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.

Fisheries-dependent and -Independent data used to model the distribution of diadromous fish at-sea.

A database of 168 904 hauls covering the period from 1965 to 2019, from 46 surveys containing both fisheries-dependent (fishing vessels) and -independent data (scientific surveys) were collated from across the eastern Atlantic (Greater North Sea, Celtic Sea, Bay of Biscay and Iberian coast) and Metropolitan French Mediterranean waters. Data on diadromous fish (the European sturgeon (Acipenser sturio), allis shad (Alosa alosa), twait shad (Alosa fallax), Mediterranean twaite shad (Alosa agone), European eel (Anguilla anguilla), thinlip mullet (Chelon ramada), river lamprey (Lampetra fluviatilis), sea lamprey (Petromyzon marinus), smelt (Osmerus eperlanus), European flounder (Platichthys flesus), Atlantic salmon (Salmo salar) and the sea trout (Salmo trutta)) presence-absence was extracted and cleaned. The gear type and gear category which caught these species, their spatial location, and the date of capture (year and month), were also cleaned and standardised. Very little is known about diadromous fish at-sea and modelling data-poor and poorly detectable species such as diadromous fish is challenging for species conservation. Furthermore, databases which contain both scientific surveys and fisheries-dependent data on data-poor species at the temporal and geographical scale of this database are uncommon. This data could therefore be used to improve knowledge of diadromous fish spatial and temporal trends, and modelling techniques for data-poor species.

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.

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.

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.

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.

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.

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.

Empirical observations of the spawning migration of European eels: The long and dangerous road to the Sargasso Sea.

The spawning migration of the European eel (Anguilla anguilla L.) to the Sargasso Sea is one of the greatest animal migrations. However, the duration and route of the migration remain uncertain. Using fishery data from 20 rivers across Europe, we show that most eels begin their oceanic migration between August and December. We used electronic tagging techniques to map the oceanic migration from eels released from four regions in Europe. Of 707 eels tagged, we received 206 data sets. Many migrations ended soon after release because of predation events, but we were able to reconstruct in detail the migration routes of >80 eels. The route extended from western mainland Europe to the Azores region, more than 5000 km toward the Sargasso Sea. All eels exhibited diel vertical migrations, moving from deeper water during the day into shallower water at night. The range of migration speeds was 3 to 47 km day-1. Using data from larval surveys in the Sargasso Sea, we show that spawning likely begins in December and peaks in February. Synthesizing these results, we show that the timing of autumn escapement and the rate of migration are inconsistent with the century-long held assumption that eels spawn as a single reproductive cohort in the springtime following their escapement. Instead, we suggest that European eels adopt a mixed migratory strategy, with some individuals able to achieve a rapid migration, whereas others arrive only in time for the following spawning season. Our results have consequences for eel management.

Influence of introduced vs. native parasites on the body condition of migrant silver eels.

Because parasitism is among the reasons invoked to explain the collapse of Anguilla anguilla, we evaluated the parasitic constraint on body condition (BC) of migrant silver eels as a proxy of fitness with inter-site comparisons. Metazoan parasites were studied in 149 silver eels from five sites (northern Europe). In total, 89% were infected by 13 species including Myxozoa, Monogenea, Cestoda, Nematoda, and Acanthocephala. Anguillicoloides crassus was most common (56%), then Acanthocephalus clavula (30%), and Pseudodactylogyrus sp. (17%). BC, calculated for 58 females, was negatively correlated by abundance of the introduced Pseudodactylogyrus sp. but not by other parasite taxa. Nevertheless, the introduced A. crassus was considered as a severe pathogen based on previous data, whereas the native A. clavula was supposed to have limited impact. Parasite component communities and BC were different between sites. Silver eels from Stockholm Archipelago (Sweden) were the least parasitized (40% vs. 90-95% for other sites) with no parasites on the gills. Burrishoole (Ireland) differed by the absence of A. crassus and high prevalence of A. clavula (84%) but without consequences on BC. Gudenaa (Denmark), Corrib (Ireland), and Frémur (France) were close due to high prevalence of A. crassus (89-93%). Gudenaa and Corrib were the most similar because Pseudodactylogyrus sp. was also highly prevalent (respectively 71% and 60%) whereas absent in Frémur. Our results suggest that the fitness loss induced by the introduced parasites could affect the spawning success of migrant silver eels from Gudenaa and Corrib, and to a lesser extent from Frémur, but probably not those from Stockholm Archipelago and Burrishoole.

Fitness consequences of individual specialisation in resource use and trophic morphology in European eels.

