Social and genetic connectivity despite ecological variation in a killer whale network.

Philopatric kin-based societies encourage a narrow breadth of conservative behaviours owing to individuals primarily learning from close kin, promoting behavioural homogeneity. However, weaker social ties beyond kin, and across a behaviourally diverse social landscape, could be sufficient to induce variation and a greater ecological niche breadth. We investigated a network of 457 photo-identified killer whales from Norway (548 encounters in 2008-2021) with diet data available (46 mixed-diet individuals feeding on both fish and mammals, and 411 exclusive fish-eaters) to quantify patterns of association within and between diet groups, and to identify underlying correlates. We genotyped a subset of 106 whales to assess patterns of genetic differentiation. Our results suggested kinship as main driver of social bonds within and among cohesive social units, while diet was most likely a consequence reflective of cultural diffusion, rather than a driver. Flexible associations within and between ecologically diverse social units led to a highly connected network, reducing social and genetic differentiation between diet groups. Our study points to a role of social connectivity, in combination with individual behavioural variation, in influencing population ecology in killer whales.

Persistence of fish populations to longer, more intense, and more frequent mass mortality events.

Over the last decades, mass mortality events have become increasingly common across taxa with sometimes devastating effects on population biomass. In the aquatic environment, fish are sensitive to mass mortality events, particularly at the early life stages that are crucial for population dynamics. However, it has recently been shown for fish, that a single mass mortality event in early life typically does not lead to population collapse. Moreover, the frequency and intensity of extreme events that can cause mass mortality, such as marine heatwaves, are increasing. Here, we show that increasing frequency and intensity of mass mortality events may lead to population collapse. Since the drivers of mass mortality events are diverse, and often linked to climate change, it is challenging to predict the frequency and severity of future mass mortality events. As an alternative, we quantify the probability of population collapse depending on the frequency and intensity as well as the duration of mass mortality events. Based on 39 fish species, we show that the probability of collapse typically increases with increasing frequency, intensity, and duration of the mortality events. In addition, we show that the collapse depends on key traits such as natural mortality, recruitment variation, and density dependence. The presented framework provides quantitative estimates of the sensitivity of fish species to these increasingly common extreme events, which paves the way for potential mitigation actions to alleviate adverse impacts on harvested fish populations across the globe.

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.

Empirical evidence of nonlinearity in bottom up effect in a marine predator-prey system.

The strength of species interactions may have profound effects on population dynamics. Empirical estimates of interaction strength are often based on the assumption that the interaction strengths are constant. Barents Sea (BS) cod and capelin are two fish populations for which such an interaction has been acknowledged and used, under the assumption of constant interaction strength, when studying their population dynamics. However, species interactions can often be nonlinear in marine ecosystems and might profoundly change our understanding of food chains. Analysing long-term time series data comprising a survey over 37 years in the Arcto-boreal BS, using a state-space modelling framework, we demonstrate that the effect of capelin on cod is not linear but shifts depending on capelin abundance: while capelin is beneficial for cod populations at high abundance; below the threshold, it becomes less important for cod. Our analysis therefore shows the importance of investigating nonlinearity in species interactions and may contribute to an improved understanding on species assemblages.

Nonlinearity in interspecific interactions in response to climate change: Cod and haddock as an example.

Climate change has profound ecological effects, yet our understanding of how trophic interactions among species are affected by climate change is still patchy. The sympatric Atlantic haddock and cod are co-occurring across the North Atlantic. They compete for food at younger stages and thereafter the former is preyed by the latter. Climate change might affect the interaction and coexistence of these two species. Particularly, the increase in sea temperature (ST) has been shown to affect distribution, population growth and trophic interactions in marine systems. We used 33-year long time series of haddock and cod abundances estimates from two data sources (acoustic and trawl survey) to analyse the dynamic effect of climate on the coexistence of these two sympatric species in the Arcto-Boreal Barents Sea. Using a Bayesian state-space threshold model, we demonstrated that long-term climate variation, as expressed by changes of ST, affected species demography through different influences on density-independent processes. The interaction between cod and haddock has shifted in the last two decades due to an increase in ST, altering the equilibrium abundances and the dynamics of the system. During warm years (ST over ca. 4°C), the increase in the cod abundance negatively affected haddock abundance while it did not during cold years. This change in interactions therefore changed the equilibrium population size with a higher population size during warm years. Our analyses show that long-term climate change in the Arcto-Boreal system can generate differences in the equilibrium conditions of species assemblages.

Size- and stage-dependence in cause-specific mortality of migratory brown trout.

