Sardines at a junction: Seascape genomics reveals ecological and oceanographic drivers of variation in the NW Mediterranean Sea.

By evaluating genetic variation across the entire genome, one can address existing questions in a novel way while raising new ones. The latter includes how different local environments influence adaptive and neutral genomic variation within and among populations, providing insights into local adaptation of natural populations and their responses to global change. Here, under a seascape genomic approach, ddRAD data of 4609 single nucleotide polymorphisms (SNPs) from 398 sardines (Sardina pilchardus) collected in 11 Mediterranean and one Atlantic site were generated. These were used along with oceanographic and ecological information to detect signals of adaptive divergence with gene flow across environmental gradients. The studied sardines constitute two clusters (FST  = 0.07), a pattern attributed to outlier loci, highlighting putative local adaptation. The trend in the number of days with sea surface temperature above 19°C, a critical threshold for successful sardine spawning, was crucial at all levels of population structuring with implications on the species' key biological processes. Outliers link candidate SNPs to the region's environmental heterogeneity. Our findings provide evidence for a dynamic equilibrium in which population structure is maintained by physical and ecological factors under the opposing influences of migration and selection. This dynamic in a natural system warrants continuous monitoring under a seascape genomic approach that might benefit from a temporal and more detailed spatial dimension. Our results may contribute to complementary studies aimed at providing deeper insights into the mechanistic processes underlying population structuring. Those are key to understanding and predicting future changes and responses of this highly exploited species in the face of climate change.

Retrospective analysis of the pelagic ecosystem of the Western Mediterranean Sea: Drivers, changes and effects.

In the Western Mediterranean Sea, forage fishes have changed in abundance, body condition, growth, reproduction, and distribution in the last decades. Different hypotheses have been proposed to explain these changes, including increase in fishing mortality; changes in environmental conditions affecting species fitness, and planktonic productivity and quality; recovery of top predators; and increase in competitors. We investigated the main drivers and changes of the pelagic ecosystem and their effects using an ecosystem-based modelling approach. Specifically, we (1) quantified the potential historical contribution of various drivers of change, (2) investigated changes in temporal trends and spatial distributions of main ecosystem components, and (3) identified ecological consequences of these changes in top predator and competitors, their fisheries and ecosystem traits during 2000-2020. We updated an established Ecopath food-web model representing the Spanish and French Mediterranean sub-areas (GSA06 and GSA07) in 2000 with recent available data. We applied the temporal dynamic Ecosim module, and tested historical time series of fishing effort, fishing mortality and environmental factors as potential drivers. Observed biomass and landings of key species were used to validate model projections. A spatial-temporal Ecospace model was developed to project species distribution changes. Results showed historical biomass and catch changes driven by a combination of high fishing pressure and environmental change (i.e. increase in temperature and salinity, and decline in primary productivity). Small pelagic fish showed significant temporal changes and predicted shifts in their distributions, following a latitudinal gradient. Predators and competitors showed changes as well, displaying heterogeneous spatial patterns, while fisheries landings declined. Overall, results matched observations (e.g., decline of sardine, fluctuations of anchovy and increases in bluefin tuna) and illustrated the need to complement traditional assessments with integrative frameworks to move towards an ecosystem-based approach in the Mediterranean. They also highlighted important knowledge gaps to guide future research in the region.

Organophosphate ester plasticizers in edible fish from the Mediterranean Sea: Marine pollution and human exposure.

Concentrations of organophosphate esters (OPEs) plasticizers were analysed in the present study. Fifty-five fish samples belonging to three highly commercial species, European sardine (Sardina pilchardus), European anchovy (Engraulis encrasicolus), and European hake (Merluccius merluccius), were taken from the Western Mediterranean Sea. OPEs were detected in all individuals, except for two hake samples, with concentrations between 0.38 and 73.4 ng/g wet weight (ww). Sardines presented the highest mean value with 20.5 ± 20.1 ng/g ww, followed by anchovies with 14.1 ± 8.91 ng/g ww and hake with 2.48 ± 1.76 ng/g ww. The lowest OPE concentrations found in hake, which is a partial predator of anchovy and sardine, and the higher δ15N values (as a proxy of trophic position), may indicate the absence of OPEs biomagnification. Eleven out of thirteen tested OPEs compounds were detected, being diphenyl cresyl phosphate (DCP) one of the most frequently detected in all the species. The highest concentration values were obtained for tris(1,3-dichloro-2-propyl) phosphate (TDClPP), trihexyl phosphate (THP), and tris(2-butoxyethyl) phosphate (TBOEP), for sardines, anchovies, and hakes, respectively. The human health risk associated with the consumption of these fish species showing that their individual consumption would not pose a considerable threat to public health regarding OPE intake.

