Northeast Atlantic elasmobranch community on the move: Functional reorganization in response to climate change.

While spatial distribution shifts have been documented in many marine fishes under global change, the responses of elasmobranchs have rarely been studied, which may have led to an underestimation of their potential additional threats. Given their irreplaceable role in ecosystems and their high extinction risk, we used a 24-year time series (1997-2020) of scientific bottom trawl surveys to examine the effects of climate change on the spatial distribution of nine elasmobranch species within Northeast Atlantic waters. Using a hierarchical modeling of species communities, belonging to the joint species distribution models, we found that suitable habitats for four species increased on average by a factor of 1.6 and, for six species, shifted north-eastwards and/or to deeper waters over the past two decades. By integrating species traits, we showed changes in habitat suitability led to changes in the elasmobranchs trait composition. Moreover, communities shifted to deeper waters and their mean trophic level decreased. We also note an increase in the mean community size at maturity concurrent with a decrease in fecundity. Because skates and sharks are functionally unique and dangerously vulnerable to both climate change and fishing, we advocate for urgent considerations of species traits in management measures. Their use would make it better to identify species whose loss could have irreversible impacts in face of the myriad of anthropogenic threats.

Population genetics reveals divergent lineages and ongoing hybridization in a declining migratory fish species complex.

Deciphering the effects of historical and recent demographic processes responsible for the spatial patterns of genetic diversity and structure is a key objective in evolutionary and conservation biology. Using population genetic analyses, we investigated the demographic history, the contemporary genetic diversity and structure, and the occurrence of hybridization and introgression of two species of anadromous fish with contrasting life history strategies and which have undergone recent demographic declines, the allis shad (Alosa alosa) and the twaite shad (Alosa fallax). We genotyped 706 individuals from 20 rivers and 5 sites at sea in Southern Europe at thirteen microsatellite markers. Genetic structure between populations was lower for the nearly semelparous species A. alosa, which disperses greater distances compared to the iteroparous species, A. fallax. Individuals caught at sea were assigned at the river level for A. fallax and at the region level for A. alosa. Using an approximate Bayesian computation framework, we inferred that the most likely long term historical divergence scenario between both species and lineages involved historical separation followed by secondary contact accompanied by strong population size decline. Accordingly, we found evidence for contemporary hybridization and bidirectional introgression due to gene flow between both species and lineages. Moreover, our results support the existence of at least one distinct species in the Mediterrannean sea: A. agone in Golfe du Lion area, and another divergent lineage in Corsica. Overall, our results shed light on the interplay between historical and recent demographic processes and life history strategies in shaping population genetic diversity and structure of closely related species. The recent demographic decline of these species' populations and their hybridization should be carefully considered while implementing conservation programs.

Molecular detection of the swim bladder parasite Anguillicola crassus (Nematoda) in fecal samples of the endangered European eel Anguilla anguilla.

The European eel Anguilla anguilla is listed as critically endangered by the IUCN. Among many threats, the introduced parasitic nematode Anguillicola crassus is suspected to alter the eels' swim bladder and jeopardize their reproductive oceanic migration. To date, gaining knowledge about the distribution and prevalence of A. crassus requires individual sacrifice (over 50,000 eels were sacrificed for epidemiology studies since 2010). This paper describes a non-lethal molecular protocol for identifying prevalence of A. crassus in A. anguilla, based on searching for A. crassus DNA in the feces of eels. Tests using three DNA microsatellite markers specific to the nematode showed that molecular detection provided similar results to visual examination of the swim bladder in up to 80% of the cases, and allowed for comparison of prevalence among sites. Easy to implement, this non-lethal protocol for detecting A. crassus could be valuable for management plans of this endangered species.

Distribution of anguillid leptocephali and possible spawning areas in the South Pacific Ocean.

