Atlantic cod individual spatial behaviour and stable isotope associations in a no-take marine reserve.

Foraging is a behavioural process and, therefore, individual behaviour and diet are theorized to covary. However, few comparisons of individual behaviour type and diet exist in the wild. We tested whether behaviour type and diet covary in a protected population of Atlantic cod, Gadus morhua. Working in a no-take marine reserve, we could collect data on natural behavioural variation and diet choice with minimal anthropogenic disturbance. We inferred behaviour using acoustic telemetry and diet from stable isotope compositions (expressed as δ13 C and δ15 N values). We further investigated whether behaviour and diet could have survival costs. We found cod with shorter diel vertical migration distances fed at higher trophic levels. Cod δ13 C and δ15 N values scaled positively with body size. Neither behaviour nor diet predicted survival, indicating phenotypic diversity is maintained without survival costs for cod in a protected ecosystem. The links between diet and diel vertical migration highlight that future work is needed to understand whether the shifts in this behaviour during environmental change (e.g. fishing or climate), could lead to trophic cascades.

Protected areas buffer against harvest selection and rebuild phenotypic complexity.

Harvest mortality typically truncates the harvested species' size structure, thereby reducing phenotypic complexity, which can lead to reduced population productivity, increased population variability, and selection on an array of life history traits that can further alter these demographic processes. Marine protected areas (MPAs) are a potential tool to protect older, larger individuals and therefore mitigate such ecological and evolutionary effects of harvest, depending on the degree of connectivity among areas. Such MPA protection relies on a shift in size-dependent mortality, the measurement of which can therefore serve as an early indicator of whether MPAs might achieve the desired longer-term ecological and evolutionary responses. We directly measured MPA effects on size-selective mortality and associated size structure using mark-recapture data on European lobster (Homarus gammarus) collected at three MPA-control area pairs in southern Norway during one decade (n = 5,943). Mark-recapture modeling, accounting for variation in recapture probabilities, revealed (1) that annual mean survival was higher inside MPAs (0.592) vs. control areas (0.298) and (2) that significant negative relationships between survival and body size occurred at the control areas but not in the MPAs, where the effect of body size was predominantly positive. Additionally, we found (3) that mean and maximum body size increased over time inside MPAs but not in control areas. Overall, our results suggest that MPAs can rebuild phenotypic complexity (i.e., size structure) and provide protection from harvest selection.

Possible adverse impact of contaminants on Atlantic cod population dynamics in coastal ecosystems.

While many in-laboratory ecotoxicological studies have shown the adverse impact of pollutants to the fitness of an individual, direct evidence from the field on the population dynamics of wildlife animals has been lacking. Here, we provide empirical support for a negative effect of pollution on Atlantic cod (Gadus morhua) population dynamics in coastal waters of Norway by combining unique time series of juvenile cod abundance, body size, environmental concentration of toxic contaminants and a spatially structured population dynamics model. The study shows that mercury concentration might have decreased the reproductive potential of cod in the region despite the general decline in the environmental concentration of mercury, cadmium and hexachlorobenzene since the implementation of national environmental laws. However, some cod populations appeared to be more resistant to mercury pollution than others, and the strength and shape of mercury effect on cod reproductive potential was fjord-specific. Additionally, cod growth rate changed at scales smaller than fjords with a gradient related to the exposure to the open ocean and offshore cod. These spatial differences in life-history traits emphasize the importance of local adaptation in shaping the dynamics of local wildlife populations. Finally, this study highlights the possibility to mitigate pollution effects on natural populations by reducing the overall pollution level, but also reveals that pollution reduction alone is not enough to rebuild local cod populations. Cod population recovery probably requires complementary efforts on fishing regulation and habitat restoration.

Disentangling structural genomic and behavioural barriers in a sea of connectivity.

