Otolith morphogenesis during the early life stages of fish is temperature-dependent: Validation by experimental approach applied to European seabass (Dicentrarchus labrax).

Otolith shape is often used as a tool in fish stock identification. The goal of this study was to experimentally assess the influence of changing temperature and ontogenic evolution on the shape component of the European seabass (Dicentrarchus labrax) otolith during early-life stages. A total of 1079 individuals were reared in a water temperature of 16°C up to 232 days post hatch (dph). During this experiment, several specimens were transferred into tanks with a water temperature of 21°C to obtain at the end of this study four different temperature treatments, each with varying ratios between the number of days at 16 and 21°C. To evaluate the otolith morphogenesis, samples were examined at 43, 72, 86 and 100 dph. The evolution of normalized otolith shape from hatching up to 100 dph showed that there were two main successive changes. First, faster growth in the antero-posterior axis than in the dorso-ventral axis changed the circular-shaped otolith from that observed at hatching and, second, increasing the complexity relating to the area between the rostrum and the anti-rostrum. To test the effect of changing temperature, growing degree-day was used in three linear mixed-effect models. Otolith morphogenesis was positively correlated to growing degree-day, but was also dependent on temperature level. Otolith shape is influenced by environmental factors, particularly temperature, making it an efficient tool for fish stock identification.

Hypoxia tolerance of common sole juveniles depends on dietary regime and temperature at the larval stage: evidence for environmental conditioning.

An individual's environmental history may have delayed effects on its physiology and life history at later stages in life because of irreversible plastic responses of early ontogenesis to environmental conditions. We chose a marine fish, the common sole, as a model species to study these effects, because it inhabits shallow marine areas highly exposed to environmental changes. We tested whether temperature and trophic conditions experienced during the larval stage had delayed effects on life-history traits and resistance to hypoxia at the juvenile stage. We thus examined the combined effect of global warming and hypoxia in coastal waters, which are potential stressors to many estuarine and coastal marine fishes. Elevated temperature and better trophic conditions had a positive effect on larval growth and developmental rates; warmer larval temperature had a delayed positive effect on body mass and resistance to hypoxia at the juvenile stage. The latter suggests a lower oxygen demand of individuals that had experienced elevated temperatures during larval stages. We hypothesize that an irreversible plastic response to temperature occurred during early ontogeny that allowed adaptive regulation of metabolic rates and/or oxygen demand with long-lasting effects. These results could deeply affect predictions about impacts of global warming and eutrophication on marine organisms.

Predictive systems ecology.

Human societies, and their well-being, depend to a significant extent on the state of the ecosystems that surround them. These ecosystems are changing rapidly usually in response to anthropogenic changes in the environment. To determine the likely impact of environmental change on ecosystems and the best ways to manage them, it would be desirable to be able to predict their future states. We present a proposal to develop the paradigm of predictive systems ecology, explicitly to understand and predict the properties and behaviour of ecological systems. We discuss the necessary and desirable features of predictive systems ecology models. There are places where predictive systems ecology is already being practised and we summarize a range of terrestrial and marine examples. Significant challenges remain but we suggest that ecology would benefit both as a scientific discipline and increase its impact in society if it were to embrace the need to become more predictive.

Estimating age at maturation and energy-based life-history traits from individual growth trajectories with nonlinear mixed-effects models.

A new method is presented to estimate individuals' (1) age at maturation, (2) energy acquisition rate, (3) energy expenditure for body maintenance, and (4) reproductive investment, and the multivariate distribution of these traits in a population. The method relies on adjusting a conceptual energy allocation model to individual growth curves using nonlinear mixed-effects modelling. The method's performance was tested using simulated growth curves for a range of life-history types. Individual age at maturation, energy acquisition rate and the sum of maintenance and reproductive investment rates, and their multivariate distribution, were accurately estimated. For the estimation of maintenance and reproductive investment rates separately, biases were observed for life-histories with a large imbalance between these traits. For low reproductive investment rates and high maintenance rates, reproductive investment rate estimates were strongly biased whereas maintenance rate estimates were not, the reverse holding in the opposite situation. The method was applied to individual growth curves back-calculated from otoliths of North Sea plaice (Pleuronectes platessa) and from scales of Norwegian spring spawning herring (Clupea harengus). For plaice, maturity ogives derived from our individual estimates of age at maturation were almost identical to the maturity ogives based on gonad observation in catch samples. For herring, we observed 51.5% of agreement between our individual estimates and those directly obtained from scale reading, with a difference lower than 1 year in 97% of cases. We conclude that the method is a powerful tool to estimate the distribution of correlated life-history traits for any species for which individual growth curves are available.