Evidence-based management of natural populations under strong human influence frequently requires not only estimates of survival but also knowledge about how much mortality is due to anthropogenic vs. natural causes. This is the case particularly when individuals vary in their vulnerability to different causes of mortality due to traits, life history stages, or locations. Here, we estimated harvest and background (other cause) mortality of landlocked migratory salmonids over half a century. In doing so, we quantified among-individual variation in vulnerability to cause-specific mortality resulting from differences in body size and spawning location relative to a hydropower dam. We constructed a multistate mark-recapture model to estimate harvest and background mortality hazard rates as functions of a discrete state (spawning location) and an individual time-varying covariate (body size). We further accounted for among-year variation in mortality and migratory behaviour and fit the model to a unique 50-year time series of mark-recapture-recovery data on brown trout (Salmo trutta) in Norway. Harvest mortality was highest for intermediate-sized trout, and outweighed background mortality for most of the observed size range. Background mortality decreased with body size for trout spawning above the dam and increased for those spawning below. All vital rates varied substantially over time, but a trend was evident only in estimates of fishers' reporting rate, which decreased from over 50% to less than 10% throughout the study period. We highlight the importance of body size for cause-specific mortality and demonstrate how this can be estimated using a novel hazard rate parameterization for mark-recapture models. Our approach allows estimating effects of individual traits and environment on cause-specific mortality without confounding, and provides an intuitive way to estimate temporal patterns within and correlation among different mortality sources.

Effect of a fish stock's demographic structure on offspring survival and sensitivity to climate.

Commercial fishing generally removes large and old individuals from fish stocks, reducing mean age and age diversity among spawners. It is feared that these demographic changes lead to lower and more variable recruitment to the stocks. A key proposed pathway is that juvenation and reduced size distribution causes reduced ranges in spawning period, spawning location, and egg buoyancy; this is proposed to lead to reduced spatial distribution of fish eggs and larvae, more homogeneous ambient environmental conditions within each year-class, and reduced buffering against negative environmental influences. However, few, if any, studies have confirmed a causal link from spawning stock demographic structure through egg and larval distribution to year class strength at recruitment. We here show that high mean age and size in the spawning stock of Barents Sea cod (Gadus morhua) is positively associated with high abundance and wide spatiotemporal distribution of cod eggs. We find, however, no support for the hypothesis that a wide egg distribution leads to higher recruitment or a weaker recruitment-temperature correlation. These results are based on statistical analyses of a spatially resolved data set on cod eggs covering a period (1959-1993) with large changes in biomass and demographic structure of spawners. The analyses also account for significant effects of spawning stock biomass and a liver condition index on egg abundance and distribution. Our results suggest that the buffering effect of a geographically wide distribution of eggs and larvae on fish recruitment may be insignificant compared with other impacts.

Ticket to spawn: Combining economic and genetic data to evaluate the effect of climate and demographic structure on spawning distribution in Atlantic cod.

Climate warming and harvesting affect the dynamics of species across the globe through a multitude of mechanisms, including distribution changes. In fish, migrations to and distribution on spawning grounds are likely influenced by both climate warming and harvesting. The Northeast Arctic (NEA) cod (Gadus morhua) performs seasonal migrations from its feeding grounds in the Barents Sea to spawning grounds along the Norwegian coast. The distribution of cod between the spawning grounds has historically changed at decadal scales, mainly due to variable use of the northern and southern margins of the spawning area. Based on historical landing records, two major hypotheses have been put forward to explain these changes: climate and harvesting. Climate could affect the distribution through, for example, spatial habitat shifts. Harvesting could affect the distribution through impacting the demographic structure. If demographic structure is important, theory predicts increasing spawner size with migration distance. Here, we evaluate these hypotheses with modern data from a period (2000-2016) of increasing temperature and recovering stock structure. We first analyze economic data from the Norwegian fisheries to investigate geographical differences in size of spawning fish among spawning grounds, as well as interannual differences in mean latitude of spawning in relation to changes in temperature and demographic parameters. Second, we analyze genetically determined fish sampled at the spawning grounds to unambiguously separate between migratory NEA cod and potentially smaller sized coastal cod of local origin. Our results indicate smaller spawners farther away from the feeding grounds, hence not supporting the hypothesis that harvesting is a main driver for the contemporary spawning ground distribution. We find a positive correlation between annual mean spawning latitude and temperature. In conclusion, based on contemporary data, there is more support for climate compared to harvesting in shaping spawning ground distribution in this major fish stock in the North Atlantic Ocean.

Disentangling the mechanisms behind climate effects on zooplankton.