Genetic divergence among populations arises through natural selection or drift and is counteracted by connectivity and gene flow. In sympatric populations, isolating mechanisms are thus needed to limit the homogenizing effects of gene flow to allow for adaptation and speciation. Chromosomal inversions act as an important mechanism maintaining isolating barriers, yet their role in sympatric populations and divergence with gene flow is not entirely understood. Here, we revisit the question of whether inversions play a role in the divergence of connected populations of the marine fish Atlantic cod (Gadus morhua), by exploring a unique data set combining whole-genome sequencing data and behavioural data obtained with acoustic telemetry. Within a confined fjord environment, we find three genetically differentiated Atlantic cod types belonging to the oceanic North Sea population, the western Baltic population and a local fjord-type cod. Continuous behavioural tracking over 4 year revealed temporally stable sympatry of these types within the fjord. Despite overall weak genetic differentiation consistent with high levels of gene flow, we detected significant frequency shifts of three previously identified inversions, indicating an adaptive barrier to gene flow. In addition, behavioural data indicated that North Sea cod and individuals homozygous for the LG12 inversion had lower fitness in the fjord environment. However, North Sea and fjord-type cod also occupy different depths, possibly contributing to prezygotic reproductive isolation and representing a behavioural barrier to gene flow. Our results provide the first insights into a complex interplay of genomic and behavioural isolating barriers in Atlantic cod and establish a new model system towards an understanding of the role of genomic structural variants in adaptation and diversification.

Personalities influence spatial responses to environmental fluctuations in wild fish.

Although growing evidence supports the idea that animal personality can explain plasticity in response to changes in the social environment, it remains to be tested whether it can explain spatial responses of individuals in the face of natural environmental fluctuations. This is a major challenge in ecology and evolution as spatial dynamics link individual- and population-level processes. In this study, we investigated the potential of individual personalities to predict differences in fish behaviour in the wild. Specifically, our goal was to answer if individual differences in plasticity of space use to sea surface temperature could be explained by differences in personality along the reactive-proactive axis. To address this question, we first conducted repeated standard laboratory assays (i.e., open-field test, novel object test and mirror stimulation test) to assess the personality type of 76 wild-caught Atlantic cod (Gadus morhua). Next, we released the fish back into the sea and monitored their spatial behaviour over large temporal (16 months) and spatial (a whole fjord) scales, using high-resolution acoustic tracking. We demonstrate that (a) cod personality traits are structured into a proactive-reactive syndrome (proactive fish being more bold, exploratory and aggressive), (b) mean depth use of individuals is mainly driven by sea temperature and (c) personality is a significant predictor of home range changes in the wild, where reactive, but not proactive, individuals reduced their home range as sea temperature increased. These findings expand our understanding of the ecological consequences of animal personality and the mechanisms shaping spatial dynamics of animals in nature.

Fine-scale population dynamics in a marine fish species inferred from dynamic state-space models.

Identifying the spatial scale of population structuring is critical for the conservation of natural populations and for drawing accurate ecological inferences. However, population studies often use spatially aggregated data to draw inferences about population trends and drivers, potentially masking ecologically relevant population sub-structure and dynamics. The goals of this study were to investigate how population dynamics models with and without spatial structure affect inferences on population trends and the identification of intrinsic drivers of population dynamics (e.g. density dependence). Specifically, we developed dynamic, age-structured, state-space models to test different hypotheses regarding the spatial structure of a population complex of coastal Atlantic cod (Gadus morhua). Data were from a 93-year survey of juvenile (age 0 and 1) cod sampled along >200 km of the Norwegian Skagerrak coast. We compared two models: one which assumes all sampled cod belong to one larger population, and a second which assumes that each fjord contains a unique population with locally determined dynamics. Using the best supported model, we then reconstructed the historical spatial and temporal dynamics of Skagerrak coastal cod. Cross-validation showed that the spatially structured model with local dynamics had better predictive ability. Furthermore, posterior predictive checks showed that a model which assumes one homogeneous population failed to capture the spatial correlation pattern present in the survey data. The spatially structured model indicated that population trends differed markedly among fjords, as did estimates of population parameters including density-dependent survival. Recent biomass was estimated to be at a near-record low all along the coast, but the finer scale model indicated that the decline occurred at different times in different regions. Warm temperatures were associated with poor recruitment, but local changes in habitat and fishing pressure may have played a role in driving local dynamics. More generally, we demonstrated how state-space models can be used to test evidence for population spatial structure based on survey time-series data. Our study shows the importance of considering spatially structured dynamics, as the inferences from such an approach can lead to a different ecological understanding of the drivers of population declines, and fundamentally different management actions to restore populations.

