Natural hybridization between pen shell species: Pinna rudis and the critically endangered Pinna nobilis may explain parasite resistance in P. nobilis

Recently, Pinna nobilis pen shells population in Mediterranean Sea has plummeted due to a Mass Mortality Event caused by an haplosporidian parasite. In consequence, this bivalve species has been included in the IUCN Red List as “Critically Endangered”. In the current scenario, several works are in progress to protect P. nobilis from extinction, being identification of hybrids (P. nobilis x P. rudis) among survivors extremely important for the conservation of the species. Morphological characteristics and molecular analyses were used to identify putative hybrids. A total of 10 individuals of each species (P. nobilis and P. rudis) and 3 doubtful individuals were considered in this study. The putative hybrids showed shell morphology and mantle coloration intermingled exhibiting both P. nobilis and P. rudis traits. Moreover, the analyses of 1150 bp of the 28S gene showed 9 diagnostic sites between P. rudis and P. nobilis, whereas hybrids showed both parental diagnostic alleles at the diagnostic loci. Regarding the multilocus genotypes from the 8 microsatellite markers, the segregation of two Pinna species was clearly detected on the PCoA plot and the 3 hybrids showed intermediate positions. This is the first study evidencing the existence of hybrids P. nobilis x P. rudis, providing molecular methodology for a proper identification of new hybrids. Further studies testing systematically all parasite-resisting isolated P. nobilis should be undertaken to determine if the resistance is resulting from introgression of P. rudis into P. nobilis genome and identifying aspects related to resistance.En prens

Unexpected residual habitats raise hope for the survival of the fan mussel Pinna nobilis along the Occitan coast (Northwest Mediterranean Sea)

In 2019, the status of the Mediterranean fan mussel Pinna nobilis was elevated to ‘Critically Endangered’ on the IUCN Red List, in response to the pandemic caused by the parasite Haplosporidium pinnae. Identifying refuge habitats, free from parasites, is critical to the survival of the mussel. The distribution of P. nobilis was investigated along the Occitan coast (Northwest Mediterranean Sea) because of the presence of a unique lagoonal system that may provide potential refuges. Interviews with users and managers were conducted to identify target zones where the species was sighted. In situ surveys were carried out to define the main aggregations of fan mussels and characterize the habitat. Line transects were deployed to count and measure individuals to estimate density, abundance, and size distribution. Population densities were variable, ranging from 0.6 ± 0.2 (SE) to 70.8 ± 7.6 ind. 100 m−2, representing one of the highest densities re - ported in the Mediterranean Sea. The total abundance of individuals across the coast was extra - polated to 163 000, with 87% located in Thau and Salses-Leucate, highlighting these lagoons as essential for the survival of the species. This study also revealed the diversity of habitats colonized by P. nobilis. In the context of the pandemic, only the lagoon populations remain unaffected and provide natural refuges that have disappeared from all open-water coastal areas. However, the conditions in these lagoons could become unfavorable, leading to the collapse of the last P. nobilis populations. We therefore propose that Thau and Salses-Leucate lagoons, which harbor the largest remaining populations of P. nobilis, should be declared as conservation priorities.En prens

Genetic homogeneity of the critically endangered fan mussel, Pinna nobilis, throughout lagoons of the Gulf of Lion (North‑Western Mediterranean Sea)

The fan mussel, Pinna nobilis, endemic to the Mediterranean Sea, is a critically endangered species facing mass mortality events in almost all of its populations, following the introduction of the parasite Haplosporidium pinnae. Such a unique pandemic in a marine organism, which spreads rapidly and with mortality rates reaching up to 100%, could lead to the potential extinction of the species. Only few regions, involving lagoon habitats, remain healthy throughout the entire Mediterranean Sea. This study describes the genetic structure of P. nobilis across the Gulf of Lion, including confined locations such as lagoons and ports. A total of 960 samples were collected among 16 sites distributed at 8 localities, and then genotyped using 22 microsatellite markers. Genetic diversity was high in all sites with mean allele numbers ranging between 10 and 14.6 and with observed heterozygosities (Ho) between 0.679 and 0.704. No genetic differentiation could be identified (FST ranging from 0.0018 to 0.0159) and the percentages of related individuals were low and similar among locations (from 1.6 to 6.5%). Consequently, all fan mussels, over the entire coastline surveyed, including those in the most geographically isolated areas, belong to a large genetically homogeneous population across the Gulf of Lion. Considering the ongoing mass mortality context, this result demonstrates that almost all of the genetic diversity of P. nobilis populations is still preserved even in isolated lagoons, which might represent a refuge habitat for the future of the species.En prensa2,92

Investigating population dynamics from parentage analysis in the highly endangered fan mussel Pinna nobilis

