and its habitat, the development of a management plan appears imperative for the conservation of the species.
Article
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An updated climatology, based on a comprehensive dataset (1911-2009) of temperature, salinity and dissolved oxygen, has been produced for the whole Adriatic Sea with the Variational Inverse Method using the DIVA (Data-Interpolating Variational Analysis) software. Climatological maps were produced at 26 levels and validated with Ordinary Cross Validation and with real vs synthetic Temperature–Salinity diagram intercomparison. The concept of Climatology–Observation Misfit (COM) has been introduced as an estimate of the physical variability associated with the climatological structures. In order to verify the temporal stability of the climatology, long-term variability has been investigated in the Mid Adriatic and the South Adriatic Pits, regarded as the most suitable records of possible long-term changes. Compared with previous climatologies, this study allows a clear identification of the seasonal dynamic of the South Adriatic, where a clear oxygen minimum is typically recognized in the centre of the South Adriatic Gyre. New or better resolved features emerged from this analysis: (1) below 100 m all properties profoundly differ between the Middle and the South Adriatic and seem characterized by different biogeochemical dynamics; (2) the South Adriatic Pit clearly shows the remote effects of the Eastern Mediterranean Transient, while no effect is observed in Middle Adriatic Pits; (3) the deepest part of the South Adriatic seems now to be significantly saltier (+0.18 since the period 1910-1914, with an increase of +0.018 decade-1 since the late 1940s) and warmer (+0.54°C since 1910-1914), even though a long-term temperature trend could not be statistically demonstrated; (4) the Middle Adriatic Pits present a long-term increase in apparent oxygen utilisation (+0.77 ml l-1 since 1910-1914, with a constant increase of +0.2 ml l-1 decade-1 after the 1970s).
Article
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http://www.ocean-sci-discuss.net/11/331/2014/osd-11-331-2014.html An updated climatology, based on a comprehensive dataset (1911–2009) of temperature, salinity and dissolved oxygen, has been produced for the whole Adriatic Sea with the Variational Inverse Method using the DIVA software. Climatological maps were produced at 26 levels and validated with Ordinary Cross Validation and with real vs. synthetic Temperature–Salinity diagram intercomparison. The concept of Climatology–Observation Misfit (COM) has been introduced as an estimate of the physical variability associated with the climatological structures. In order to verify the temporal stability of the climatology, long-term variability has been investigated in the Mid Adriatic and the South Adriatic Pits, regarded as the most suitable records of possible long-term changes. Compared with previous climatologies, this study reveals a surface temperature rise (up to 2 °C), a clear deep dissolved oxygen minimum in the South Adriatic Gyre and a bottom summer oxygen minimum in the North Adriatic. Below 100 m all properties profoundly differ between the Middle and the South Adriatic. The South Adriatic Pit clearly shows the remote effects of the Eastern Mediterranean Transient, while no effect is observed in Middle Adriatic Pits. The deepest part of the South Adriatic seems now to be significantly saltier (+0.18 since the period 1911–1914, with an increase of +0.018 decade−1 since the late 1940s) and warmer (+0.54 °C since 1911–1914), even though a long-term temperature trend could not be statistically demonstrated. Conversely, the Middle Adriatic Pits present a long-term increase in apparent oxygen utilisation (+0.77 mL L−1 since 1911–1914, with a constant increase of +0.2 mL L−1 decade−1 after the 1970s).
