Disparate behavioral types in wild and reared juveniles of gilthead seabream.

Fish differ consistently in behavior within the same species and population, reflecting distinct behavioral types (BTs). Comparing the behavior of wild and reared individuals provides an excellent opportunity to delve into the ecological and evolutionary consequences of BTs. In this work, we evaluated the behavioral variation of wild and reared juvenile gilthead seabreams, Sparus aurata, a highly relevant species for aquaculture and fisheries. We quantified behavioral variation along the five major axes of fish behavioral traits (exploration-avoidance, aggressiveness, sociability, shyness-boldness, and activity) using standardized behavioral tests and a deep learning tracking algorithm for behavioral annotation. Results revealed significant repeatability in all five behavior traits, suggesting high consistency of individual behavioral variation across the different axes in this species. We found reared fish to be more aggressive, social and active compared to their wild conspecifics. Reared individuals also presented less variance in their aggressiveness, lacking very aggressive and very tame individuals. Phenotypic correlation decomposition between behavioral types revealed two different behavioral syndromes: exploration-sociability and exploration-activity. Our work establishes the first baseline of repeatability scores in wild and reared gilthead seabreams, providing novel insight into the behavior of this important commercial species with implications for fisheries and aquaculture.

Food determines ephemerous and non-stable gut microbiome communities in juvenile wild and farmed Mediterranean fish.

Novel insights were provided by contrasting the composition of wild and farmed fish gut microbiomes because the latter had essentially different environmental conditions from those in the wild. This was reflected in the gut microbiome of the wild Sparus aurata and Xyrichtys novacula studied here, which showed highly diverse microbial community structures, dominated by Proteobacteria, mostly related to an aerobic or microaerophilic metabolism, but with some common shared major species, such as Ralstonia sp. On the other hand, farmed non-fasted S. aurata individuals had a microbial structure that mirrored the microbial composition of their food source, which was most likely anaerobic, since several members of the genus Lactobacillus, probably revived from the feed and enriched in the gut, dominated the communities. The most striking observation was that after a short fasting period (86 h), farmed gilthead seabream almost lost their whole gut microbiome, and the resident community associated with the mucosa had a very much reduced diversity that was highly dominated by a single potentially aerobic species Micrococcus sp., closely related to M. flavus. The results pointed to the fact that, at least for the juvenile S. aurata studied, most of the microbes in the gut were transient and highly dependent on the feed source, and that only after fasting for at least 2 days could the resident microbiome in the intestinal mucosa be determined. Since an important role of this transient microbiome in relation to fish metabolism could not be discarded, the methodological approach needs to be well designed in order not to bias the results. The results have important implications for fish gut studies that could explain the diversity and occasional contradictory results published in relation to the stability of marine fish gut microbiomes, and might provide important information for feed formulation in the aquaculture industry.

Atmospheric-ocean coupling drives prevailing and synchronic dispersal patterns of marine species with long pelagic durations.

Dispersal shapes population connectivity and plays a critical role in marine metacommunities. Prominent species for coastal socioecological systems, such as jellyfish and spiny lobsters, feature long pelagic dispersal phases (LPDPs), which have long been overlooked. Here, we use a cross-scale approach combining field surveys of these species with a high-resolution hydrodynamic model to decipher the underlying mechanisms of LPDP patterns in northwestern Mediterranean shores. We identified basin-scale prevailing dispersal routes and synchronic year-to-year patterns tightly linked to prominent circulation features typical of marginal seas and semienclosed basins, with an outstanding role of a retentive source area replenishing shores and potentially acting as a pelagic nursery area. We show how the atmospheric forcing of the ocean, a marked hydrological driver of the Mediterranean Sea, modulates dispersal routes and sources of LPDP at interannual scales. These findings represent a crucial advance in our understanding of the functioning of metapopulations of species with LPDP in marginal seas and may contribute to the effective management of coastal ecosystem services in the face of climate change.

Projected effects of ocean warming on an iconic pelagic fish and its fishery.

Increasing sea temperature is a driver of change for many fish traits, particularly for fast-growing epipelagic species with short life spans. With warming, altered spawning phenology and faster growth may produce substantially larger body sizes of the new cohort, affecting fishery productivity. We present an individual-based model (IBM) that predicts the distribution of fish length at catch under observed and projected thermal scenarios, accounting for mortality, temperature-dependent spawning phenology, temperature- and photoperiod- dependent growth. This IBM was demonstrated with Coryphaena hippurus (common dolphinfish), a circumglobally-distributed and highly thermophilic species sustaining commercial and recreational fisheries where it is present. The model projected a 13.2% increase in the average length at catch under marine heatwave conditions compared to the current thermal regime (1995-2005 average). Projections under RCP scenarios 4.5 and 8.5 by the end of the century led to 5.1% and 12.8% increase in average length, respectively. Furthermore, these thermal scenarios affected spawning phenology differently, producing higher variance in body size under RCP 8.5 scenario with respect to marine heatwave conditions. This study highlights how the environmental effects of climate change can alter the distribution of species length at catch.

Reversible morphological changes in a juvenile marine fish after exposure to predatory alarm cues.