Understanding dispersal patterns is a major focus for conservation biology as it influences local survival and resilience in case of local disturbance, particularly for sessile species. Dispersal can be assessed through parentage analyses by estimating family structure and self-recruitment. This study documents the family structure of a pelagic spawner, Pinna nobilis, which is facing a major crisis that threatens its survival as most of its populations have been decimated by a parasite, Haplosporidium pinnae. In this context, we focused on a single population (Peyrefite, Banyuls-sur- mer, France) where 640 individuals were sampled in 2011, 2015, and 2018 and genotyped for 22 microsatellite markers. Genetic diversity was high and homogeneous among years, with mean allele numbers ranging between 13.6 and 14.8 and observed heterozygosities (Ho) between 0.7121 and 0.7331. Low, but significant, genetic differentiations were found between 2011–2015 and 2015–2018. A parentage analysis described 11 clusters, including one prevailing, and revealed that 46.9% of individuals were involved in half-sib relationships, even between years, suggesting that source populations were recurrent year after year. There were few individuals resampled between years (30 in 2015 and 14 in 2018), indicating a rapid turnover. Considering the large number of half-sib relationships but the low number of relations per individual, we conclude that P. nobilis exhibit homogeneous reproductive success. Self-recruitment was not detected, making this population highly vulnerable as replenishment only relies on connectivity from neighboring populations. In the context of the pandemic caused by H. pinnae, these results will have to be considered when choosing a location to reintroduce individuals in potential future rescue plans.En prensa

Ecological dependencies make remote reef fish communities most vulnerable to coral loss

yEcosystems face both local hazards, such as over-exploitation, and global hazards, such as climate change. Since the impact of local hazards attenuates with distance from humans, local extinction risk should decrease with remoteness, making faraway areas safe havens for biodiversity. However, isolation and reduced anthropogenic disturbance may increase ecological specialization in remote communities, and hence their vulnerability to secondary effects of diversity loss propagating through networks of interacting species. We show this to be true for reef fish communities across the globe. An increase in fish-coral dependency with the distance of coral reefs from human settlements, paired with the far-reaching impacts of global hazards, increases the risk of fish species loss, counteracting the benefits of remoteness. Hotspots of fish risk from fish-coral dependency are distinct from those caused by direct human impacts, increasing the number of risk hotspots by similar to 30% globally. These findings might apply to other ecosystems on Earth and depict a world where no place, no matter how remote, is safe for biodiversity, calling for a reconsideration of global conservation priorities.Peer reviewe

Global tropical reef fish richness could decline by around half if corals are lost

Reef fishes are a treasured part of marine biodiversity, and also provide needed protein for many millions of people. Although most reef fishes might survive projected increases in ocean temperatures, corals are less tolerant. A few fish species strictly depend on corals for food and shelter, suggesting that coral extinctions could lead to some secondary fish extinctions. However, secondary extinctions could extend far beyond those few coral-dependent species. Furthermore, it is yet unknown how such fish declines might vary around the world. Current coral mass mortalities led us to ask how fish communities would respond to coral loss within and across oceans. We mapped 6964 coral-reef-fish species and 119 coral genera, and then regressed reef-fish species richness against coral generic richness at the 1 degrees scale (after controlling for biogeographic factors that drive species diversification). Consistent with small-scale studies, statistical extrapolations suggested that local fish richness across the globe would be around half its current value in a hypothetical world without coral, leading to more areas with low or intermediate fish species richness and fewer fish diversity hotspots.Peer reviewe

Wide-Geographic and Long-Term Analysis of the Role of Pathogens in the Decline of Pinna nobilis to Critically Endangered Species

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 was the infection by H. pinnae. It was the only non-detected pathogen before the MME while, during MME spreading, its prevalence was higher in sick and dead individuals than in asymptomatic ones, in MME-affected areas than in non-affected sites, and it was not associated with host size, infecting both juveniles and adults. Conversely, infection with mycobacteria was independent from the period (before or during MME), from the affection of the area by MME and from the host health condition, and it was associated with host size. Gram (-) bacteria neither appeared associated with MME.En prens

The science of european marine reserves: Status, efficacy, and future needs

The ecologically and socio-economically important marine ecosystems of Europe are facing severe threats from a variety of human impacts. To mitigate and potentially reverse some of these impacts, the European Union (EU) has mandated the implementation of the Marine Strategy Framework Directive (MSFD) in order to achieve Good Environmental Status (GES) in EU waters by 2020. The primary initiative for achieving GES is the implementation of coherent networks of marine protected areas (MPAs). Marine reserves are an important type of MPA in which no extraction is allowed, but their usefulness depends upon a number of ecological, management, and political factors. This paper provides a synthesis of the ecological effects of existing European marine reserves and the factors (social and ecological) underlying their effectiveness. Results show that existing European marine reserves foster significant positive increases in key biological variables (density, biomass, body size, and species richness) compared with areas receiving less protection, a pattern mirrored by marine reserves around the globe. For marine reserves to achieve their ecological and social goals, however, they must be designed, managed, and enforced properly. In addition, identifying whether protected areas are ecologically connected as a network, as well as where new MPAs should be established according to the MSFD, requires information on the connectivity of populations across large areas. The adoption of the MSFD demonstrates willingness to achieve the long-term protection of Europe’s marine ecosystems, but whether the political will (local, regional, and continent wide) is strong enough to see its mandates through remains to be seen. Although the MSFD does not explicitly require marine reserves, an important step towards the protection of Europe’s marine ecosystems is the establishment of marine reserves within wider-use MPAs as connected networks across large spatial scales