Different mechanisms underpin the decline in growth of anchovies and sardines of the Bay of Biscay.

Declines in individuals' growth in exploited fish species are generally attributed to evolutionary consequences of size-selective fishing or to plastic responses due to constraints set by changing environmental conditions dampening individuals' growth. However, other processes such as growth compensation and non-directional selection can occur and their importance on the overall phenotypic response of exploited populations has largely been ignored. Using otolith growth data collected in European anchovy and sardine of the Bay of Biscay (18 cohorts from 2000 to 2018), we parameterized the breeder's equation to determine whether declines in size-at-age in these species were due to an adaptive response (i.e. related to directional or non-directional selection differentials within parental cohorts) or a plastic response (i.e. related to changes in environmental). We found that growth at age-0 in anchovy declined between parents and their offspring when biomass increased and the selective disappearance of large individuals was high in parents. Therefore, an adaptive response probably occurred in years with high fishing effort and the large increase in biomass after the collapse of this stock maintained this adaptive response subsequently. In sardine offspring, higher growth at age-0 was associated with increasing biomass between parents and offspring, suggesting a plastic response to a bottom-up process (i.e. a change in food quantity or quality). Parental cohorts in which selection favoured individuals with high growth compensation produced offspring high catch up growth rates, which may explain the smaller decline in growth in sardine relative to anchovy. Finally, on non-directional selection differentials were not significantly related to the changes in growth at age-0 and growth compensation at age-1 in both species. Although anchovy and sardine have similar ecologies, the mechanisms underlying the declines in their growth are clearly different. The consequences of the exploitation of natural populations could be long lasting if density-dependent processes follow adaptive changes.

Impact of environmental covariation in growth and mortality on evolving maturation reaction norms.

Maturation age and size have important fitness consequences through their effects on survival probabilities and body sizes. The evolution of maturation reaction norms in response to environmental covariation in growth and mortality is therefore a key subject of life-history theory. The eco-evolutionary model we present and analyze here incorporates critical features that earlier studies of evolving maturation reaction norms have often neglected: the trade-off between growth and reproduction, source-sink population structure, and population regulation through density-dependent growth and fecundity. We report the following findings. First, the evolutionarily optimal age at maturation can be decomposed into the sum of a density-dependent and a density-independent component. These components measure, respectively, the hypothetical negative age at which an individual's length would be 0 and the delay in maturation relative to this offset. Second, along any growth trajectory, individuals mature earlier when mortality is higher. This allows us to deduce, third, how the shapes of evolutionarily optimal maturation reaction norms depend on the covariation between growth and mortality (positive or negative, linear or curvilinear, and deterministic or probabilistic). Providing eco-evolutionary explanations for many alternative reaction-norm shapes, our results appear to be in good agreement with current empirical knowledge on maturation dynamics.

New scale analyses reveal centenarian African coelacanths.

The extant coelacanth was discovered in 1938;1 its biology and ecology remain poorly known due to the low number of specimens collected. Only two previous studies1,2 have attempted to determine its age and growth. They suggested a maximum lifespan of 20 years, placing the coelacanth among the fastest growing marine fish. These findings are at odds with the coelacanth's other known biological features including low oxygen-extraction capacity, slow metabolism, ovoviviparity, and low fecundity, typical of fish with slow life histories and slow growth. In this study, we use polarized light microscopy to study growth on scales based on a large sample of 27 specimens. Our results demonstrate for the first time nearly imperceptible annual calcified structures (circuli) on the scales and show that maximal age of the coelacanth was underestimated by a factor of 5. Our validation method suggests that circuli are indeed annual, thus supporting that the coelacanth is among the longest-living fish species, its lifespan being probably around 100 years. Like deep-sea sharks with a reduced metabolism, the coelacanth has among the slowest growth for its size. Further reappraisals of age at first sexual maturity (in the range 40 to 69 years old) and gestation duration (of around 5 years) show that the living coelacanth has one of the slowest life histories of all marine fish and possibly the longest gestation. As long-lived species with slow life histories are extremely vulnerable to natural and anthropogenic perturbations, our results suggest that coelacanths may be more threatened than previously considered.

Plasticity of trophic interactions in fish assemblages results in temporal stability of benthic-pelagic couplings.