Main drivers of spatial change in the biomass of commercial species between summer and winter in the NW Mediterranean Sea.

There is a general lack of information related to the spatial structure and functioning of marine ecosystems considering seasonality. Here, we modeled the biomass distribution of eight commercial marine species in the northwestern Mediterranean Sea during winter and summer. We hypothesised that the seasonal differences of the water column and the spatial heterogeneity of oceanographic conditions in the study area could result in seasonal variations on the species biomass distributions. We employed a Bayesian hierarchical species distribution modelling approach (B-SDM) with data from two experimental trawl surveys to analyse which are the significant drivers in each season. Our results showed that bathymetry, temperature and fishing patterns are important variables explaining the species spatial biomass distributions. Furthermore, we found seasonal differentiation in the spatial distribution of biomass for all the studied species. Our results provide essential knowledge about the seasonal distributions of key species in the Mediterranean Sea, with important management implications.

Energy content of anchovy and sardine using surrogate calorimetry methods.

European anchovy (Engraulis encrasicolus) and sardine (Sardina pilchardus) are crucial species for the marine ecosystem of the Northwestern Mediterranean Sea. They account for a high percentage of fish landings and they represent an important economic income for the fishery sector. Concerns over their stock status are rising in recent years as biomass, growth, reproductive capacity, and body condition of both species are declining, with latitudinal variations. Therefore, there is an urgent need for a body condition monitoring scheme. Energy storage variability has important implications for both fish recruitment and population structure. Direct condition indices, such as energy density (ED) with bomb calorimetry, are highly reliable for measuring the energy content, but time-consuming. Alternatively, fatmeter analysis and relative condition index (Kn) have been proposed as effective indirect methods. The aim of this study is to test the application of fatmeter as a surrogate of bomb calorimetry to infer the energy content of sardine and anchovy. To validate its use, fatmeter values were compared with both ED and Kn values. Individuals of both species were sampled monthly for a year in order to assess seasonal variations in energy content. Our results highlight that fatmeter measurements are strongly correlated with calorimetry ED for sardine, while a weaker but significant correlation was found for anchovy. The observed differences between the two species are related to their breeding strategies. Based on this study, Kn cannot be considered a good proxy of the energy density of sardine, in particular during the resting period. By contrast, fatmeter analysis appears to be a faster and suitable method to evaluate the energy content of both species routinely. In addition, we provide a linear model to infer ED from fatmeter values for both small pelagic fish. Eventually, these findings could be used to implement body condition monitoring protocols and boost continuous large-scale monitoring.

Trophic niche overlap between round sardinella (Sardinella aurita) and sympatric pelagic fish species in the Western Mediterranean.

The northward expansion of round sardinella (Sardinella aurita) in the Mediterranean Sea, together with declines and fluctuations in biomass and landings of European sardine (Sardina pilchardus) and anchovy (Engraulis encrasicolus) observed in recent decades, may suggest potential inter-specific competition in the pelagic domain. The coexistence of sympatric zooplanktivorous fish species might therefore be exposed in part to trophic niche overlap and competition for food. Combining visual diet characterization under the microscope with DNA metabarcoding from stomach contents of fish collected in spring results show that predation on relatively large krill is equally important for sardinella than for the other two niche overlapping species. Furthermore, an important overlap is found in their isotopic niche, especially with anchovy, using nitrogen (δ15N) and carbon (δ13C) stable isotopes in muscle tissue. In fact, the three fish species are able to feed effectively in the whole prey size spectrum available during the sampled season, from the smallest diatoms and copepods to the larger prey (i.e., decapods and euphausiids), including fish larvae. Moreover, effective predation upon other large prey like siphonophores, which is observed only when multi-proxy analyses in stomach contents are applied, might also be relevant in the diet of sardinella. The overlapping diet composition in spring, together with the effective use of food resource by sardinella, can be of special interest in potential future scenarios with warmer water temperature leading to lower zooplankton and/or higher jellyfish availability, where sardinella may take advantage over other species due to its feeding plasticity.