Eight decades of sampling reveal a contemporary novel fish assemblage in coastal nursery habitats.

In order to adequately monitor biodiversity trends through time and their responses to natural or anthropogenic impacts, researchers require long time series that are often unavailable. This general lack of datasets that are several decades or longer makes establishing a background or baseline of diversity metrics difficult - especially when attempting to understand species composition changes against a backdrop of climate and ecological variability. Here, we present an analysis of a community of juvenile nearshore fishes based on nearly 8 decades of highly standardized Norwegian survey records. Using multivariate statistical techniques, we: (i) characterize the change in taxonomic community composition through time, (ii) determine whether there has been an increase in warm-water affinity species relative to their cold water affinity counterparts, and (iii) characterize the temporal change in the species' functional trait assemblage. Our results strongly indicate a shift toward a novel fish assemblage between the late 1990s and 2000s. The context of changes within the most recent two decades is in stark contrast to those during the 1960s and 1970s, but similar to those during the previous warm period during the 1930s and 1940s. This novel assemblage is tightly linked to the warming temperatures in the region portrayed by the increased presence of warm-water species and a higher incidence of pelagic, planktivorous species. The results indicate a clear influence of ocean temperature on the region's juvenile fish community that points to climate-mediated effects on the species assemblages of an important fish nursery area.

Temperature-associated habitat selection in a cold-water marine fish.

Habitat selection is a complex process, which involves behavioural decisions guided by the multiple needs and constraints faced by individuals. Climate-induced changes in environmental conditions may alter those trade-offs and resulting habitat use patterns. In this study, we investigated the effect of sea temperature on habitat selection and habitat use of acoustically tagged Atlantic cod (Gadus morhua) at the Norwegian Skagerrak coast. Significant relationships between ocean temperature and habitat selection and use were found. Under favourable sea temperature thresholds (<16 °C), cod selected vegetated habitats, such as eelgrass and macroalgae beds, available in shallow areas. Selection for those habitats was especially high at night, when cod tended to ascend to shallower areas, presumably to feed. Selection and use of those habitats decreased significantly as temperature rose. Under increased sea surface temperature conditions, cod were absent from vegetated shallow habitats, both during the day and night, and selected instead non-vegetated rocky bottoms and sand habitats, available in deeper, colder areas. This study shows the dynamic nature of habitat selection and strongly suggests that cod in this region have to trade off food availability against favourable temperature conditions. Future increases in ocean temperature are expected to further influence the spatial behaviour of marine fish, potentially affecting individual fitness and population dynamics.

Contrasting evolutionary demography induced by fishing: the role of adaptive phenotypic plasticity.

Mounting evidence now shows that fishing activity modifies both heritable life-history traits and ecological processes in harvested populations. However, ecological and evolutionary changes are intimately linked and can occur on the same time scale, and few studies have investigated their combined effect on fish population dynamics. Here, we contrast two population subunits of a harvested fish species in the Northeast Atlantic, the European hake (Merluccius merluccius), in the light of the emerging field of evolutionary demography, which considers the interacting processes between ecology and evolution. The two subunits experienced similar age/size truncation due to size-selective fishing, but displayed differences in key ecological processes (recruitment success) and phenotypic characteristics (maturation schedule). We investigate how temporal variation in maturation and recruitment success interactively shape the population dynamics of the two subunits. We document that the two subunits of European hake displayed different responses to fishing in maturation schedules, possibly because of the different level of adaptive phenotypic plasticity. Our results also suggest that high phenotypic plasticity can dampen the effects of fisheries-induced demographic truncation on population dynamics, whereas a population subunit characterized by low phenotypic plasticity may suffer from additive effects of ecological and life-history responses. Similar fishing pressure may thus trigger contrasting interactions between life history variation and ecological processes within the same population. The presented findings improve our understanding of how fishing impacts eco-evolutionary dynamics, which is a keystone for a more comprehensive management of harvested species.

Climate and population density drive changes in cod body size throughout a century on the Norwegian coast.