Article
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A substantial population of the endangered Mediterranean bivalve Pinna nobilis exists in the marine Lake Vouliagmeni (Korinthiakos Gulf, Greece). The population density of P. nobilis was estimated in the lake with line transect sampling. Individuals of the youngest age class (small) had peak densities in the 1 to 3 m bathymetric zone and their densities were higher in poorly sorted sediments. Older (large) individuals (belonging to all age classes except the first one, 9 to 11 mo) had peak densities in the 11 to 13 m bathymetric zone. No P. nobilis was found deeper than 22 m. The absence of large individuals in shallow waters may partly be explained by illegal fishing. There are several hypotheses proposed to explain the lack of small individuals in deeper areas, but no definitive explanation is offered. In Lake Vouliagmeni, P. nobilis densities were high, although marine seagrass was completely absent. Thus, P. nobilis does not actually require seagrass meadows, as stated by many authors, and it may exist in large numbers in bare soft-sediment areas as well. P. nobilis grew fast, mostly during the first 3 yr of life, and may live beyond 15 yr. By recording the exact location of each P. nobilis individual within 800 m2 transects, as a pair of coordinates, the exact spatial distribution was defined and aggregation indices were calculated. P. nobilis had an aggregated dispersion, but no evidence for preferential settlement near adults or previously-settled individuals was found. The aggregated dispersion of P. nobilis probably relates to the patchiness of the local environment. The size of P. nobilis population in Lake Vouliagmeni was estimated to be 8501 ± 4395 (mean ± 1 SD) individuals, of which 4355 ± 3460 belonged to the first age class and 4146 ± 1405 belonged to all other age classes.
Article
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Late in summer 2003, extensive mass mortality of at least 25 rocky benthic macro-invertebrate species (mainly gorgonians and sponges) was observed in the entire Northwestern (NW) Mediterranean region, affecting several thousand kilometers of coastline. We were able to characterize the mortality event by studying six areas covering the main regions of the NW Mediterranean basin. The degree of impact on each study area was quantified at 49 sites by estimating the proportion of colonies affected in populations of several gorgonian species compared with reference data obtained in years without mortality signs. According to these data, the western areas (Catalan coast and Balearic Islands) were the least affected, while the central areas (Provence coast and Corsica-Sardinia) showed a moderate impact. The northernmost and eastern areas (Gulf of Genoa and Gulf of Naples) displayed the highest impact, with almost 80% of gorgonian colonies affected. The heat wave of 2003 in Europe caused an anomalous warming of seawater, which reached the highest temperatures ever recorded in the studied regions, between 1 and 3 °C above the climatic values (mean and maximum). Because this exceptional warming was observed in the depth ranges most affected by the mortality, it seems likely that the 2003 anomalous temperature played a key role in the observed mortality event. A correlation analysis between temperature conditions and degree of impact seems to support this hypothesis. Under the present climate warming trend, new mass mortality events may occur in the near future, possibly driving a major biodiversity crisis in the Mediterranean Sea.
Article
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Oligonucleotides specific at a genus, group, or species level were defined by a systematic comparison of small-subunit rRNA sequences from Mycobacterium tuberculosis, M. bovis, M. africanum, M. bovis BCG, M. avium, M. kansasii, M. marinum, M. gastri, M. chelonae, M. smegmatis, M. terrae, M. nonchromogenicum, M. xenopi, M. malmoense, M. szulgai, M. scrofulaceum, M. fortuitum, M. gordonae, M. intracellulare, M. simiae, M. flavescens, M. paratuberculosis, M. sphagni, M. cookii, M. komossense, M. phlei, and M. farcinica. On the basis of the defined oligonucleotides, the polymerase chain reaction technique was explored to develop a sensitive taxon-specific detection system for mycobacteria. By using M. tuberculosis as a model system, fewer than 10 bacteria could be reliably detected by this kind of assay. These results suggest that amplification of rRNA sequences by the polymerase chain reaction may provide a highly sensitive and specific tool for the direct detection of microorganisms without the need for prior cultivation.
Article
Anthropogenic drivers and global warming are altering the occurrence of infectious marine diseases, some of which produce mass mortalities with considerable ecosystemic and economic costs. The Mediterranean Sea is considered a laboratory to examine global processes, and the fan mussel Pinna nobilis a sentinel species within it. Since September 2016, fan mussels suffer a die-off, very likely provoked by the protozoan Haplosporidium pinnae. Population dynamic surveys, rescue programmes, larvae collector installation and protection of infected adults from predators, have increased knowledge about the factors conditioning the spread of the die-off; previous model simulations indicate that water temperature and salinity seem to be related to the manifestation of the disease, which at the end are strongly influenced by climate change and anthropogenic actions. The absence of natural recruitment implies that fan mussel populations are not recovering, but the survival of populations living in paralic environments provides an opportunity to study the disease and its conditioning factors. The fan mussel disease outbreak provides a case example for how climate change may mediate host-protozoan dynamics and poses several questions: are we witnessing the potential extinction of a sentinel species? Can we avoid it by applying active measures? If so, which measures will be more effective? How many other more overlooked species might experience a massive and unnoticed die-off before it is too late to implement any preservation action? This is especially relevant because the loss of keystone species can drive to community effects that influence marine ecosystem processes.