Seven South Pacific anguillid eel species live from New Guinea to French Polynesia, but their spawning areas and life histories are mostly unknown despite previous sampling surveys. A July-October 2016 research cruise was conducted to study the spawning areas and times, and larval distributions of South Pacific anguillid eels, which included a short 155°E station-line northeast of New Guinea and five long transects (5-25°S, 160°E-140°W) crossing the South Equatorial (SEC) and other currents. This survey collected nearly 4000 anguilliform leptocephali at 179 stations using an Isaacs-Kidd Midwater Trawl accompanied by 104 CTD casts. Based on mor-phometric observations and DNA sequencing, 74 anguillid leptocephali were collected, which in the southern areas included 29 larvae of six species: Anguilla bicolor pacifica, A. marmorata, A. australis, A. reinhardtii, A. megastoma, and A. obscura (all anguillid species of the region were caught except A. dieffenbachii). Small A. australis (9.0-16.8 mm) and A. reinhardtii (12.4, 12.5 mm) leptocephali were collected south of the Solomon Islands, other A. australis (10.8-12.0 mm) larvae were caught northwest of Fiji along with an A. obscura (20.0 mm) larva, and an A. marmorata (7.8 mm) larva was collected near Samoa. Considering collection sites, larval ages from otolith analysis, and westward SEC drift, multiple spawning locations occurred from south of the Solomon Islands and the Fiji area (16-20 days old larvae) to near Samoa (19 days old larva) during June and July in areas where high-salinity Subtropical Underwater (STUW, ~150 m depth) and the warm, low-salinity surface Fresh Pool were present. Five long hydrographic sections showed the strong Fresh Pool in the west and the STUW formation area in the east.

Resolving the trade-off between silver eel escapement and hydropower generation with simple decision rules for turbine shutdown.

Hydropower plants are commonly reported as a major cause of the worldwide decline of freshwater eels (Anguillidae), so that management solutions are urgently needed to mitigate their impacts. Where downstream passage solutions are complex to develop, turbine shutdown appears as an effective management solution to protect silver eels during their river migration toward spawning areas. However, the definition of operational decision rules for turbine shutdown is challenging due to the duality between the benefit for eel conservation and the concomitant cost in term of hydropower production. Here, we proposed a decision framework for turbine shutdown based on simple hydrological criteria to guide negotiations between stakeholders toward a trade-off between silver eel escapement and hydropower generation. Eel migration was assumed to be triggered by a minimum river flow associated with a minimum discharge pulse, so that threshold values can be directly implemented as decision rules for turbine shutdown. To estimate relevant thresholds, a generic methodological framework was developed to generate alternative decision rules from data collected at hydropower plants, which can include telemetry surveys and estimates of eel abundance. A multiple-criteria decision analysis was then conducted to rank alternatives and to determine the best compromise between promoting silver eel escapement and limiting turbine shutdown duration. Graphic outputs can help stakeholders to understand the competitive interests between eel conservation and hydropower production, while visually identifying a range of consensual alternatives to support negotiations in the choice of operational thresholds. The method was illustrated for three river systems in Europe featured by distinct hydrological conditions and can be applied in other areas, providing that eel monitoring surveys and flow data are available.

Metazoan parasite communities in Alosa alosa (Linnaeus, 1758) and Alosa fallax (Lacépède, 1803) (Clupeidae) from North-East Atlantic coastal waters and connected rivers.

Metazoan parasites were studied in 96 Alosa alosa and 78 Alosa fallax from North-East Atlantic coastal waters and connected rivers (among them three sympatric sites) in order to increase knowledge on these anadromous endangered fish and measure the parasitic impact on host condition. All shads were infected by one to six metazoan parasite taxa among the 12 identified in the whole sampling, with a mean abundance of parasites higher for A. alosa (167 ± 10) than for A. fallax (112 ± 11). Helminths, mostly trophically transmitted, were the best represented (eight taxa, prevalence up to 99%) in contrast with crustaceans and Petromyzontidae that rarely occurred (four taxa, prevalence <6%). Despite some quantitative differences, metazoan parasite communities of A. alosa and A. fallax remained stable in composition whatever the host developmental stage, sex, sample site, and salinity. Among the nine parasite taxa harbored by each Alosa species, six were shared with some differences in distribution patterns including in sympatric conditions, suggesting increasing dissimilarities between A. alosa and A. fallax with the age. Information on feeding ecology provided by trophically transmitted helminths confirmed euryphagous opportunistic diet of immatures and adults of both shad species, and assessed feeding of adults during spawning migrations. Our study also revealed the significant negative impact of Hemiurus appendiculatus on A. alosa and Pronoprymna ventricosa on A. fallax. Because helminth parasites are omnipresent in the shads and decrease their fitness, parasitological data must be included in further investigations and management programs on A. alosa and A. fallax.