Understanding how populations respond to changes in climate requires long-term, high-quality datasets, which are rare for marine systems. We estimated the effects of climate warming on cod lengths and length variability using a unique 91-y time series of more than 100,000 individual juvenile cod lengths from surveys that began in 1919 along the Norwegian Skagerrak coast. Using linear mixed-effects models, we accounted for spatial population structure and the nested structure of the survey data to reveal opposite effects of spring and summer warming on juvenile cod lengths. Warm summer temperatures in the coastal Skagerrak have limited juvenile growth. In contrast, warmer springs have resulted in larger juvenile cod, with less variation in lengths within a cohort, possibly because of a temperature-driven contraction in the spring spawning period. A density-dependent reduction in length was evident only at the highest population densities in the time series, which have rarely been observed in the last decade. If temperatures rise because of global warming, nonlinearities in the opposing temperature effects suggest that negative effects of warmer summers will increasingly outweigh positive effects of warmer springs, and the coastal Skagerrak will become ill-suited for Atlantic cod.

Eco-evolutionary dynamics of Atlantic cod spatial behavior maintained after the implementation of a marine reserve.

The effects of marine reserves on the life history and demography of the protected populations are well-established, typically increasing population density and body size. However, little is known about how marine reserves may alter the behavior of the populations that are the target of protection. In theory, marine reserves can relax selection on spatial behavioral phenotypes that were previously targeted by the fishery and also drive selection in favor of less mobile individuals. In this study, we used acoustic telemetry to monitor the individual spatial behavior of 566 Atlantic cod (Gadus morhua Linnaeus, 1758) moving within a marine reserve and a control site in southern Norway, starting 1 year before the implementation of the marine reserve and lasting up to 9 years after. Following a before-after-control-impact approach, we investigated changes in (1) survival, (2) selection acting on behavioral traits, and (3) mean behavioral phenotypes, after the implementation of the marine reserve. We focused on three behavioral traits commonly used to describe the mobility of aquatic animals: home range size, depth position, and diel vertical migration range. Survival increased after reserve implementation, but contrary to our expectations, it subsequently decreased to preprotection levels after just 3 years. Further, we found no significance in selection patterns acting on any of the three behavioral traits after reserve implementation. Although some changes related to water column use (the tendency to occupy deeper waters) were observed in the marine reserve after 9 years, they cannot unequivocally be attributed to protection. Our results show that survival and behavioral responses to marine reserves in some cases may be more complex than previously anticipated and highlight the need for appropriately scaled management experiments and more integrated approaches to understand the effects of marine protected areas on harvested aquatic species.

Empirical support for sequential imprinting during downstream migration in Atlantic salmon (Salmo salar) smolts.

The precise homing of Atlantic salmon to their natal river and spawning grounds is the foundation for locally adapted genetically differentiated populations across rivers or across river sections. A sequential imprinting hypothesis states that salmon smolts may imprint on environmental clues along the outward migration route and then use this in reverse order to direct the spawning migration later in life. In this study, we provide empirical support for this hypothesis. PIT-tagged wild Atlantic salmon using a 2 km hydropower tunnel as downstream migrating smolts had a 18% (1SW) and 23% (2SW) lower probability of successfully migrating through the parallel river stretch as adult spawners compared to spawners that migrated through the same river stretch as smolts. These findings highlight how a fine-scale riverine migration route may be imprinted in wild Atlantic salmon smolts. From an applied perspective, these results stress the importance of not depriving smolts from parts of their migration route to ensure successful return of adults to their natal spawning grounds.

Warming Accelerates the Onset of the Molecular Stress Response and Increases Mortality of Larval Atlantic Cod.