Understanding how climate influences ecosystems is complicated by the many correlated and interrelated impacting factors. Here we quantify climate effects on Calanus finmarchicus in the northeastern Norwegian Sea and southwestern Barents Sea. By combining oceanographic drift models and statistical analyses of field data from 1959 to 1993 and investigating effects across trophic levels, we are able to elucidate pathways by which climate influences zooplankton. The results show that both chlorophyll biomass in spring and C. finmarchicus biomass in summer relate positively to a combination of shallow mixed layer depth and increased wind in spring, suggesting that C. finmarchicus biomass in summer is influenced by bottom-up effects of food availability. Furthermore, spatially resolved C. finmarchicus biomass in summer is linked to favorable transport from warmer, core areas to the south. However, increased mean temperature in spring does not lead to increased C. finmarchicus biomass in summer. Rather, spring biomass is generally higher, but population growth from spring to summer is lower, after a warm compared with a cold spring. Our study illustrates how improved understanding of climate effects can be obtained when different datasets and different methods are combined in a unified approach.

Predator-prey interactions cause apparent competition between marine zooplankton groups.

Predator-mediated apparent competition is an indirect negative interaction between two prey species mediated by a shared predator. Quantifying such indirect ecosystem effects is methodologically challenging but important for understanding ecosystem functioning. Still, there are few examples of apparent competition from pelagic marine environments. Using state-space statistical modeling, we here provide evidence for apparent competition between two dominant zooplankton groups in a large marine ecosystem, i.e., krill and copepods in the Barents Sea. This effect is mediated by a positive association between krill biomass and survival of the main planktivorous fish in the Barents Sea, capelin Mallotus villosus, and a negative association between capelin and copepod biomasses. The biomass of Atlantic krill species is expected to increase in the Barents Sea due to ongoing climate change, thereby potentially negatively affecting copepods through apparent competition. By demonstrating and quantifying apparent competition in a large marine ecosystem, our study paves the way for more realistic projections of indirect ecosystem effects of climate change and harvesting.

Individual heterogeneity and early life conditions shape growth in a freshwater top predator.

Body size can have profound impacts on survival, movement, and reproductive schedules shaping individual fitness, making growth a central process in ecological and evolutionary dynamics. Realized growth is the result of a complex interplay between life history schedules, individual variation, and environmental influences. Integrating all of these aspects into growth models is methodologically difficult, depends on the availability of repeated measurements of identifiable individuals, and consequently represents a major challenge in particular for natural populations. Using a unique 30-yr time series of individual length measurements inferred from scale year rings of wild brown trout, we develop a Bayesian hierarchical model to estimate individual growth trajectories in temporally and spatially varying environments. We reveal a gradual decrease in average juvenile growth, which has carried over to adult life and contributed to decreasing sizes observed at the population level. Commonly studied environmental drivers like temperature and water flow did not explain much of this trend and overall persistent and among-year individual variation dwarfed temporal variation in growth patterns. Our model and results are relevant to a wide range of questions in ecology and evolution requiring a detailed understanding of growth patterns, including conservation and management of many size-structured populations.

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.

Fitness consequences of early life conditions and maternal size effects in a freshwater top predator.

Conditions experienced in early life stages can be an important determinant of individual life histories. In fish, environmental conditions are known to affect early survival and growth, but recent studies have also emphasized maternal effects mediated by size or age. However, the relative sensitivity of the mean fitness (population growth rate λ) to different early life impacts remains largely unexplored. Using a female-based integral projection model (IPM) parameterized from unique long-term demographic data for pike (Esox lucius), we evaluated the relative fitness consequences of different early life impacts, including (i) maternal effects of length on egg weight, potentially affecting offspring (first year) survival, and (ii) effects of temperature on offspring growth and survival. Of the seven vital rates defining the model, offspring survival could not be directly estimated and four scenarios were defined for this rate. Elasticity analyses of the IPM were performed to calculate (i) the total contribution from different lengths to the elasticity of λ to the projection kernel, and (ii) the elasticity of λ to underlying variables of female current length, female offspring length at age 1, and temperature. These elasticities were decomposed into contributions from different vital rates across length. Egg weight increased with female length, as expected, but the effect leveled off for the largest females. However, λ was largely insensitive to this effect, even when egg weight was assumed to have a strong effect on offspring survival. In contrast, λ was sensitive to early temperature conditions through growth and survival. Among mature females, the total elasticity of λ to the projection kernel generally increased with length. The results were robust to a wide range of assumptions. These results suggest that environmental conditions experienced in early life represent a more important driver of mean population growth and fitness of pike than maternal effects of size on offspring survival. We discuss two general mechanisms underlying the weak influence of this maternal effect, suggesting that these may be general for long-lived and highly fecund fishes. This model and results are relevant for the management of long-lived top predators, including many commercially important fish species.