Shark critical life stage vulnerability to monthly temperature variations under climate change.

In a 10-month experimental study, we assessed the combined impact of warming and acidification on critical life stages of small-spotted catshark (Scyliorhinus canicula). Using recently developed frameworks, we disentangled individual and group responses to two climate scenarios projected for 2100 (SSP2-4.5: Middle of the road and SSP5-8.5: Fossil-fueled Development). Seasonal temperature fluctuations revealed the acute vulnerability of embryos to summer temperatures, with hatching success ranging from 82% for the control and SSP2-4.5 treatments to only 11% for the SSP5-8.5 treatment. The death of embryos was preceded by distinct individual growth trajectories between the treatments, and also revealed inter-individual variations within treatments. Embryos with the lowest hatching success had lower yolk consumption rates, and growth rates associated with a lower energy assimilation, and almost all of them failed to transition to internal gills. Within 6 months after hatching, no additional mortality was observed due to cooler temperatures.

Quantifying larval dispersal portfolio in seabass nurseries using otolith chemical signatures.

The temporal asynchronies in larvae production from different spawning areas are fundamental components for ensuring stability and resilience of marine metapopulations. Such a concept, named portfolio effect, supposes that diversifying larval dispersal histories should minimize the risk of recruitment failure by increasing the probability that at least some larvae successfully settle in nursery. Here, we used a reconstructive approach based on otolith chemistry to quantify the larval dispersal portfolio of the European seabass, Dicentrarchus labrax, across six estuarine nursery areas of the northeast Atlantic Ocean. The analysis of natal and trajectory signatures indicated that larvae hatch in distinct environments and then dispersed in water masses featured by contrasting chemical signatures. While some trace elements appeared affected by temporal changes (Mn and Sr), others varied spatially during the larval stage but remained poorly affected by temporal fluctuation and fish physiology (Ba, Cu, Rb and Zn). We then proposed two diversity metrics based on richness and variations of chemical signatures among populations to reflect spatio-temporal diversity in natal origins and larval trajectories (i.e., estimates of dispersal portfolio). Along the French coast, the diversity estimates were maximum in nurseries located at proximity of offshore spawning sites and featured by complex offshore hydrodynamic contexts, such as the Mont St-Michel bay. Finally, our findings indicate that the dispersal portfolio was positively related with the local abundance of seabass juveniles, supporting the assumption that heterogeneity in dispersal history contributes to promote recruitment success in nurseries.

Decoupling carry-over effects from environment in fish nursery grounds.

Life-history trait expression not only depends on the current environmental constraints, but also on the past ones that shaped traits expressed earlier in life. Such an effect, named carry-over, can occur in fish nursery grounds when juvenile performances after settlement are influenced by their larval traits in combination with conditions experienced in nurseries. To date, the impacts of environmental and human stressors on post-settlement traits have been assessed, but independently from larval traits, so that the contributions of environmental versus carry-over constraints remain unquantified. Here, we used a reconstructive approach based on otolith microstructure to investigate how carry-over and environment affect life-history traits of the European seabass, Dicentrarchus labrax. In the northeast Atlantic Ocean, seabass juveniles were collected in six French estuarine nursery areas with contrasted environmental conditions (water temperature, salinity, food availability, and anthropogenic impacts), and five of their life-history traits across ontogenetic stages were measured (pelagic growth, larval duration, size at settlement, post-settlement growth and body condition). Piecewise structural equation model emphasized the strong co-variation of larval traits in response to food availability and temperature in the pelagic environment, stressing that fast growing larvae are characterized by shorter pelagic larval duration, but larger size at recruitment. However, the magnitude of carry-over effects greatly varied between traits, revealing that larval trait impacts on post-settlement traits remained minor as compared to the nursery environment. In estuarine nurseries, our findings suggest that resource allocation results from a trade-off between somatic growth and energy storage. Fish juveniles exposed to anthropogenic stress or risk of food limitation tended to predominantly invest in storage, whereas individuals in favourable conditions allocated their resources in somatic growth. These findings highlight the importance of heterogeneity in pelagic and nursery environments in understanding trait variations and population dynamic of estuarine dependent fish.