Temperature profoundly affects ectotherm physiology. Although differential thermal responses influence fitness, thus driving population dynamics and species distributions, our understanding of the molecular architecture underlying these responses is limited, especially during the critical larval stage. Here, using RNA-sequencing of laboratory-reared Atlantic cod (Gadus morhua) larvae of wild origin, we find changes in gene expression in thousands of transcripts consistent with a severe cellular stress response at both ambient and projected (+2°C and +4°C) temperatures. In addition, specific responses to stress, heat, and hypoxia were commonly identified in gene ontology enrichment analyses and 33 of the 44 genes comprising the minimum stress proteome of all organisms were upregulated. Earlier onset of the stress response was evident at higher temperatures; concomitant increased growth and mortality suggests a reduction in fitness. Temporal differences in gene expression levels do not correspond to differences in growing degree days, suggesting negative physiological consequences of warming beyond accelerated development. Because gene expression is costly, we infer that the upregulation of thousands of transcripts in response to warming in larval cod might act as an energetic drain. We hypothesize that the energetically costly stress response, coupled with increased growth rate at warmer temperatures, leads to faster depletion of energy reserves and increased risk of mortality in larval cod. As sea surface temperatures continue to rise over the next century, reduced fitness of Atlantic cod larvae might lead to population declines in this ecologically and socioeconomically important species. Further, our findings expand our understanding of transcriptomic responses to temperature by ectothermic vertebrate larvae beyond the critical first-feeding stage, a time when organisms begin balancing the energetic demands of growth, foraging, development, and maintenance. Linking the molecular basis of a thermal response to key fitness-related traits is fundamentally important to predicting how global warming will affect ectotherms.

Hydropower-induced selection of behavioural traits in Atlantic salmon (Salmo salar).

Renewable energy projects such as hydropower facilities contribute towards meeting the world`s growing energy demands and urgent need for mitigating climate change. However, such infrastructure has the potential to substantially alter the environment which, in turn, can induce new challenges related to for instance fish migration conditions. As a consequence, local adaptations related to pre-development migration conditions may be affected for influenced populations. To explore selection regimes operating at a river hydropower plant, we monitored Atlantic salmon smolt individuals during their seaward migration. When passing the hydropower plant, the smolts chose between a surface fish passage or a submerged turbine intake. Smolts were scored for behavioural type (basal locomotor activity, net restrain (a measure of escape responses) and willingness to leave a familiar environment) prior to their migration choice, and we found that smolts with high basal activity had higher probability of using the fish passage than the turbine intake. In addition, migration route choice was a partly consistent trait in that fish that had previously passed a hydroelectric facility by using a fish passage rather than the turbine intake were significantly more likely to use it again when faced with the same choice. Higher mortality among turbine migrants could potentially reduce or eliminate particular behaviour types within populations- and the corresponding population genetic diversity that is essential to cope with future environmental challenges.

Mating patterns and determinants of individual reproductive success in brown trout (Salmo trutta) revealed by parentage analysis of an entire stream living population.

Reproductive success and its determinants are difficult to infer for wild populations of species with no parental care where behavioural observations are difficult or impossible. In this study, we characterized the breeding system and provide estimates of individual reproductive success under natural conditions for an exhaustively sampled stream-resident brown trout (Salmo trutta) population. We inferred parentage using a full probability Bayesian model that combines genetic (microsatellite) with phenotypic data. By augmenting the potential parents file with inferred parental genotypes from sib-ship analysis in cases where large families had unsampled parents, we could make more precise inference on variance of family size. We observed both polygamous and monogamous matings and large reproductive skew for both sexes, particularly in males. Correspondingly, we found evidence for sexual selection on body size for both sexes. We show that the mating system of brown trout has the potential to be very flexible and we conjecture that environmental uncertainty could be driving the evolution and perhaps select for the maintenance of plasticity of the mating system in this species.

Small-scale genetic structure in a marine population in relation to water circulation and egg characteristics.

Until the last decade it was assumed that most marine species have pronounced gene flow over vast areas, largely because of their potential for dispersal during early life stages. However, recent genetic, modeling, and field studies have shown that marine populations may be structured at scales that are inconsistent with extensive dispersal of eggs and larvae. Such findings have stimulated the birth of new studies explaining the mechanisms that promote population structure and isolation in the oceans, in the face of high potential for dispersal. Here we study the vertical and horizontal distribution of cod (Gadus morhua) eggs in relation to small-scale circulation and water column hydrography in a coastal location of southern Norway. Previous studies conducted in this region have shown that cod populations inhabiting fjord locations, which are on average 30 km apart, are genetically differentiated, a remarkable outcome considering that Atlantic cod have pelagic egg stages and long pelagic larval duration. We document that cod eggs are found in greater abundance in shallow water layers, which on average are flowing up the fjord (away from the open ocean), and in the inner portion of the fjord, which is subject to lower current speeds compared to the outer or mouth of the fjord. Eggs were found to be neutrally buoyant at shallow depths, a trait that also favors local retention, given the local circulation. The same patterns held during two environmentally contrasting years. These results strongly suggest that population structure of Atlantic cod is favored and maintained by a balance between water circulation and egg characteristics.

