Declines in body size of sockeye salmon associated with increased competition in the ocean.

Declining body sizes have been documented for several species of Pacific salmon; however, whether size declines are caused mainly by ocean warming or other ecological factors, and whether they result primarily from trends in age at maturation or changing growth rates remain poorly understood. We quantified changes in mean body size and contributions from shifting size-at-age and age structure of mature sockeye salmon returning to Bristol Bay, Alaska, over the past 60 years. Mean length declined by 3%, corresponding to a 10% decline in mean body mass, since the early 1960s, though much of this decline occurred since the early 2000s. Changes in size-at-age were the dominant cause of body size declines and were more consistent than trends in age structure among the major rivers that flow into Bristol Bay. Annual variation in size-at-age was largely explained by competition among Bristol Bay sockeye salmon and interspecific competition with other salmon in the North Pacific Ocean. Warm winters were associated with better growth of sockeye salmon, whereas warm summers were associated with reduced growth. Our findings point to competition at sea as the main driver of sockeye salmon size declines, and emphasize the trade-off between fish abundance and body size.

Age structure affects population productivity in an exploited fish species.

Long-term changes in the age and size structure of animal populations are well documented, yet their impacts on population productivity are poorly understood. Fishery exploitation can be a major driver of changes in population age-size structure because fisheries significantly increase mortality and often selectively remove larger and older fish. Climate change is another potential driver of shifts in the demographic structure of fish populations. Northeast Arctic (NEA) cod is the largest population of Atlantic cod (Gadus morhua) and one of the world's most important commercial fish stocks. This population has experienced considerable changes in population age-size structure over the past century, largely in response to fishing. In this study, we investigate whether changes in spawner age structure have affected population productivity in NEA cod, measured as recruits per spawning stock biomass, over the past 75 years. We find evidence that shifts in age structure toward younger spawners negatively affect population productivity, implying higher recruitment success when the spawning stock is composed of older individuals. The positive effect of an older spawning stock is likely linked to maternal effects and higher reproductive output of larger females. Our results indicate a threefold difference in productivity between the youngest and oldest spawning stock that has been observed since the 1950s. Further, our results suggest a positive effect of environmental temperature and a negative effect of intraspecific cannibalism by older juveniles on population productivity, which partly masked the effect of spawner age structure unless accounted for in the model. Collectively, these findings emphasize the importance of population age structure for the productivity of fish populations and suggest that harvest-induced demographic changes can have negative feedbacks for fisheries that lead to a younger spawning stock. Incorporating demographic data into harvest strategies could thus facilitate sustainable fishery management.

Optimum growth temperature declines with body size within fish species.

According to the temperature-size rule, warming of aquatic ecosystems is generally predicted to increase individual growth rates but reduce asymptotic body sizes of ectotherms. However, we lack a comprehensive understanding of how growth and key processes affecting it, such as consumption and metabolism, depend on both temperature and body mass within species. This limits our ability to inform growth models, link experimental data to observed growth patterns, and advance mechanistic food web models. To examine the combined effects of body size and temperature on individual growth, as well as the link between maximum consumption, metabolism, and body growth, we conducted a systematic review and compiled experimental data on fishes from 52 studies that combined body mass and temperature treatments. By fitting hierarchical models accounting for variation between species, we estimated how maximum consumption and metabolic rate scale jointly with temperature and body mass within species. We found that whole-organism maximum consumption increases more slowly with body mass than metabolism, and is unimodal over the full temperature range, which leads to the prediction that optimum growth temperatures decline with body size. Using an independent dataset, we confirmed this negative relationship between optimum growth temperature and body size. Small individuals of a given population may, therefore, exhibit increased growth with initial warming, whereas larger conspecifics could be the first to experience negative impacts of warming on growth. These findings help advance mechanistic models of individual growth and food web dynamics and improve our understanding of how climate warming affects the growth and size structure of aquatic ectotherms.

Non-stationary and interactive effects of climate and competition on pink salmon productivity.