This study addresses the temporal variability of couplings between pelagic and benthic habitats for fish assemblages at five periods in a shallow epicontinental sea, the Eastern English Channel (EEC). Organic matter fluxes fueling fish assemblages and the relative contribution of their different sources were assessed using stable isotope analysis and associated isotopic functional metrics. Couplings between benthic and pelagic realms appeared to be a permanent feature in the EEC, potentially favored by shallow depth and driven by the combination of two trophic processes. First, trophic interactions exhibited plasticity and revealed resource partitioning. Second, changes in the composition of fish assemblages did not impact benthic-pelagic couplings, as most dominant species were generalists during at least one time period, allowing complete use of available resources. Examining both unweighted and biomass-weighted indices was complementary and permitted a better understanding of trophic interactions and energy fluxes.

Maturation trends indicative of rapid evolution preceded the collapse of northern cod.

Northern cod, comprising populations of Atlantic cod (Gadus morhua) off southern Labrador and eastern Newfoundland, supported major fisheries for hundreds of years. But in the late 1980s and early 1990s, northern cod underwent one of the worst collapses in the history of fisheries. The Canadian government closed the directed fishing for northern cod in July 1992, but even after a decade-long offshore moratorium, population sizes remain historically low. Here we show that, up until the moratorium, the life history of northern cod continually shifted towards maturation at earlier ages and smaller sizes. Because confounding effects of mortality changes and growth-mediated phenotypic plasticity are accounted for in our analyses, this finding strongly suggests fisheries-induced evolution of maturation patterns in the direction predicted by theory. We propose that fisheries managers could use the method described here as a tool to provide warning signals about changes in life history before more overt evidence of population decline becomes manifest.

Complementarity and discriminatory power of genotype and otolith shape in describing the fine-scale population structure of an exploited fish, the common sole of the Eastern English Channel.

Marine organisms show population structure at a relatively fine spatial scale, even in open habitats. The tools commonly used to assess subtle patterns of connectivity have diverse levels of resolution and can complement each other to inform on population structure. We assessed and compared the discriminatory power of genetic markers and otolith shape to reveal the population structure on evolutionary and ecological time scales of the common sole (Solea solea), living in the Eastern English Channel (EEC) stock off France and the UK. First, we genotyped fish with Single Nucleotide Polymorphisms to assess population structure at an evolutionary scale. Then, we tested for spatial segregation of the subunits using otolith shape as an integrative tracer of life history. Finally, a supervised machine learning framework was applied to genotypes and otolith phenotypes to probabilistically assign adults to subunits and assess the discriminatory power of each approach. Low but significant genetic differentiation was found among subunits. Moreover, otolith shape appeared to vary spatially, suggesting spatial population structure at fine spatial scale. However, results of the supervised discriminant analyses failed to discriminate among subunits, especially for otolith shape. We suggest that the degree of population segregation may not be strong enough to allow for robust fish assignments. Finally, this study revealed a weak yet existing metapopulation structure of common sole at the fine spatial scale of the EEC based on genotypes and otolith shape, with one subunit being more isolated. Our study argues for the use of complementary tracers to investigate marine population structure.

Fish life-history traits are affected after chronic dietary exposure to an environmentally realistic marine mixture of PCBs and PBDEs.

Polychlorinated biphenyls (PCBs) and polybrominated diphenyl ethers (PBDEs) are persistent organic pollutants that have been shown to affect fish life-history traits such as reproductive success, growth and survival. At the individual level, their toxicity and underlying mechanisms of action have been studied through experimental exposure. However, the number of experimental studies approaching marine environmental situations is scarce, i.e., in most cases, individuals are exposed to either single congeners, or single types of molecules, or high concentrations, so that results can hardly be transposed to natural populations. In the present study, we evaluated the effect of chronic dietary exposure to an environmentally realistic marine mixture of PCB and PBDE congeners on zebrafish life-history traits from larval to adult stage. Exposure was conducted through diet from the first meal and throughout the life cycle of the fish. The mixture was composed so as to approach environmentally relevant marine conditions in terms of both congener composition and concentrations. Life-history traits of exposed fish were compared to those of control individuals using several replicate populations in each treatment. We found evidence of slower body growth, but to a larger asymptotic length, and delayed spawning probability in exposed fish. In addition, offspring issued from early spawning events of exposed fish exhibited a lower larval survival under starvation condition. Given their strong dependency on life-history traits, marine fish population dynamics and associated fisheries productivity for commercial species could be affected by such individual-level effects of PCBs and PBDEs on somatic growth, spawning probability and larval survival.