Panmixia in the American eel extends to its tropical range of distribution: Biological implications and policymaking challenges.

The American eel (Anguilla rostrata) has long been regarded as a panmictic fish and has been confirmed as such in the northern part of its range. In this paper, we tested for the first time whether panmixia extends to the tropical range of the species. To do so, we first assembled a reference genome (975 Mbp, 19 chromosomes) combining long (PacBio and Nanopore and short (Illumina paired-end) reads technologies to support both this study and future research. To test for population structure, we estimated genotype likelihoods from low-coverage whole-genome sequencing of 460 American eels, collected at 21 sampling sites (in seven geographic regions) ranging from Canada to Trinidad and Tobago. We estimated genetic distance between regions, performed ADMIXTURE-like clustering analysis and multivariate analysis, and found no evidence of population structure, thus confirming that panmixia extends to the tropical range of the species. In addition, two genomic regions with putative inversions were observed, both geographically widespread and present at similar frequencies in all regions. We discuss the implications of lack of genetic population structure for the species. Our results are key for the future genomic research in the American eel and the implementation of conservation measures throughout its geographic range. Additionally, our results can be applied to fisheries management and aquaculture of the species.

Small- and large-scale processes including anthropogenic pressures as drivers of gastropod communities in the NE Atlantic coast: A citizen science based approach.

Rocky-shores are among the most threatened coastal habitats, particularly under human pressures. While rocky-shore communities have been increasingly used to evaluate local anthropogenic perturbations such as water eutrophication for instance, large-scale variability in relation to both natural and anthropogenic pressures is still overlooked. Here, using citizen science-based data, we applied a Random Forest modelling approach to assess the relative impact of both small-and large-scale processes (including natural and some anthropogenic pressures) on intertidal gastropod communities as well as taxa-specific gastropod abundances over more than 1000 km of the North-East Atlantic coast. Our model results demonstrate that small-scale conditions (i.e. within shore) are determinant in shaping gastropod communities. However, community responses are mainly driven by taxon-specific effects. Among large-scale predictors, high concentrations of inorganic nutrients and total suspended matter, as found in large river plumes, are the main drivers impacting the gastropod communities by depleting both taxon abundances and richness. According to models, the decline in abundance of the yet most prevalent taxa (Steromphala umbilicalis, Patella spp., S. pennanti and Phorcus lineatus) is expected to be between 65% and 85%, while Littorina littorea was the only taxon which may be favoured by high concentrations of inorganic nutrients and total suspended matter. Such results provide relevant insights in the context of ever-increasing needs for bioindicators of coastal ecosystems. Finally, this work sheds light on the value of a citizen science program resulting from a consultation between professional and citizen volunteers as a useful and efficient tool to investigate large-scale processes.

Invasiveness risks of naked goby, Gobiosoma bosc, to North Sea transitional waters.

In recent decades, gobies have dispersed or introduced from the Ponto-Caspian region of eastern Europe in a westerly direction to North American and western European waters. By contrast, the naked goby, Gobiosoma bosc, is the only known gobiid species to have been introduced in an easterly direction from North American to western Europe. The potential invasiveness of G. bosc was assessed using the Aquatic Species Invasiveness Screening Kit (AS-ISK) for rivers and transitional waters for the western and eastern sides of the North Sea. Using globally-derived thresholds, G. bosc was assessed as low-medium invasiveness risk for both sides of the North Sea under current climate conditions. Under future climate conditions, potential invasiveness will increase for both risk assessment areas. Environmental suitability assessment indicated an increase in environmental suitability for G. bosc on the eastern coastline of the North Sea under climate change scenarios and suitability remained unchanged on the western coastline, reflecting the authors' expectations of invasiveness risk.

