Whole-genome sequencing illuminates multifaceted targets of selection to humic substances in Eurasian perch.

Extreme environments are inhospitable to the majority of species, but some organisms are able to survive in such hostile conditions due to evolutionary adaptations. For example, modern bony fishes have colonized various aquatic environments, including perpetually dark, hypoxic, hypersaline and toxic habitats. Eurasian perch (Perca fluviatilis) is among the few fish species of northern latitudes that is able to live in very acidic humic lakes. Such lakes represent almost "nocturnal" environments; they contain high levels of dissolved organic matter, which in addition to creating a challenging visual environment, also affects a large number of other habitat parameters and biotic interactions. To reveal the genomic targets of humic-associated selection, we performed whole-genome sequencing of perch originating from 16 humic and 16 clear-water lakes in northern Europe. We identified over 800,000 single nucleotide polymorphisms, of which >10,000 were identified as potential candidates under selection (associated with >3000 genes) using multiple outlier approaches. Our findings suggest that adaptation to the humic environment may involve hundreds of regions scattered across the genome. Putative signals of adaptation were detected in genes and gene families with diverse functions, including organism development and ion transportation. The observed excess of variants under selection in regulatory regions highlights the importance of adaptive evolution via regulatory elements, rather than via protein sequence modification. Our study demonstrates the power of whole-genome analysis to illuminate the multifaceted nature of humic adaptation and provides the foundation for further investigation of causal mutations underlying phenotypic traits of ecological and evolutionary importance.

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.

Temperature impacts on fish physiology and resource abundance lead to faster growth but smaller fish sizes and yields under warming.

Resolving the combined effect of climate warming and exploitation in a food web context is key for predicting future biomass production, size-structure and potential yields of marine fishes. Previous studies based on mechanistic size-based food web models have found that bottom-up processes are important drivers of size-structure and fisheries yield in changing climates. However, we know less about the joint effects of 'bottom-up' and physiological effects of temperature; how do temperature effects propagate from individual-level physiology through food webs and alter the size-structure of exploited species in a community? Here, we assess how a species-resolved size-based food web is affected by warming through both these pathways and by exploitation. We parameterize a dynamic size spectrum food web model inspired by the offshore Baltic Sea food web, and investigate how individual growth rates, size-structure, and relative abundances of species and yields are affected by warming. The magnitude of warming is based on projections by the regional coupled model system RCA4-NEMO and the RCP 8.5 emission scenario, and we evaluate different scenarios of temperature dependence on fish physiology and resource productivity. When accounting for temperature-effects on physiology in addition to on basal productivity, projected size-at-age in 2050 increases on average for all fish species, mainly for young fish, compared to scenarios without warming. In contrast, size-at-age decreases when temperature affects resource dynamics only, and the decline is largest for young fish. Faster growth rates due to warming, however, do not always translate to larger yields, as lower resource carrying capacities with increasing temperature tend to result in decline in the abundance of larger fish and hence spawning stock biomass. These results suggest that to understand how global warming affects the size structure of fish communities, both direct metabolic effects and indirect effects of temperature via basal resources must be accounted for.

Effects of Warming on Intraguild Predator Communities with Ontogenetic Diet Shifts.

AbstractSpecies interactions mediate how warming affects community composition via individual growth and population size structure. While predictions on how warming affects composition of size- or stage-structured communities have so far focused on linear (food chain) communities, mixed competition-predation interactions, such as intraguild predation, are common. Intraguild predation often results from changes in diet over ontogeny ("ontogenetic diet shifts") and strongly affects community composition and dynamics. Here, we study how warming affects a community of intraguild predators with ontogenetic diet shifts, consumers, and shared prey by analyzing a stage-structured bioenergetics multispecies model with temperature- and body size-dependent individual-level rates. We find that warming can strengthen competition and decrease predation, leading to a loss of a cultivation mechanism (the feedback between predation on and competition with consumers exerted by predators) and ultimately predator collapse. Furthermore, we show that the effect of warming on community composition depends on the extent of the ontogenetic diet shift and that warming can cause a sequence of community reconfigurations in species with partial diet shifts. Our findings contrast previous predictions concerning individual growth of predators and the mechanisms behind predator loss in warmer environments and highlight how feedbacks between temperature and intraspecific size structure are important for understanding such effects on community composition.

Cardiorespiratory adjustments to chronic environmental warming improve hypoxia tolerance in European perch (Perca fluviatilis).