Individual heterogeneity in life histories and eco-evolutionary dynamics.

Individual heterogeneity in life history shapes eco-evolutionary processes, and unobserved heterogeneity can affect demographic outputs characterising life history and population dynamical properties. Demographic frameworks like matrix models or integral projection models represent powerful approaches to disentangle mechanisms linking individual life histories and population-level processes. Recent developments have provided important steps towards their application to study eco-evolutionary dynamics, but so far individual heterogeneity has largely been ignored. Here, we present a general demographic framework that incorporates individual heterogeneity in a flexible way, by separating static and dynamic traits (discrete or continuous). First, we apply the framework to derive the consequences of ignoring heterogeneity for a range of widely used demographic outputs. A general conclusion is that besides the long-term growth rate lambda, all parameters can be affected. Second, we discuss how the framework can help advance current demographic models of eco-evolutionary dynamics, by incorporating individual heterogeneity. For both applications numerical examples are provided, including an empirical example for pike. For instance, we demonstrate that predicted demographic responses to climate warming can be reversed by increased heritability. We discuss how applications of this demographic framework incorporating individual heterogeneity can help answer key biological questions that require a detailed understanding of eco-evolutionary dynamics.

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.

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.

Large biomass reduction effect on the relative role of climate, fishing, and recruitment on fish population dynamics.

Many species around the world have collapsed, yet only some have recovered. A key question is what happens to populations post collapse. Traditionally, marine fish collapses are linked to overfishing, poor climate, and recruitment. We test whether the effect on biomass change from these drivers remains the same after a collapse. We used a regression model to analyse the effect of harvesting, recruitment, and climate variability on biomass change before and after a collapse across 54 marine fish populations around the world. The most salient result was the change in fishing effect that became weaker after a collapse. The change in sea temperature and recruitment effects were more variable across systems. The strongest changes were in the pelagic habitats. The resultant change in the sensitivity to external drivers indicates that whilst biomass may be rebuilt, the responses to variables known to affect stocks may have changed after a collapse. Our results show that a general model applied to many stocks provides useful insights, but that not all stocks respond similarly to a collapse calling for stock-specific models. Stocks respond to environmental drivers differently after a collapse, so caution is needed when using pre-collapse knowledge to advise on population dynamics and management.

Predatory walls may impair climate warming-associated population expansion.

Climate change has a profound impact on species distribution and abundance globally, as well as local diversity, which affects ecosystem functioning. In particular, changes in population distribution and abundance may lead to changes in trophic interactions. Although species can often shift their spatial distribution when suitable habitats are available, it has been suggested that predator presence can be a constraint on climate-related distribution shifts. We test this using two well-studied and data-rich marine environments. Focusing on a pair of sympatric fishes, Atlantic haddock Melanogrammus aeglefinus and cod Gadus morhua, we study the effect of the presence and abundance of the latter on the former distribution. We found that the distribution of cod and increased abundance may limit the expansion of haddock to new areas and could consequently buffer ecosystem changes due to climate change. Though marine species may track the rate and direction of climate shifts, our results demonstrate that the presence of predators may limit their expansion to thermally suitable habitats. By integrating climatic and ecological data at scales that can resolve predator-prey relationships, this analysis demonstrates the usefulness of considering trophic interactions to gain a more comprehensive understanding and to mitigate the effects of climate change on species distributions.

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.

Pathogen-induced rapid evolution in a vertebrate life-history trait.

Anthropogenic factors, including climate warming, are increasing the incidence and prevalence of infectious diseases worldwide. Infectious diseases caused by pathogenic parasites can have severe impacts on host survival, thereby altering the selection regime and inducing evolutionary responses in their hosts. Knowledge about such evolutionary consequences in natural populations is critical to mitigate potential ecological and economic effects. However, studies on pathogen-induced trait changes are scarce and the pace of evolutionary change is largely unknown, particularly in vertebrates. Here, we use a time series from long-term monitoring of perch to estimate temporal trends in the maturation schedule before and after a severe pathogen outbreak. We show that the disease induced a phenotypic change from a previously increasing to a decreasing size at maturation, the most important life-history transition in animals. Evolutionary rates imposed by the pathogen were high and comparable to those reported for populations exposed to intense human harvesting. Pathogens thus represent highly potent drivers of adaptive phenotypic evolution in vertebrates.