Moderate hypoxia but not warming conditions at larval stage induces adverse carry-over effects on hypoxia tolerance of European sea bass (Dicentrarchus labrax) juveniles.

Environmental conditions, to which organisms are exposed during all their life, may cause possible adaptive responses with consequences in their subsequent life-history trajectory. The objective of this study was to investigate whether ecologically relevant combinations of hypoxia (40% and 100% air saturation) and temperature (15° and 20 °C), occurring during the larval period of European sea bass larvae (Dicentrarchus labrax), could have long-lasting impacts on the physiology of resulting juveniles. Hypoxic challenge tests were performed over one year to give an integrative evaluation of physiological performance. We revealed that juvenile performance was negatively impacted by hypoxia but not by the thermal conditions experienced at larval stage. This impact was related to the prevalence of opercular abnormalities. The present study indicates that exposure to a moderate hypoxia event during larval stage may have adverse carry-over effects, which could compromise fitness and population recruitment success.

Underestimation of chemical contamination in marine fish muscle tissue can be reduced by considering variable wet:dry weight ratios.

Whether considered as a risk for human health or as ecological tracers, contaminants' concentrations measured in fish muscles are commonly expressed relative to wet or dry mass. Comparison of results required conversion factors (CF) but accurate values are scarce and case-specific. The present paper is aimed at investigating errors linked with the use of the theoretical value. Muscles dry and wet masses were measured in 15 fish species to determine the actual CF. Most CF were lower than the theoretical wet:dry ratio of 5 classically used, with variations at individual and species level. Muscle lipid content (inferred by C/N ratios) was a crucial factor explaining discrepancies, claiming for caution when working with lipid-rich species. The observed variability demonstrated that using the theoretical CF may be inaccurate, when actual CF largely differs from the theoretical value. Dedicated measurement is the better approach when accuracy is required.

Fisheries-induced neutral and adaptive evolution in exploited fish populations and consequences for their adaptive potential.

Fishing may induce neutral and adaptive evolution affecting life-history traits, and molecular evidence has shown that neutral genetic diversity has declined in some exploited populations. Here, we theoretically study the interplay between neutral and adaptive evolution caused by fishing. An individual-based eco-genetic model is devised that includes neutral and functional loci in a realistic ecological setting. In line with theoretical expectations, we find that fishing induces evolution towards slow growth, early maturation at small size and higher reproductive investment. We show, first, that the choice of genetic model (based on either quantitative genetics or gametic inheritance) influences the evolutionary recovery of traits after fishing ceases. Second, we analyse the influence of three factors possibly involved in the lack of evolutionary recovery: the strength of selection, the effect of genetic drift and the loss of adaptive potential. We find that evolutionary recovery is hampered by an association of weak selection differentials with reduced additive genetic variances. Third, the contribution of fisheries-induced selection to the erosion of functional genetic diversity clearly dominates that of genetic drift only for the traits related to maturation. Together, our results highlight the importance of taking into account population genetic variability in predictions of eco-evolutionary dynamics.

Regime Shift in an Exploited Fish Community Related to Natural Climate Oscillations.

Identifying the various drivers of marine ecosystem regime shifts and disentangling their respective influence are critical tasks for understanding biodiversity dynamics and properly managing exploited living resources such as marine fish communities. Unfortunately, the mechanisms and forcing factors underlying regime shifts in marine fish communities are still largely unknown although climate forcing and anthropogenic pressures such as fishing have been suggested as key determinants. Based on a 24-year-long time-series of scientific surveys monitoring 55 fish and cephalopods species, we report here a rapid and persistent structural change in the exploited fish community of the eastern English Channel from strong to moderate dominance of small-bodied forage fish species with low temperature preferendum that occurred in the mid-1990s. This shift was related to a concomitant warming of the North Atlantic Ocean as attested by a switch of the Atlantic Multidecadal Oscillation from a cold to a warm phase. Interestingly, observed changes in the fish community structure were opposite to those classically induced by exploitation as larger fish species of higher trophic level increased in abundance. Despite not playing a direct role in the regime shift, fishing still appeared as a forcing factor affecting community structure. Moreover, although related to climate, the regime shift may have been facilitated by strong historic exploitation that certainly primed the system by favoring the large dominance of small-bodied fish species that are particularly sensitive to climatic variations. These results emphasize that particular attention should be paid to multidecadal natural climate variability and its interactions with both fishing and climate warming when aiming at sustainable exploitation and ecosystem conservation.

