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.

Ecological sensitivity and vulnerability of fishing fleet landings to climate change across regions.

The degree of exposure of fishing communities to environmental changes can be partially determined by the vulnerability of the target species and the landings composition. Hence, identifying the species that ecologically most contribute to the vulnerability of the landings are key steps to evaluate the risk posed by climate change. We analyse the temporal variability in intrinsic sensitivity and the ecological vulnerability of the Portuguese fisheries landings, considering the species proportions derived both from the weights and revenues. To account for the diversification of species of each fleet, we explored the species dependence of the fishery in combination with the vulnerability of them. The analyses were carried out separately for three fleet typologies and three regions. Opposite to what has been observed at a global scale, the ecological sensitivity of the fisheries landings between 1989 and 2015 did not display a decline across areas or fishing fleets. Considering each fleet independently, for trawling, where average vulnerability was lower than in the other fleets, the sensitivity of the landings increased since the 2000s. On the other hand, the high vulnerability found in multi-gear fleets was compensated by diversification of the species caught, while purse-seine fleets targeted low vulnerability species but presented a high fishery dependence on few species. The results highlight the importance of combining information on ecological vulnerability and diversification of fishing resources at a regional scale while providing a measure of the ecological exposure to climate change.

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.

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.

Modelling the spatial distribution of Sardina pilchardus and Engraulis encrasicolus spawning habitat in the NW Mediterranean Sea.

We investigated the main drivers of eggs and larvae distributions of European sardine and anchovy from the NW Mediterranean Sea. We used Generalized Additive Models and satellite environmental data. Mainly sea surface temperature, but also currents, surface height, and primary production were significantly correlated with both species' early stages distributions. Anchovy optimal temperature upper limit was not detected, but sardine eggs and larvae presented a small-ranged bell-shape curve relationship to SST with an upper SST threshold around 13 °C. Sardine spawning during winter appeared to be dependant not only on in-situ environmental conditions but also on summer conditions prior to the spawning event. Model predictions of the larval and spawning habitat distribution showed clear differences between developmental stages and between species, confirming a worsening of the sardine habitat with time. Considering the further increase of surface temperature predicted in the years to come, the survival of the sardine in the region could be compromised.

SOS small pelagics: A safe operating space for small pelagic fish in the western Mediterranean Sea.

Sustainable fishing practices must ensure human wellbeing by safeguarding the integrity of marine life-supporting systems. Unfortunately, a significant challenge to fisheries management is that sustainable fishing levels can decline, often synergistically, by co-occurring with climate-driven environmental stressors. Within one of the most impacted marine areas in the world, and encompassing a number of highly targeted commercial species, the small pelagic fish community of the western Mediterranean Sea has recently shown signs of collapse. In this study, we identify a worrying coincidence where fishing hotspots for the commercially valuable European sardine Sardina pilchardus and anchovy Engraulis encrasicolus occur in marine areas mostly affected by climate change. To identify these areas, we overlayed detailed, spatially explicit measurements of fishing pressure with the finest-scale maps of cumulative climate change impacts onto these species. According to our results, doubly impacted marine areas largely occur in the north-western Mediterranean Sea, with climate and fisheries mostly affecting European sardine. Reducing local stressors (i.e., fishing pressure) in highly impacted areas may contribute to maintain these communities within a "safe operating space" (SOS), where they remain resilient to climate change. Accordingly, the redistribution and/or reduction of fishing intensity may alleviate pressure in those areas already affected by climate change. Sustainable fishing strategies may benefit, therefore, from the SOS concept and the spatial assessments provided in this study.

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.

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.

Year-round energy dynamics of sardine and anchovy in the north-western Mediterranean Sea.

Variability in body condition and energy storage has important implications for fish recruitment and ecosystem structure. Understanding strategies for energy allocation to maintenance, reproduction and growth is essential to evaluate the state of the fish stocks. In this study, we address the energetics dynamics of the annual cycle of anchovies (Engraulis encrasicolus) and sardines (Sardina pilchardus) in the north-western Mediterranean Sea using indirect and direct condition indices. We assessed and validated the use of morphometric, biochemical and energetic indices for both species. Annual patterns of the relative condition index (Kn), gonadosomatic index (GSI), lipid content (% lipids) and energy density (ED) were linked to the energy allocation strategy. Our results highlight that anchovy mainly rely on income energy to reproduce, while sardine accumulate the energy during the resting period to be used in the reproduction period. Consequently, variability in the lipid content and ED between seasons was lower in anchovy than in sardine. In both species, we observed an early decline in energy reserves in late summer-early fall, which may be related to unfavourable environmental conditions during spring and summer. Regarding the use of different condition indices, both direct indices, lipid content and ED, were highly correlated with Kn for sardine. ED was better correlated with Kn than lipid content for anchovy. For the first time, a relationship between ED of gonads and GSI for sardine and anchovy was provided, highlighting the importance of the energy invested in reproduction. This work provides new insights into the energy dynamics of sardine and anchovy. We also demonstrate which are the most suitable indices to measure changes in the physiological condition of both species, providing tools for the future monitoring of the populations of these two commercially and ecologically important fish species.