Article
Mycobacterium sp. and Haplosporidium pinnae constitute invasive parasite species of bivalves, reported for the first time in the present study in the Aegean Sea and Thermaikos Gulf, respectively. During the last years, the endangered fan mussel (Pinna nobilis) experienced several mortality events in the Mediterranean Sea that caused deaths to 90% or more of their populations and have been attributed to infections by these pathogens. In Greece, two mass mortality events have been recently reported, namely in the Gulf of Kalloni and in Limnos island. In the present study we investigated the presence of both pathogens in P. nobilis from these marine areas as well as from Thermaikos Gulf using both histopathological microscopy and molecular markers. The detected parasite DNA was further quantified in the three populations utilizing a real time qPCR. Histopathological results indicated the presence of a Mycobacterium species alongside with the existence of the Haplosporidian parasite, which was identified in all mortality events in the Mediterranean Sea. The parasite was present in different phases mostly on the digestive gland epithelium. Phylogenetic analysis confirmed the taxonomy of the Haplosporidian parasite as the recently described Haplosporidium pinnae, whereas it failed to identify the Mycobacteria parasite at species level. While Mycobacterium sp. was detected in all examined specimens, H. pinnae was not detected in all diseased fan mussels. Interestingly, monitoring of P. nobilis population from Thermaikos Gulf, an estuary of extremely high importance for bivalve production, revealed the presence of both pathogens in a few specimens in higher quantity but with no symptoms of the disease. Besides, all the specimens from Thermaikos Gulf had inflammatory responses similarly to moribund specimens from mortality events.
Article
The fan mussel, Pinna nobilis (Linnaeus 1758), is an endemic bivalve of the Mediterranean basin, protected by international legislation as an endangered species. In the early summer of 2018, a mass mortality event (MME)of P. nobilis was recorded in the Gulf of Taranto (Southern Italy, Ionian Sea). Moribund specimens of P. nobilis were collected by scuba divers and processed by bacteriological, parasitological, histopathological and molecular analyses to investigate the causes of this MME. Different developmental stages (i.e., plasmodia, spores and sporocysts)of a presumptive haplosporidian parasite were observed during the histological analysis in the epithelium and in the lumen of the digestive tubules, where mature spores occurred either free or in sporocysts. The spores presented an operculum and an ovoid shape measuring 4.4 µm (±0.232)in length and 3.6 µm (±0.233)in width. BLAST analysis of an 18SrRNA sequence revealed a high nucleotide similarity (99%)with the reference sequence of Haplosporidium pinnae available in GenBank database. Phylogenetic analysis clustered the sequence of the pathogen in a paraphyletic clade with the reference sequence of H. pinnae, excluding other haplosporidians (i.e., Bonamia and Minchinia genera). Based on data reported, H. pinnae was the causative agent of MME in the populations of P. nobilis sampled in the Ionian Sea, where the conservation of this endangered species is heavily threatened by such a protozoan infection. Further investigations should contribute to knowledge about the life cycle of H. pinnae in order to reduce spread of the pathogen and to mitigate the burden of the disease where P. nobilis is facing the risk of extinction.