European flounder foraging movements in an estuarine nursery seascape inferred from otolith microchemistry and stable isotopes.

Despite the importance of estuarine nurseries in the regulation of many fish stocks, temporal and spatial movements and habitat use patterns of juvenile fish remain poorly understood. Overall, combining several movement metrics allowed us to characterize dispersal patterns of juvenile flounder, Platichthys flesus, along an estuarine seascape. Specifically, we investigated otolith microchemistry signatures (Sr:Ca and Ba:Ca ratios) and stable isotope ratios (δ13C and δ15N) in muscles of these juveniles, during three consecutive years to assess inter-annual fluctuations in their home range and isotopic niches. The morphological condition and lipid content of individuals were lower in years of high as compared to low dispersal along the estuarine gradient. We discuss these results in relation to the ecosystem productivity and intra- and inter-specific competition level, which in turn affects movements and foraging behaviors of juvenile flounders.

A global-scale screening of non-native aquatic organisms to identify potentially invasive species under current and future climate conditions.

The threat posed by invasive non-native species worldwide requires a global approach to identify which introduced species are likely to pose an elevated risk of impact to native species and ecosystems. To inform policy, stakeholders and management decisions on global threats to aquatic ecosystems, 195 assessors representing 120 risk assessment areas across all six inhabited continents screened 819 non-native species from 15 groups of aquatic organisms (freshwater, brackish, marine plants and animals) using the Aquatic Species Invasiveness Screening Kit. This multi-lingual decision-support tool for the risk screening of aquatic organisms provides assessors with risk scores for a species under current and future climate change conditions that, following a statistically based calibration, permits the accurate classification of species into high-, medium- and low-risk categories under current and predicted climate conditions. The 1730 screenings undertaken encompassed wide geographical areas (regions, political entities, parts thereof, water bodies, river basins, lake drainage basins, and marine regions), which permitted thresholds to be identified for almost all aquatic organismal groups screened as well as for tropical, temperate and continental climate classes, and for tropical and temperate marine ecoregions. In total, 33 species were identified as posing a 'very high risk' of being or becoming invasive, and the scores of several of these species under current climate increased under future climate conditions, primarily due to their wide thermal tolerances. The risk thresholds determined for taxonomic groups and climate zones provide a basis against which area-specific or climate-based calibrated thresholds may be interpreted. In turn, the risk rankings help decision-makers identify which species require an immediate 'rapid' management action (e.g. eradication, control) to avoid or mitigate adverse impacts, which require a full risk assessment, and which are to be restricted or banned with regard to importation and/or sale as ornamental or aquarium/fishery enhancement.

New clues on the Atlantic eels spawning behavior and area: the Mid-Atlantic Ridge hypothesis.

The Sargasso Sea has long been considered as the only spawning area for Atlantic eels, despite the absence of direct observations. The present study raises a novel scenario, deviating from Schmidt's dogma, begins with a review of historical and recent observations that were combined to build up a global theory on spawning ecology and migration behavior of Atlantic eels. From this, it is argued that a favorable spawning area could be located eastward of Sargasso Sea at the intersection between the Mid-Atlantic Ridge and the oceanic fronts. Ocean circulation models combined with 3D particle-tracking method confirmed that spawning at this specific area would result in larval distribution fitting the field observation. This study explores the hypothesis that leptocephali are able to swim and orientate to reach their specific growth areas. It proposes a novel framework about spawning ecology, based on orientation, navigation and meeting cues of silver eels to the spawning area. Together this framework may serve as a stepping-stone for solving the long-lasting mystery of eel reproduction which first came out 2,400 years ago and promotes the understanding of oceanic migration and reproduction of marine organisms.

Towards transferability in fish migration models: A generic operational tool for predicting silver eel migration in rivers.