Pacific salmon (Oncorhynchus spp.) are exposed to increased environmental change and multiple human stressors. To anticipate future impacts of global change and to improve sustainable resource management, it is critical to understand how wild salmon populations respond to stressors associated with human-caused changes such as climate warming and ocean acidification, as well as competition in the ocean, which is intensified by the large-scale production and release of hatchery reared salmon. Pink salmon (O. gorbuscha) are a keystone species in the North Pacific Ocean and support highly valuable commercial fisheries. We investigated the joint effects of changes in ocean conditions and salmon abundances on the productivity of wild pink salmon. Our analysis focused on Prince William Sound in Alaska, because the region accounts for ~50% of the global production of hatchery pink salmon with local hatcheries releasing 600-700 million pink salmon fry annually. Using 60 years of data on wild pink salmon abundances, hatchery releases, and ecological conditions in the ocean, we find evidence that hatchery pink salmon releases negatively affect wild pink salmon productivity, likely through competition between wild and hatchery juveniles in nearshore marine habitats. We find no evidence for effects of ocean acidification on pink salmon productivity. However, a change in the leading mode of North Pacific climate in 1988-1989 weakened the temperature-productivity relationship and altered the strength of intraspecific density dependence. Therefore, our results suggest non-stationary (i.e., time varying) and interactive effects of ocean climate and competition on pink salmon productivity. Our findings further highlight the need for salmon management to consider potential adverse effects of large-scale hatchery production within the context of ocean change.

Resurgence of an apex marine predator and the decline in prey body size.

In light of recent recoveries of marine mammal populations worldwide and heightened concern about their impacts on marine food webs and global fisheries, it has become increasingly important to understand the potential impacts of large marine mammal predators on prey populations and their life-history traits. In coastal waters of the northeast Pacific Ocean, marine mammals have increased in abundance over the past 40 to 50 y, including fish-eating killer whales that feed primarily on Chinook salmon. Chinook salmon, a species of high cultural and economic value, have exhibited marked declines in average size and age throughout most of their North American range. This raises the question of whether size-selective predation by marine mammals is generating these trends in life-history characteristics. Here we show that increased predation since the 1970s, but not fishery selection alone, can explain the changes in age and size structure observed for Chinook salmon populations along the west coast of North America. Simulations suggest that the decline in mean size results from the selective removal of large fish and an evolutionary shift toward faster growth and earlier maturation caused by selection. Our conclusion that intensifying predation by fish-eating killer whales contributes to the continuing decline in Chinook salmon body size points to conflicting management and conservation objectives for these two iconic species.

Effects of warming climate and competition in the ocean for life-histories of Pacific salmon.

The life-histories of exploited fish species, such as Pacific salmon, are vulnerable to a wide variety of anthropogenic stressors including climate change, selective exploitation and competition with hatchery releases for finite foraging resources. However, these stressors may generate unexpected changes in life-histories due to developmental linkages when species complete their migratory life cycle in different habitats. We used multivariate time-series models to quantify changes in the prevalence of different life-history strategies of sockeye salmon from Bristol Bay, Alaska, over the past half-century-specifically, how they partition their lives between freshwater habitats and the ocean. Climate warming has decreased the time spent by salmon in their natal freshwater habitat, as climate-enhanced growth opportunities have enabled earlier migration to the ocean. Migration from freshwater at a younger age, and increasing competition from wild and hatchery-released salmon, have tended to delay maturation toward the salmon spending an additional year feeding in the ocean. Models evaluating the effects of size-selective fishing on these patterns had only small support. These stressors combine to reduce the size-at-age of fish vulnerable to commercial fisheries and have increasingly favoured a single-age class, potentially affecting the age class complexity that stabilizes this highly reliable resource.

Size-based ecological interactions drive food web responses to climate warming.

Predicting climate change impacts on animal communities requires knowledge of how physiological effects are mediated by ecological interactions. Food-dependent growth and within-species size variation depend on temperature and affect community dynamics through feedbacks between individual performance and population size structure. Still, we know little about how warming affects these feedbacks. Using a dynamic stage-structured biomass model with food-, size- and temperature-dependent life history processes, we analyse how temperature affects coexistence, stability and size structure in a tri-trophic food chain, and find that warming effects on community stability depend on ecological interactions. Predator biomass densities generally decline with warming - gradually or through collapses - depending on which consumer life stage predators feed on. Collapses occur when warming induces alternative stable states via Allee effects. This suggests that predator persistence in warmer climates may be lower than previously acknowledged and that effects of warming on food web stability largely depend on species interactions.

Recruitment variation disrupts the stability of alternative life histories in an exploited salmon population.