Adaptive changes in harvested populations: plasticity and evolution of age and size at maturation.

We investigate harvest-induced adaptive changes in age and size at maturation by modelling both plastic variation and evolutionary trajectories. Harvesting mature individuals displaces the reaction norm for age and size at maturation toward older ages and larger sizes and rotates it clockwise, whereas harvesting immature individuals has the reverse qualitative effect. If both immature and mature individuals are harvested, the net effect has approximately the same trend as when harvesting immature individuals only. This stems from the sensitivity of the evolutionary response, which depends on the maturity state of harvested individuals, but also on the type of harvest mortality (negatively or positively density dependent, density independent) and the value of three life-history parameters (natural mortality, growth rate and the trade-off between growth and reproduction). Evolutionary changes in the maturation reaction norm have strong repercussions for the mean size and the density of harvested individuals that, in most cases, result in the reduction of biomass--a response that population dynamical models would overlook. These results highlight the importance of accounting for evolutionary trends in the long-term management of exploited living resources and give qualitative insights into how to minimize the detrimental consequences of harvest-induced evolutionary changes in maturation reaction norms.

[Sounds recorded in salt marshes and attributed to the European eel]. / Emissions sonores enregistrées en marais salé et attribuées a l'anguille européenne.

The sounds were recorded in coastal ponds off the French Atlantic coast. They are characterized by continuous series of regularly spaced sounds, each sound being composed of one to four pulses of 7.8-ms duration. The main frequencies of these sounds are under 350 Hz. Due to the special characteristics of these sounds, their temporal patterning, their coastal pond provenance and their close similarity to sounds made by the American eel (Anguilla rostrata), we attribute them to the European eel (Anguilla anguilla).

Evolutionary impact assessment: accounting for evolutionary consequences of fishing in an ecosystem approach to fisheries management.

Managing fisheries resources to maintain healthy ecosystems is one of the main goals of the ecosystem approach to fisheries (EAF). While a number of international treaties call for the implementation of EAF, there are still gaps in the underlying methodology. One aspect that has received substantial scientific attention recently is fisheries-induced evolution (FIE). Increasing evidence indicates that intensive fishing has the potential to exert strong directional selection on life-history traits, behaviour, physiology, and morphology of exploited fish. Of particular concern is that reversing evolutionary responses to fishing can be much more difficult than reversing demographic or phenotypically plastic responses. Furthermore, like climate change, multiple agents cause FIE, with effects accumulating over time. Consequently, FIE may alter the utility derived from fish stocks, which in turn can modify the monetary value living aquatic resources provide to society. Quantifying and predicting the evolutionary effects of fishing is therefore important for both ecological and economic reasons. An important reason this is not happening is the lack of an appropriate assessment framework. We therefore describe the evolutionary impact assessment (EvoIA) as a structured approach for assessing the evolutionary consequences of fishing and evaluating the predicted evolutionary outcomes of alternative management options. EvoIA can contribute to EAF by clarifying how evolution may alter stock properties and ecological relations, support the precautionary approach to fisheries management by addressing a previously overlooked source of uncertainty and risk, and thus contribute to sustainable fisheries.

Size-selective fishing gear and life history evolution in the Northeast Arctic cod.

Industrial fishing has been identified as a cause for life history changes in many harvested stocks, mainly because of the intense fishing mortality and its size-selectivity. Because these changes are potentially evolutionary, we investigate evolutionarily stable life-histories and yield in an energy-allocation state-dependent model for Northeast Arctic cod Gadus morhua. We focus on the evolutionary effects of size-selective fishing because regulation of gear selectivity may be an efficient management tool. Trawling, which harvests fish above a certain size, leads to early maturation except when fishing is low and confined to mature fish. Gillnets, where small and large fish escape, lead to late maturation for low to moderate harvest rates, but when harvest rates increase maturation age suddenly drops. This is because bell-shaped selectivity has two size-refuges, for fish that are below and above the harvestable size-classes. Depending on the harvest rate it either pays to grow through the harvestable slot and mature above it, or mature small below it. Sustainable yield on the evolutionary time-scale is highest when fishing is done by trawling, but only for a small parameter region. Fishing with gillnets is better able to withstand life-history evolution, and maintains yield over a wider range of fishing intensities.