In the global context of river fragmentation, predicting fish migration is urgent to implement management actions aimed at protecting and promoting the free movement of diadromous fish. However, large-scale applicability of conservation measures requires transferable models that enable prediction of migration even in data-poor regions. Here, we surveyed 12 contrasted European river sites to predict the activity peaks of silver eels (Anguilla anguilla) during river migration towards spawning areas through an ensemble modelling approach. Site-specific Boosted Regression Tree (BRT) models were adjusted using standardized hydrological variables to predict migration probability, which were aggregated in consensus predictions. Results of independent cross-validations demonstrated that silver eel migration runs were accurately predicted in response to changes in river discharge. Transferability and predictive performance were improved by considering catchment-size dissimilarity between river sites (85 to 109,930 km2) when combining the site-specific predictions. Nevertheless, we provided two examples for which the effects of human actions on flow conditions were so high that they prevented reliable predictions of migration runs. Further contributions should thus take advantage of the flexibility of our approach for updating model collection with new sites to extend the predictive performance under a larger range of ecological conditions. Our transferable hydrological-based modelling framework offers an opportunity to implement large-scale management strategies for eel conservation, even in rivers where eel monitoring data lack. The BRT models and prediction functions were compiled in an R package named 'silvRpeak' to facilitate operational implementation by end-user managers, which can determine when mitigation measures should be implemented to improve river continuity (e.g. turbine shutdown and sluice gate opening) and balance their economic activity towards eel conservation. The only input required is discharge records that are widely available across European hydrological stations.

Stable species boundaries despite ten million years of hybridization in tropical eels.

Genomic evidence is increasingly underpinning that hybridization between taxa is commonplace, challenging our views on the mechanisms that maintain their boundaries. Here, we focus on seven catadromous eel species (genus Anguilla) and use genome-wide sequence data from more than 450 individuals sampled across the tropical Indo-Pacific, morphological information, and three newly assembled draft genomes to compare contemporary patterns of hybridization with signatures of past introgression across a time-calibrated phylogeny. We show that the seven species have remained distinct for up to 10 million years and find that the current frequencies of hybridization across species pairs contrast with genomic signatures of past introgression. Based on near-complete asymmetry in the directionality of hybridization and decreasing frequencies of later-generation hybrids, we suggest cytonuclear incompatibilities, hybrid breakdown, and purifying selection as mechanisms that can support species cohesion even when hybridization has been pervasive throughout the evolutionary history of clades.

Assessment of the quality of European silver eels and tentative approach to trace the origin of contaminants - A European overview.

The European eel is critically endangered. Although the quality of silver eels is essential for their reproduction, little is known about the effects of multiple contaminants on the spawning migration and the European eel management plan does not take this into account. To address this knowledge gap, we sampled 482 silver eels from 12 catchments across Europe and developed methods to assess three aspects of eel quality: muscular lipid content (N = 169 eels), infection with Anguillicola crassus (N = 482), and contamination by persistent organic pollutants (POPs, N = 169) and trace elements (TEs, N = 75). We developed a standardized eel quality risks index (EQR) using these aspects for the subsample of 75 female eels. Among 169 eels, 33% seem to have enough muscular lipids content to reach the Sargasso Sea to reproduce. Among 482 silver eels, 93% were infected by A. crassus at least once during their lifetime. All contaminants were above the limit of quantification, except the 1,2-bis(2,4,6-tribromophenoxy)ethane (BTBPE), Ag and V. The contamination by POPs was heterogeneous between catchments while TEs were relatively homogeneous, suggesting a multi-scale adaptation of management plans. The EQR revealed that eels from Warwickshire were most impacted by brominated flame-retardants and agricultural contaminants, those from Scheldt were most impacted by agricultural and construction activities, PCBs, coal burning, and land use, while Frémur eels were best characterized by lower lipid contents and high parasitic and BTBPE levels. There was a positive correlation between EQR and a human footprint index highlighting the capacity of silver eels for biomonitoring human activities and the potential impact on the suitability of the aquatic environment for eel population health. EQR therefore represents a step forward in the standardization and mapping of eel quality risks, which will help identify priorities and strategies for restocking freshwater ecosystems.