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.

Disentangling conditional effects of multiple regime shifts on Atlantic cod productivity.

Regime shifts are increasingly prevalent in the ecological literature. However, definitions vary and detection methods are still developing. Here, we employ a novel statistical algorithm based on the Bayesian online change-point detection framework to simultaneously identify shifts in the mean and (or) variance of time series data. We detected multiple regime shifts in long-term (59-154 years) patterns of coastal Norwegian Atlantic cod (>70% decline) and putative drivers of cod productivity: North Atlantic Oscillation (NAO); sea-surface temperature; zooplankton abundance; fishing mortality (F). The consequences of an environmental or climate-related regime shift on cod productivity are accentuated when regime shifts coincide, fishing mortality is high, and populations are small. The analyses suggest that increasing F increasingly sensitized cod in the mid 1970s and late 1990s to regime shifts in NAO, zooplankton abundance, and water temperature. Our work underscores the necessity of accounting for human-induced mortality in regime shift analyses of marine ecosystems.

Fine-scale population differences in Atlantic cod reproductive success: A potential mechanism for ecological speciation in a marine fish.

Successful resource-management and conservation outcomes ideally depend on matching the spatial scales of population demography, local adaptation, and threat mitigation. For marine fish with high dispersal capabilities, this remains a fundamental challenge. Based on daily parentage assignments of more than 4,000 offspring, we document fine-scaled temporal differences in individual reproductive success for two spatially adjacent (<10 km) populations of a broadcast-spawning marine fish. Distinguished by differences in genetics and life history, Atlantic cod (Gadus morhua) from inner- and outer-fjord populations were allowed to compete for mating and reproductive opportunities. After accounting for phenotypic variability in several traits, reproductive success of outer-fjord cod was significantly lower than that of inner-fjord cod. This finding, given that genomically different cod ecotypes inhabit inner- and outer-fjord waters, raises the intriguing hypothesis that the populations might be diverging because of ecological speciation. Individual reproductive success, skewed within both sexes (more so among males), was positively affected by body size, which also influenced the timing of reproduction, larger individuals spawning later among females but earlier among males. Our work suggests that spatial mismatches between management and biological units exist in marine fishes and that studies of reproductive interactions between putative populations or ecotypes can provide an informative basis on which determination of the scale of local adaptation can be ascertained.

Stable coexistence of genetically divergent Atlantic cod ecotypes at multiple spatial scales.

Coexistence in the same habitat of closely related yet genetically different populations is a phenomenon that challenges our understanding of local population structure and adaptation. Identifying the underlying mechanisms for such coexistence can yield new insight into adaptive evolution, diversification and the potential for organisms to adapt and persist in response to a changing environment. Recent studies have documented cryptic, sympatric populations of Atlantic cod (Gadus morhua) in coastal areas. We analysed genetic origin of 6,483 individual cod sampled annually over 14 years from 125 locations along the Norwegian Skagerrak coast and document stable coexistence of two genetically divergent Atlantic cod ecotypes throughout the study area and study period. A "fjord" ecotype dominated in numbers deep inside fjords while a "North Sea" ecotype was the only type found in offshore North Sea. Both ecotypes coexisted in similar proportions throughout coastal habitats at all spatial scales. The size-at-age of the North Sea ecotype on average exceeded that of the fjord ecotype by 20% in length and 80% in weight across all habitats. Different growth and size among individuals of the two types might be one of several ecologically significant variables that allow for stable coexistence of closely related populations within the same habitat. Management plans, biodiversity initiatives and other mitigation strategies that do not account for the mixture of species ecotypes are unlikely to meet objectives related to the sustainability of fish and fisheries.