Chemical cues from predators induce a range of predator-induced morphological defences (PIMDs) observed across fish taxa. However, the mechanisms, consistency, direction and adaptive value of PIMDs are still poorly studied. Here, we have tested if predatory cues can induce changes in the body shape of the juvenile marine fish Sparus aurata reared under controlled conditions without the presence of predators by exposing individuals to the olfactory stimulus of a fish predator. We tested our hypothesis using a nested replicated before-after-control-impact experiment, including recovery (potential reversibility) after the cessation of the predator stimulus. Differences in the size-independent body shape were explored using landmark-based geometric morphometrics and revealed that, on average, individuals exposed to a predatory cue presented deeper bodies and longer caudal regions, according to our adaptive theoretical predictions. These average plastic responses were reversible after withdrawal of the stimulus and individuals returned to average body shapes. We, therefore, provide evidence supporting innate reversible PIMDs in marine naive fish reared under controlled conditions. The effects at the individual level, including fitness and the associated applied implications, deserve further research.

Anthropogenic chemical cues can alter the swimming behaviour of juvenile stages of a temperate fish.

Human pressure on coastal areas is affecting essential ecosystems including fish nursery habitats. Among these anthropogenic uses, the seasonal increment in the pressure due to leisure activities such as coastal tourism and yachting is an important environmental stressor in many coastal zones. These pressures may elicit understudied impacts due to, for example, sunscreens or other seasonal pollutants. The island of Majorca, northwest Mediterranean Sea, experiences one of the highest number of tourist visits per capita in the world, thus the surrounding coastal habitat is subject to high anthropogenic seasonal stress. Studies on early stages of fishes have observed responses to coastal chemical cues for the selection or avoidance of habitats. However, the potential interferences of human impacts on these signals are largely unknown. A choice chamber was used to determine water type preference and behaviour in naïve settled juvenile gilt-head sea bream (Sparus aurata), a temperate species of commercial interest. Fish were tested individually for behavioural changes with respect to water types from potential beneficial habitats, such as seawater with extract of the endemic seagrass Posidonia oceanica, anthropogenically influenced habitats such as water extracted from a commercial and recreational harbour and seawater mixed with sunscreen at concentrations observed in coastal waters. Using a Bayesian approach, we investigated a) water type preference; b) mean speed; and c) variance in the movement (as an indicator of burst swimming activity, or "sprint" behaviour) as behavioural descriptors with respect to water type. Fish spent similar percentage of time in treatment and control water types. However, movement descriptors showed that fish in sunscreen water moved slower (98.43% probability of being slower) and performed fewer sprints (90.1% probability of having less burst in speed) compared to control water. Less evident increases in sprints were observed in harbour water (73.56% more sprints), and seagrass (79.03% more) in comparison to control water. When seagrass water was tested against harbour water, the latter elicited a higher number of sprints (91.66% increase). We show that juvenile gilt-head seabream are able to react to a selection of naturally occurring chemically different odourscapes, including the increasingly important presence of sunscreen products, and provide a plausible interpretation of the observed behavioural patterns.

Oceanographic drivers and mistiming processes shape breeding success in a seabird.

Understanding the processes driving seabirds' reproductive performance through trophic interactions requires the identification of seasonal pulses in marine productivity. We investigated the sequence of environmental and biological processes driving the reproductive phenology and performance of the storm petrel (Hydrobates pelagicus) in the Western Mediterranean. The enhanced light and nutrient availability at the onset of water stratification (late winter/early spring) resulted in annual consecutive peaks in relative abundance of phytoplankton, zooplankton and ichthyoplankton. The high energy-demanding period of egg production and chick rearing coincided with these successive pulses in food availability, pointing to a phenological adjustment to such seasonal patterns with important fitness consequences. Indeed, delayed reproduction with respect to the onset of water stratification resulted in both hatching and breeding failure. This pattern was observed at the population level, but also when confounding factors such as individuals' age or experience were also accounted for. We provide the first evidence of oceanographic drivers leading to the optimal time-window for reproduction in an inshore seabird at southern European latitudes, along with a suitable framework for assessing the impact of environmentally driven changes in marine productivity patterns in seabird performance.

Ocean acidification increases fatty acids levels of larval fish.

Rising levels of anthropogenic carbon dioxide in the atmosphere are acidifying the oceans and producing diverse and important effects on marine ecosystems, including the production of fatty acids (FAs) by primary producers and their transfer through food webs. FAs, particularly essential FAs, are necessary for normal structure and function in animals and influence composition and trophic structure of marine food webs. To test the effect of ocean acidification (OA) on the FA composition of fish, we conducted a replicated experiment in which larvae of the marine fish red drum (Sciaenops ocellatus) were reared under a climate change scenario of elevated CO2 levels (2100 µatm) and under current control levels (400 µatm). We found significantly higher whole-body levels of FAs, including nine of the 11 essential FAs, and altered relative proportions of FAs in the larvae reared under higher levels of CO2. Consequences of this effect of OA could include alterations in performance and survival of fish larvae and transfer of FAs through food webs.

Recruiting at the edge: kinetic energy inhibits anchovy populations in the western Mediterranean.

The Strait of Gibraltar replenishes the Mediterranean with Atlantic waters through an intense eastward current known as the Atlantic Jet (AJ). The AJ fertilizes the southwestern Mediterranean and is considered to be the ultimate factor responsible for the comparatively high fish production of this region. Here, we perform an analysis of the available historical catches and catch per unit effort (CPUE), together with a long series of surface currents, kinetic energy and chlorophyll concentration. We show that the high kinetic energy of the AJ increases primary production but also negatively impacts the recruitment of anchovy. We contend that anchovy recruitment in the region is inhibited by the advection and dispersion of larvae and post-larvae during periods of strong advection by the AJ. The inhibitory impact of kinetic energy on anchovy landings is not a transient but rather a persistent state of the system. An exceptional combination of events creates an outbreak of this species in the Alboran Sea. These events depend on the Mediterranean-Atlantic exchange of water masses and, therefore, are highly sensitive to climate changes that are projected, though not always negatively, for fish landings.