Ingestion of microplastics and occurrence of parasite association in Mediterranean anchovy and sardine.

We quantified the incidence of microplastics in the gut contents of the European sardine (Sardina pilchardus) and anchovy (Engraulis encrasicolus) in the Northwestern Mediterranean Sea and tested which variables influence this abundance, including the prevalence of parasites (i.e., trematoda larvae and nematodes). We detected a 58% occurrence of microplastics ingestion in sardines and a 60% in anchovies. With respect to sardines, the individuals with lower body conditions were found to have the highest microplastics ingestion probabilities, whereas in anchovies such probabilities were observed in individuals with higher gonadosomatic indices and smaller size. The areas with the highest microplastics ingestion probabilities were the Gulf of Alicante for sardines and the Gulf of Lion - Ebro Delta for anchovies. Both species showed a positive relationship between parasites and microplastics ingestion. These results highlight that both parasitism and ingestion of microplastics are concerns for the health of marine stocks and human consumers.

Marine protected areas for demersal elasmobranchs in highly exploited Mediterranean ecosystems.

Marine ecosystems are complex socio-ecological systems where sustainable solutions can be best gained by satisfying both conservation and socioeconomic demands. Concretely, the Mediterranean Sea is facing a huge demand of resources and marine activities while hosting abundant and unique biodiversity. It is considered an important elasmobranch hotspot where seventy-two elasmobranch species are present in the basin. Despite the recognised importance of elasmobranchs as umbrella species, to date only a small number of marine protected areas have been designated towards their protection. The paucity of spatially-explicit abundance data on elasmobranchs often precludes the designation of these areas to protect these marine predators. Here, we aimed to identify marine areas to protect elasmobranch species by means of a systematic spatial planning approach. We first estimated the spatial distribution of five elasmobranch species (three sharks and two rays) in the western Mediterranean Sea and then applied Marxan decision support tools to find priority marine conservation areas. We found that the five elasmobranchs are distributed in coastal and slope areas of the southern waters of the study area while in the northern region they are abundant in the continental slope and towards offshore waters. Conservation priority areas were identified in the southern part of the western Mediterranean. Adding more complex cost layers and zoning to the analysis did not alter conservation priority areas, confirming such areas are highly consistent and highly important for elasmobranch protection. The marine conservation priority areas identified here can contribute to designate a proactive area-based protection strategy towards elasmobranch conservation, related species and the habitats that they depend in the western Mediterranean Sea.

A trophic latitudinal gradient revealed in anchovy and sardine from the Western Mediterranean Sea using a multi-proxy approach.

This work combines state-of-the-art methods (DNA metabarcoding) with classic approaches (visual stomach content characterization and stable isotope analyses of nitrogen (δ15N) and carbon (δ13C)) to investigate the trophic ecology of anchovy (Engraulis encrasicolus) and sardine (Sardina pilchardus) at high taxonomic and spatial resolution in the Western Mediterranean Sea. Gut contents observed are in accordance with the dietary plasticity generally described for anchovy and sardine, suggesting a diet related to the opportunistic ingestion of available prey in a certain area and/or time. Genetic tools also showed modest inter-specific differences regarding ingested species. However, inter-specific and intra-specific differences in ingested prey frequencies and prey biomass reflected a latitudinal signal that could indicate a more effective predation on large prey like krill by anchovy versus sardine, as well as a generalized higher large prey ingestion by both species southwards. In fact, both species presented lower δ15N in the northernmost area. This latitudinal gradient indicates changes in the trophic ecology of anchovy and sardine that coincide with previously described better biological conditions for fish in the southern part of the study area as well as higher landings of both species in recent years.

Accounting for preferential sampling in species distribution models.