Males of many fish species exhibit alternative reproductive tactics, which can influence the maturation schedules, fishery productivity, and resilience to harvest of exploited populations. While alternative mating phenotypes can persist in stable equilibria through frequency-dependent selection, shifts in tactic frequencies have been observed and can have substantial consequences for fisheries. Here, we examine the dynamics of precocious sneaker males called "jacks" in a population of sockeye salmon (Oncorhynchus nerka) from Frazer Lake, Alaska. Jacks, which are of little commercial value due to their small body sizes, have recently been observed at unusually high levels in this stock, degrading the value of regional fisheries. To inform future strategies for managing the prevalence of jacks, we used long-term monitoring data to identify what regulates the frequencies of alternative male phenotypes in the population over time. Expression of the jack life history could not be explained by environmental factors expected to influence juvenile body condition and maturation probability. Instead, we found a strong positive association between the proportion of individuals maturing as jacks within a cohort and the prevalence of jacks among the males that sired that cohort. Moreover, due to differences in age-at-maturity between male phenotypes, and large interannual variability in recruitment strength, jacks from strong year-classes often spawn among older males from the weaker recruitments of earlier cohorts. Through such "cohort mismatches," which are amplified by size-selective harvest on older males, jacks frequently achieve substantial representation in the breeding population, and likely high total fertilizations. The repeated occurrence of these cohort mismatches appears to disrupt the stabilizing influence of frequency-dependent selection, allowing the prevalence of jacks to exceed what might be expected under equilibrium conditions. These results emphasize that the dynamics of alternative life histories can profoundly influence fishery performance and should be explicitly considered in the management of exploited populations.

Temperature-dependent body size effects determine population responses to climate warming.

Current understanding of animal population responses to rising temperatures is based on the assumption that biological rates such as metabolism, which governs fundamental ecological processes, scale independently with body size and temperature, despite empirical evidence for interactive effects. Here, we investigate the consequences of interactive temperature- and size scaling of vital rates for the dynamics of populations experiencing warming using a stage-structured consumer-resource model. We show that interactive scaling alters population and stage-specific responses to rising temperatures, such that warming can induce shifts in population regulation and stage-structure, influence community structure and govern population responses to mortality. Analysing experimental data for 20 fish species, we found size-temperature interactions in intraspecific scaling of metabolic rate to be common. Given the evidence for size-temperature interactions and the ubiquity of size structure in animal populations, we argue that accounting for size-specific temperature effects is pivotal for understanding how warming affects animal populations and communities.

Cascading effects of mass mortality events in Arctic marine communities.

Mass mortality events caused by pulse anthropogenic or environmental perturbations (e.g., extreme weather, toxic spills or epizootics) severely reduce the abundance of a population in a short time. The frequency and impact of these events are likely to increase across the globe. Studies on how such events may affect ecological communities of interacting species are scarce. By combining a multispecies Gompertz model with a Bayesian state-space framework, we quantify community-level effects of a mass mortality event in a single species. We present a case study on a community of fish and zooplankton in the Barents Sea to illustrate how a mass mortality event of different intensities affecting the lower trophic level (krill) may propagate to higher trophic levels (capelin and cod). This approach is especially valuable for assessing community-level effects of potential anthropogenic-driven mass mortality events, owing to the ability to account for uncertainty in the assessed impact due to uncertainty about the ecological dynamics. We hence quantify how the assessed impact of a mass mortality event depends on the degree of precaution considered. We suggest that this approach can be useful for assessing the possible detrimental outcomes of toxic spills, for example oil spills, in relatively simple communities such as often found in the Arctic, a region under increasing influence of human activities due to increased land and sea use.

Pathogens trigger top-down climate forcing on ecosystem dynamics.

Evaluating the effects of climate variation on ecosystems is of paramount importance for our ability to forecast and mitigate the consequences of global change. However, the ways in which complex food webs respond to climate variations remain poorly understood. Here, we use long-term time series to investigate the effects of temperature variation on the intraguild-predation (IGP) system of Windermere (UK), a lake where pike (Esox lucius, top predator) feed on small-sized perch (Perca fluviatilis) but compete with large-sized perch for the same food sources. Spectral analyses of time series reveal that pike recruitment dynamics are temperature controlled. In 1976, expansion of a size-truncating perch pathogen into the lake severely impacted large perch and favoured pike as the IGP-dominant species. This pathogen-induced regime shift to a pike-dominated IGP apparently triggered a temperature-controlled trophic cascade passing through pike down to dissolved nutrients. In simple food chains, warming is predicted to strengthen top-down control by accelerating metabolic rates in ectothermic consumers, while pathogens of top consumers are predicted to dampen this top-down control. In contrast, the local IGP structure in Windermere made warming and pathogens synergistic in their top-down effects on ecosystem functioning. More generally, our results point to top predators as major mediators of community response to global change, and show that size-selective agents (e.g. pathogens, fishers or hunters) may change the topological architecture of food webs and alter whole ecosystem sensitivity to climate variation.