Individual specialisation can lead to the exploitation of different trophic and habitat resources and the production of morphological variability within a population. Although the ecological causes of this phenomenon are relatively well known, its consequences on individual fitness are less recognised. We have investigated the extent of individual specialisation in resource use and trophic morphology and its fitness consequences through a combination of tagging-recapture, stable isotope analyses and telemetry. The European eel (Anguilla anguilla) was the model species as it displays significant variability in head shape. Independent to their body length, individuals with broader heads displayed a significantly higher trophic position (δ(15)N) than individuals with narrower heads. This corresponded with a significantly higher proportion of prey fish in their diet compared with invertebrates and was associated with the use of a habitat niche located further from the river bank. The European eel therefore provides a rare empirical example of individual specialisation in resource use and trophic morphology in a natural population occurring at a very small spatial scale. Individuals with intermediate head morphology displayed lower body condition (a proxy of fitness) than individuals with extreme head morphology (i.e. narrower and broader headed individuals), demonstrating the existence of disruptive selection associated with individual specialisation.

Impact of toxic cyanobacteria on gastropods and microcystin accumulation in a eutrophic lake (Grand-Lieu, France) with special reference to Physa (= Physella) acuta.

Hepatotoxic microcystins (MCs) produced by cyanobacteria are known to accumulate in gastropods following grazing of toxic cyanobacteria and/or absorption of MCs dissolved in water, with adverse effects on life history traits demonstrated in the laboratory. In the field, such effects may vary depending on species, according to their relative sensitivity and ecology. The aims of this study were to i) establish how various intensities of MC-producing cyanobacteria proliferations alter the structure of gastropod community and ii) compare MC tissue concentration in gastropods in the field with those obtained in our previous laboratory experiments on the prosobranch Potamopyrgus antipodarum and the pulmonate Lymnaea stagnalis. We explored these questions through a one-year field study at three stations at Grand-Lieu Lake (France) affected by different intensities of cyanobacteria proliferations. A survey of the community structure and MC content of both cyanobacteria and gastropods was associated with a caging experiment involving P. antipodarum and L. stagnalis. In total, 2592 gastropods belonging to 7 prosobranch and 16 pulmonate species were collected. However, distribution among the stations was unequal with 62% vs 2% of gastropods sampled respectively at the stations with the lowest vs highest concentrations of MC. Irrespective of the station, pulmonates were always more diverse, more abundant and occurred at higher frequencies than prosobranchs. Only the pulmonate Physa acuta occurred at all stations, with abundance and MC tissue concentration (< or = 4.32 microg g DW(-1)) depending on the degrees of MC-producing cyanobacteria proliferations in the stations; therefore, P. acuta is proposed as a potential sentinel species. The caging experiment demonstrated a higher MC accumulation in L. stagnalis (< or = 0.36 microg g DW(-1) for 71% of individuals) than in P. antipodarum (< or = 0.02 microg g DW(-1) for 12%), corroborating previous laboratory observations. Results are discussed in terms of differential gastropod sensitivity and MC transfer through the food web.

Plant invasion phenomenon enhances reproduction performance in an endangered spider.

Current models in evolutionary ecology predict life history alterations in response to habitat suitability to optimize fitness. Only few empirical studies have demonstrated how life history traits that are expected to trade off against each other differ among environments. In Europe, many salt marshes have been recently invaded by the grass Elymus athericus. Previous studies however showed higher densities of the endangered spider Arctosa fulvolineata (Araneae: Lycosidae) in invaded salt marshes compared to natural habitats, which suggests a lower habitat suitability in the latter. The aim of this study was to determine if this emerging habitat (1) affects the amount of resource acquisition and (2) alters the balance between life history traits that are expected to trade off against each other in this stenotopic salt marsh species. As suggested by theoretical studies, an optimization of fitness by increasing egg size at the cost of decreasing fecundity in unsuitable (i.e., natural) habitats was expected. Females presenting cocoon were then collected in close invaded and natural salt marsh areas within the Mont Saint-Michel Bay (France). By considering female mass as covariate, cocoon mass, number of eggs, and egg volume were compared between both habitats. Clutch mass was strongly determined by female mass in both habitats. Clutch mass was however significantly smaller in the natural habitat compared to the invaded habitat, indicating a higher resource acquisition in the latter. When correcting for female size, fecundity was additionally increased in the invaded habitat through a significant decrease in egg size. This phenotypic response can be explained by differences in habitat structure between invaded and natural habitats: the former offers a more complex litter favoring nocturnal wanderers like A. fulvolineata. The existence of such an adaptive reproduction strategy depending on habitat suitability constitutes an original case of an invasion that favors an endangered species.

Influence of toxic cyanobacteria on community structure and microcystin accumulation of freshwater molluscs.

Community structure and microcystin accumulation of freshwater molluscs were studied before and after cyanobacterial proliferations, in order to assess the impact of toxic blooms on molluscs and the risk of microcystin transfer in food web. Observed decrease in mollusc abundance and changes in species richness in highly contaminated waters were not significant; however, relative abundances of taxa (prosobranchs, pulmonates, bivalves) were significantly different before and after cyanobacterial bloom. Pulmonates constituted the dominant taxon, and bivalves never occurred after bloom. Microcystin accumulation was significantly higher in molluscs from highly (versus lowly) contaminated waters, in adults (versus juveniles) and in pulmonates (versus prosobranchs and bivalves). Results are discussed according to the ecology of molluscs, their sensitivity and their ability to detoxify.