Article
This study provides morphological and molecular characterization of a new species, Haplosporidium pinnae, very likely responsible for mass mortality of fan mussels, Pinna nobilis, in the Western Mediterranean Sea. The parasite was found in dead or moribund P. nobilis but did not occur in healthy fan mussels from locations that were not affected by abnormal mortality. Histological examination of infected fan mussels showed uninucleate cells of a haplosporidan parasite throughout the connective tissue and hemolymph sinuses of the visceral mass and binucleate cells and, rarely, multinucleate plasmodia were also detected in the connective tissue. Additionally, stages of sporulation occurred in the epithelium of the host digestive gland tubules. Spores were slightly ellipsoidal with a hinged operculum in one pole. Typical haplosporosomes were not found with TEM but vesicles with two concentric membranes resembling haplosporosomes were abundant in the cytoplasm of the multinucleate plasmodia occurring in host digestive gland tubules. SEM analysis showed multiple structures on the spore surface; some spores had two or four long tape-like filaments attached to the spore wall. Phylogenetic analysis based on the SSU rDNA sequence placed this parasite within a large clade including species of the order Haplosporida, not in the Bonamia/Minchinia subclade or the subclade containing most Haplosporidium species, but within a subclade of Haplosporidium sp. from Penaeus vannamei. Our results suggested that H. pinnae and the parasite of P. vannamei may represent a distinct new genus within the order Haplosporida.
Book
Because of its centrallocation in the Old World, the Adriatic Sea has long been explored and studied. Modern methods of investigation, however, have accelerated the pace of study during the last decade. These are the ADCP currentmeter, satellite imagery, drifter technology, and, last but not least, the computer with its arsenal of tools for data analysis and model simulations. As a result of this renaissance, the Adriatic Sea and its sub-basins are currently the object of intensified scrutiny by a number of scientific teams, in Europe and be­ yond. Questions concerning the mesoscale variability that dominates regional motions, the seasonal circulation of the sea, and its long-term climatic role in the broader Mediterranean, have become topics of lively discussions. The time was ripe then when an international workshop dedicated to the physical oceanography of the Adriatic Sea was convened in Trieste on 21-25 September 1998. Its objectives were to assess the current knowledge of the oceanography of the Adriatic Sea, to review the newly acquired observations, to create syn­ ergy between model simulations and observations, and to identify directions for future Adriatic oceanography. This book, however,is not the mere proceedings of the workshop. It was written as a monograph synthetizing the current knowledge of the physical oceanography of the Adriatic Sea, with the hope that it will serve as a reference to anyone interested in the Adriatic. The book also identifies topics in need of additional inquiry and proposes research directions for the next decade.
Article
A mass mortality event (MME) impacting the bivalve Pinna nobilis was detected across a wide geographical area of the Spanish Mediterranean Sea (Western Mediterranean Sea) in early autumn 2016. Underwater visual censuses were conducted across several localities separated by hundreds of kilometers along the Spanish Mediterranean coasts and revealed worrying high mortality rates reaching up to 100% in the center and southernmost coasts of the Iberian Peninsula including Balearic Islands. Populations on the northern coasts of the Spanish Mediterranean Sea seemed to be unaffected (Catalonian region). Histological examination of affected individuals revealed the presence of a haplosporidan-like parasite within the digestive gland being probably the pathogen that causes this mortality. The present MME has spread rapidly, causing high mortality rates in infected populations. Taking into account the degree of impact, the geographic extent, and the high probability that the infection is still in a spreading phase, this might be considered the largest MME ever registered for P. nobilis up to date, forcing this emblematic bivalve into a critical viability status over hundreds of kilometers of coast.
Article
Several stages of a haplosporidan parasite, including spores, were detected infecting three out of four specimens of the Pen Shell Pinna nobilis from the coast of Alicante (Western Mediterranean). A mortality event initiated few weeks before the sampling. The infection was systemic in the connective tissue, with free uni-nucleate stages and early plasmodia, whereas sporulation process took place in the digestive tubules disrupting them. Morphological details, by light and transmission electron microscopy, and PCR amplification confirmed that the parasite belongs to the haplosporidan group. Spores were pleomorphic, usually elongated ovoid, with round to elongated haplosporosomes-like in the sporoplasma. The operculum was situated in the apical zone of the wall, with an external lid, and the nucleus tended to be eccentric in the basal zone. Spore ornamentation was not observed. The single uninfected specimen appeared to be healthy. This is the first report of a haplosporidan parasite infecting a member of the Superfamily Pinnoidea and this is the first histopathological study of a mortality event in the endangered and protected P. nobilis.