Population resilience to catastrophic mortality events during early life stages.

Catastrophic mortality events that drastically reduce the abundance of a population or a particular life stage can have long-term ecological and economic effects, and are of great concern in species conservation and management. Severe die-offs may be caused by natural catastrophes such as disease outbreaks and extreme climates, or human-caused disturbances such as toxic spills. Forecasting potential impacts of such disturbances is difficult and highly uncertain due to unknown future conditions, including population status and environmental conditions at the time of impact. Here, we present a framework for quantifying the range of potential, population-level effects of catastrophic events based on a hindcasting approach. A dynamic population model with Bayesian parameter estimation is used to simulate the impact of severe (50-99%) mortality events during the early life stages of Northeast Arctic cod (Gadus morhua), an abundant marine fish population of high economic value. We quantify the impact of such die-offs in terms of subsequent changes in population biomass and harvest through direct comparison of simulated and historical trends, and estimate the duration of the impact as a measure of population resilience. Our results demonstrate strong resilience to catastrophic events that affect early life stages owing to density dependence in survival and a broad population age structure. Yet, while population recovery is. relatively fast, losses in harvest and economic value can be substantial. Future research efforts should focus on long-term and indirect effects via food web interactions in order to better understand the ecological and economic ramifications of catastrophic mortality events.

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.

When phenology matters: age-size truncation alters population response to trophic mismatch.

Climate-induced shifts in the timing of life-history events are a worldwide phenomenon, and these shifts can de-synchronize species interactions such as predator-prey relationships. In order to understand the ecological implications of altered seasonality, we need to consider how shifts in phenology interact with other agents of environmental change such as exploitation and disease spread, which commonly act to erode the demographic structure of wild populations. Using long-term observational data on the phenology and dynamics of a model predator-prey system (fish and zooplankton in Windermere, UK), we show that age-size truncation of the predator population alters the consequences of phenological mismatch for offspring survival and population abundance. Specifically, age-size truncation reduces intraspecific density regulation due to competition and cannibalism, and thereby amplifies the population sensitivity to climate-induced predator-prey asynchrony, which increases variability in predator abundance. High population variability poses major ecological and economic challenges as it can diminish sustainable harvest rates and increase the risk of population collapse. Our results stress the importance of maintaining within-population age-size diversity in order to buffer populations against phenological asynchrony, and highlight the need to consider interactive effects of environmental impacts if we are to understand and project complex ecological outcomes.

Stochasticity and determinism: how density-independent and density-dependent processes affect population variability.

A persistent debate in population ecology concerns the relative importance of environmental stochasticity and density dependence in determining variability in adult year-class strength, which contributes to future reproduction as well as potential yield in exploited populations. Apart from the strength of the processes, the timing of density regulation may affect how stochastic variation, for instance through climate, translates into changes in adult abundance. In this study, we develop a life-cycle model for the population dynamics of a large marine fish population, Northeast Arctic cod, to disentangle the effects of density-independent and density-dependent processes on early life-stages, and to quantify the strength of compensatory density dependence in the population. The model incorporates information from scientific surveys and commercial harvest, and dynamically links multiple effects of intrinsic and extrinsic factors on all life-stages, from eggs to spawners. Using a state-space approach we account for observation error and stochasticity in the population dynamics. Our findings highlight the importance of density-dependent survival in juveniles, indicating that this period of the life cycle largely determines the compensatory capacity of the population. Density regulation at the juvenile life-stage dampens the impact of stochastic processes operating earlier in life such as environmental impacts on the production of eggs and climate-dependent survival of larvae. The timing of stochastic versus regulatory processes thus plays a crucial role in determining variability in adult abundance. Quantifying the contribution of environmental stochasticity and compensatory mechanisms in determining population abundance is essential for assessing population responses to climate change and exploitation by humans.

Effects of climate change on trait-based dynamics of a top predator in freshwater ecosystems.