Species distribution models (SDMs) are now being widely used in ecology for management and conservation purposes across terrestrial, freshwater, and marine realms. The increasing interest in SDMs has drawn the attention of ecologists to spatial models and, in particular, to geostatistical models, which are used to associate observations of species occurrence or abundance with environmental covariates in a finite number of locations in order to predict where (and how much of) a species is likely to be present in unsampled locations. Standard geostatistical methodology assumes that the choice of sampling locations is independent of the values of the variable of interest. However, in natural environments, due to practical limitations related to time and financial constraints, this theoretical assumption is often violated. In fact, data commonly derive from opportunistic sampling (e.g., whale or bird watching), in which observers tend to look for a specific species in areas where they expect to find it. These are examples of what is referred to as preferential sampling, which can lead to biased predictions of the distribution of the species. The aim of this study is to discuss a SDM that addresses this problem and that it is more computationally efficient than existing MCMC methods. From a statistical point of view, we interpret the data as a marked point pattern, where the sampling locations form a point pattern and the measurements taken in those locations (i.e., species abundance or occurrence) are the associated marks. Inference and prediction of species distribution is performed using a Bayesian approach, and integrated nested Laplace approximation (INLA) methodology and software are used for model fitting to minimize the computational burden. We show that abundance is highly overestimated at low abundance locations when preferential sampling effects not accounted for, in both a simulated example and a practical application using fishery data. This highlights that ecologists should be aware of the potential bias resulting from preferential sampling and account for it in a model when a survey is based on non-randomized and/or non-systematic sampling.

A spatially explicit risk assessment approach: Cetaceans and marine traffic in the Pelagos Sanctuary (Mediterranean Sea).

Spatially explicit risk assessment is an essential component of Marine Spatial Planning (MSP), which provides a comprehensive framework for managing multiple uses of the marine environment, minimizing environmental impacts and conflicts among users. In this study, we assessed the risk of the exposure to high intensity vessel traffic areas for the three most abundant cetacean species (Stenella coeruleoalba, Tursiops truncatus and Balaenoptera physalus) in the southern area of the Pelagos Sanctuary, which is the only pelagic Marine Protected Area (MPA) for marine mammals in the Mediterranean Sea. In particular, we modeled the occurrence of the three cetacean species as a function of habitat variables in June by using hierarchical Bayesian spatial-temporal models. Similarly, we modelled the marine traffic intensity in order to find high risk areas and estimated the potential conflict due to the overlap with the cetacean home ranges. Results identified two main hot-spots of high intensity marine traffic in the area, which partially overlap with the area of presence of the studied species. Our findings emphasize the need for nationally relevant and transboundary planning and management measures for these marine species.

Pollutants and parasites in bycatch teleosts from south eastern Spanish Mediterranean's fisheries: Concerns relating the foodstuff harnessing.

This research provides an evaluation of the quality and health status of some locally abundant fish species, usually otter-trawl bycatch species. The study was conducted in the southern and eastern Spanish Mediterranean coast. Mean concentration of heavy metals in muscle and parasitisation indices showed moderate levels. Higher lead concentration was found in fish from the western Alboran and arsenic, cadmium and mercury were more present on fishes from the eastern Alboran area, although most species analysed contain moderate levels of heavy metals in muscle. Concerning parasitisation, F. Anisakidae nematodes were present in all the species, except sardine. Only mercury showed a positive relationship with parasitisation. We also considered three feeding guilds. Metal mean concentrations were higher in benthivores and more littoral fishes. Pelagic planktivores species are the healthiest and the more suitable for consumers from the sanitary point of view.

Parasites of the head of Scomber colias (Osteichthyes: Scombridae) from the western Mediterranean Sea.

The metazoan parasite assemblage of the head of 30 specimens of the Atlantic chub mackerel (Scomber colias) from the western Mediterranean Sea was analysed. Eight species of parasites were found, four mazocraeid monogeneans: Grubea cochlear (prevalence = 10%), Kuhnia scombercolias (59%), K. scombri (52%), Pseudokuhnia minor (86%); three didymozoid trematodes: Nematobothrium cf. faciale (21%), N. filiforme (41%), N. scombri (7%); and one laerneopodid copepod: Clavelissa scombri (7%). Results were compared with previously published data from 14 localities of the eastern Mediterranean Sea and the Atlantic Ocean, using non-parametric univariate and multivariate analyses, and the whole parasite fauna of S. colias was compared with that of the congeners (S. australasicus, S. japonicus and S. scombrus). Parasites showed to reflect the biogeographical and phylogenetic history of host. From a methodological point of view, the use of both non-parametric univariate and multivariate techniques proved to be effective tools to detect dissimilarities between parasite assemblages.