Article
Recreational diving engages 20 million people worldwide. Most of the literature refers to tropical destinations but at least 1 million dives per year take place in Mediterranean marine protected areas (MPAs). 2. Divers may negatively affect underwater habitats. However, if effectively engaged, they can contribute to science, territorial management and more sustainable local economies. 3. During 2006–2014, volunteers trained by the not-for-profit organization Reef Check Italia (RCI) completed 24 714 observations and 2417 dives in six Mediterranean countries, contributing to a dataset that supports scientific papers about climate change, rare and non-indigenous species (NIS), and informs MPA management decision-making. 4. The wide range of opportunities offered by this dataset is illustrated with two examples relevant to marine conservation in the context of MPA management. They concern: (i) the spread of the NIS Caulerpa cylindracea along the Ligurian coasts, with a focus on Portofino MPA, and (ii) the distribution and abundance of protected species in the Portofino MPA. 5. A diver-focused survey showed that RCI volunteers are highly committed, and that participation in RCI activities has led to a better understanding of, and a sense of stewardship towards, favoured dive sites and the marine world. Knowing who volunteers are, and why they volunteer in their favourite sector, is crucial to designing citizen-science based projects able to achieve their multiple goals.
Article
An investigation to characterize the causes of Pinna nobilis population structure in Moraira bay (Western Mediterranean) was developed. Individuals of two areas of the same Posidonia meadow, located at different depths (A1, −13 and A2, −6 m), were inventoried, tagged, their positions accurately recorded and monitored from July 1997 to July 2002. On each area, different aspects of population demography were studied (i.e. spatial distribution, size structure, displacement evidences, mortality, growth and shell orientation). A comparison between both groups of individuals was carried out, finding important differences between them. In A1, the individuals were more aggregated and mean and maximum size were higher (A1, 10.3 and A2, 6 individuals/100 m2; A1, x = 47.2 ± 9.9; A2, x = 29.8 ± 7.4 cm, P < 0.001, respectively). In A2, growth rate and mortality were higher, the latter concentrated on the largest individuals, in contrast to A1, where the smallest individuals had the higher mortality rate [A1, L = 56.03(1 − e−0.17t ); A2, L = 37.59(1 − e−0.40t ), P < 0.001; mean annual mortality A1: 32 dead individuals out of 135, 23.7% and A2: 16 dead individuals out of 36, 44.4%, and total mortality coefficients (z), z A1(−30) = 0.28, z A1(31–45) = 0.05, z A1(46−) = 0.08; z A2(−30) = 0.15, z A2(31–45) = 0.25]. A common shell orientation N–S, coincident with the maximum shore exposure, was observed in A2. Spatial distribution in both areas showed not enough evidence to discard a random distribution of the individuals, despite the greater aggregation on the deeper area (A1) (A1, χ 2 = 0.41, df = 3, P > 0.5, A2, χ 2 = 0.98, df = 2 and 0.3 < P < 0.5). The obtained results have demonstrated that the depth-related size segregation usually shown by P. nobilis is mainly caused by differences in mortality and growth among individuals located at different depths, rather than by the active displacement of individuals previously reported in the literature. Furthermore, dwarf individuals are observed in shallower levels and as a consequence, the relationship between size and age are not comparable even among groups of individuals inhabiting the same meadow at different depths. The final causes of the differences on mortality and growth are also discussed.
Haplosporidaium pinnae sp
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Deudero, S., Darriba, S., Carballal, M.J., Villalba, A. 2018. Haplosporidaium pinnae sp.
Mapping and monitoring of the noble pen shell (Pinna nobilis) habitats (in 319 the Nature Park "Telašćica"). Marine Explorers Society -20000 Leagues
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Čižmek, H. 2016. Mapping and monitoring of the noble pen shell (Pinna nobilis) habitats (in 319 the Nature Park "Telašćica"). Marine Explorers Society -20000 Leagues. Technical
Pinna nobilis) during a mortality event in Alicante
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Pinnoidea (Pinna nobilis) during a mortality event in Alicante (Spain, Western
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