Predicted universal responses of ectotherms to climate warming include increased maximum population growth rate and changes in body size through the temperature-size rule. However, the mechanisms that would underlie these predicted responses are not clear. Many studies have focused on proximate mechanisms of physiological processes affecting individual growth. One can also consider ultimate mechanisms involving adaptive explanations by evaluating temperature effects on different vital rates across the life history and using the information in a population dynamical model. Here, we combine long-term data for a top predator in freshwater ecosystems (pike; Esox lucius) with a stochastic integral projection model to analyze concurrent effects of temperature on vital rates, body size, and population dynamics. As predicted, the net effect of warming on population growth rate (fitness) is positive, but the thermal sensitivity of this rate is highly size- and vital rate-dependent. These results are not sensitive to increasing variability in temperature. Somatic growth follows the temperature-size rule, and our results support an adaptive explanation for this response. The stable length structure of the population shifts with warming toward an increased proportion of medium-sized but a reduced proportion of small and large individuals. This study highlights how demographic approaches can help reveal complex underlying mechanisms for population responses to warming.

Adaptive phenotypic diversification along a temperature-depth gradient.

Theoretical models suggest that sympatric speciation along environmental gradients might be common in nature. Here we present the first data-based model of evolutionary diversification along a continuous environmental gradient. On the basis of genetic analyses, it has been suggested that a pair of coregonid fishes (Coregonus spp.) in a postglacial German lake originated by sympatric speciation. Within this lake, the two species segregate vertically and show metabolic adaptations to, as well as behavioral preferences for, correspondingly different temperatures. We test the plausibility of the hypothesis that this diversifying process has been driven by adaptations to different thermal microhabitats along the lake's temperature-depth gradient. Using an adaptive-dynamics model that is calibrated with empirical data and allows the gradual evolution of a quantitative trait describing optimal foraging temperature, we show that under the specific environmental conditions in the lake, evolutionary branching of a hypothetical ancestral population into two distinct phenotypes may have occurred. We also show that the resultant evolutionary diversification yields two stably coexisting populations with trait values and depth distributions that are in agreement with those currently observed in the lake. We conclude that divergent thermal adaptations along the temperature-depth gradient might have brought about the two species observed today.

Community-level consequences of cannibalism.

Ecological interactions determine the structure and dynamics of communities and their responses to the environment. Understanding the community-level effects of ecological interactions, such as intra- and interspecifc competition, predation, and cannibalism, is therefore central to ecological theory and ecosystem management. Here, we investigate the community-level consequences of cannibalism in populations with density-dependent maturation and reproduction. We model a stage-structured consumer population with an ontogenetic diet shift to analyze how cannibalism alters the conditions for the invasion and persistence of stage-specific predators and competitors. Our results demonstrate that cannibalistic interactions can facilitate coexistence with other species at both trophic levels. This effect of cannibalism critically depends on the food dependence of the demographic processes. The underlying mechanism is a cannibalism-induced shift in the biomass distribution between the consumer life stages. These findings suggest that cannibalism may alter the structure of ecological communities through its effects on species coexistence.

Does increasing mortality change the response of fish populations to environmental fluctuations?

Fluctuations of fish populations abundances are shaped by the interplay between population dynamics and the stochastic forcing of the environment. Age-structured populations behave as a filter of the environment. This filter is characterised by the species-specific life cycle and life-history traits. An increased mortality of mature individuals alters these characteristics and may therefore induce changes in the variability of populations. The response of a generic age-structured model was analysed to investigate the expected changes in the fluctuations of fish populations in response to decreased adult survival. These expectations were then tested on an extensive dataset. In accordance with theory, the analyses revealed that decreased adult survival and mean age of spawners were linked to an increase in the relative importance of short-term fluctuations. It suggests that intensive exploitation can lead to a change in the variability of fish populations, an issue of central interest from both conservation and management perspectives.

Temperature-driven regime shifts in the dynamics of size-structured populations.

Global warming impacts virtually all biota and ecosystems. Many of these impacts are mediated through direct effects of temperature on individual vital rates. Yet how this translates from the individual to the population level is still poorly understood, hampering the assessment of global warming impacts on population structure and dynamics. Here, we study the effects of temperature on intraspecific competition and cannibalism and the population dynamical consequences in a size-structured fish population. We use a physiologically structured consumer-resource model in which we explicitly model the temperature dependencies of the consumer vital rates and the resource population growth rate. Our model predicts that increased temperature decreases resource density despite higher resource growth rates, reflecting stronger intraspecific competition among consumers. At a critical temperature, the consumer population dynamics destabilize and shift from a stable equilibrium to competition-driven generation cycles that are dominated by recruits. As a consequence, maximum age decreases and the proportion of younger and smaller-sized fish increases. These model predictions support the hypothesis of decreasing mean body sizes due to increased temperatures. We conclude that in size-structured fish populations, global warming may increase competition, favor smaller size classes, and induce regime shifts that destabilize population and community dynamics.