Aquatic hypoxia will become increasingly prevalent in the future as a result of eutrophication combined with climate warming. While short-term warming typically constrains fish hypoxia tolerance, many fishes cope with warming by adjusting physiological traits through thermal acclimation. Yet, little is known about how such adjustments affect tolerance to hypoxia. We examined European perch (Perca fluviatilis) from the Biotest enclosure (23°C, Biotest population), a unique ∼1 km2 ecosystem artificially warmed by cooling water from a nuclear power plant, and an adjacent reference site (16-18°C, reference population). Specifically, we evaluated how acute and chronic warming affect routine oxygen consumption rate (MO2,routine) and cardiovascular performance in acute hypoxia, alongside assessment of the thermal acclimation of the aerobic contribution to hypoxia tolerance (critical O2 tension for MO2,routine: Pcrit) and absolute hypoxia tolerance (O2 tension at loss of equilibrium; PLOE). Chronic adjustments (possibly across lifetime or generations) alleviated energetic costs of warming in Biotest perch by depressing MO2,routine and cardiac output, and by increasing blood O2 carrying capacity relative to reference perch acutely warmed to 23°C. These adjustments were associated with improved maintenance of cardiovascular function and MO2,routine in hypoxia (i.e. reduced Pcrit). However, while Pcrit was only partially thermally compensated in Biotest perch, they had superior absolute hypoxia tolerance (i.e. lowest PLOE) relative to reference perch irrespective of temperature. We show that European perch can thermally adjust physiological traits to safeguard and even improve hypoxia tolerance during chronic environmental warming. This points to cautious optimism that eurythermal fish species may be resilient to the imposition of impaired hypoxia tolerance with climate warming.

Population and size-specific distribution of Atlantic salmon Salmo salar in the Baltic Sea over five decades.

Population-specific assessment and management of anadromous fish at sea requires detailed information about the distribution at sea over ontogeny for each population. However, despite a long history of mixed-stock sea fisheries on Atlantic salmon, Salmo salar, migration studies showing that some salmon populations feed in different regions of the Baltic Sea and variation in dynamics occurs among populations feeding in the Baltic Sea, such information is often lacking. Also, current assessment of Baltic salmon assumes equal distribution at sea and therefore equal responses to changes in off-shore sea fisheries. Here, we test for differences in distribution at sea among and within ten Atlantic salmon Salmo salar populations originating from ten river-specific hatcheries along the Swedish Baltic Sea coast, using individual data from >125,000 tagged salmon, recaptured over five decades. We show strong population and size-specific differences in distribution at sea, varying between year classes and between individuals within year classes. This suggests that Atlantic salmon in the Baltic Sea experience great variation in environmental conditions and exploitation rates over ontogeny depending on origin and that current assessment assumptions about equal exploitation rates in the offshore fisheries and a shared environment at sea are not valid. Thus, our results provide additional arguments and necessary information for implementing population-specific management of salmon, also when targeting life stages at sea.

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.

Experimental evidence of gradual size-dependent shifts in body size and growth of fish in response to warming.

A challenge facing ecologists trying to predict responses to climate change is the few recent analogous conditions to use for comparison. For example, negative relationships between ectotherm body size and temperature are common both across natural thermal gradients and in small-scale experiments. However, it is unknown if short-term body size responses are representative of long-term responses. Moreover, to understand population responses to warming, we must recognize that individual responses to temperature may vary over ontogeny. To enable predictions of how climate warming may affect natural populations, we therefore ask how body size and growth may shift in response to increased temperature over life history, and whether short- and long-term growth responses differ. We addressed these questions using a unique setup with multidecadal artificial heating of an enclosed coastal bay in the Baltic Sea and an adjacent reference area (both with unexploited populations), using before-after control-impact paired time-series analyses. We assembled individual growth trajectories of ~13,000 unique individuals of Eurasian perch and found that body growth increased substantially after warming, but the extent depended on body size: Only among small-bodied perch did growth increase with temperature. Moreover, the strength of this response gradually increased over the 24 year warming period. Our study offers a unique example of how warming can affect fish populations over multiple generations, resulting in gradual changes in body growth, varying as organisms develop. Although increased juvenile growth rates are in line with predictions of the temperature-size rule, the fact that a larger body size at age was maintained over life history contrasts to that same rule. Because the artificially heated area is a contemporary system mimicking a warmer sea, our findings can aid predictions of fish responses to further warming, taking into account that growth responses may vary both over an individual's life history and over time.

Warmer and browner waters decrease fish biomass production.

Climate change studies have long focused on effects of increasing temperatures, often without considering other simultaneously occurring environmental changes, such as browning of waters. Resolving how the combination of warming and browning of aquatic ecosystems affects fish biomass production is essential for future ecosystem functioning, fisheries, and food security. In this study, we analyzed individual- and population-level fish data from 52 temperate and boreal lakes in Northern Europe, covering large gradients in water temperature and color (absorbance, 420 nm). We show that fish (Eurasian perch, Perca fluviatilis) biomass production decreased with both high water temperatures and brown water color, being lowest in warm and brown lakes. However, while both high temperature and brown water decreased fish biomass production, the mechanisms behind the decrease differed: temperature affected the fish biomass production mainly through a decrease in population standing stock biomass, and through shifts in size- and age-distributions toward a higher proportion of young and small individuals in warm lakes; brown water color, on the other hand, mainly influenced fish biomass production through negative effects on individual body growth and length-at-age. In addition to these findings, we observed that the effects of temperature and brown water color on individual-level processes varied over ontogeny. Body growth only responded positively to higher temperatures among young perch, and brown water color had a stronger negative effect on body growth of old than on young individuals. Thus, to better understand and predict future fish biomass production, it is necessary to integrate both individual- and population-level responses and to acknowledge within-species variation. Our results suggest that global climate change, leading to browner and warmer waters, may negatively affect fish biomass production, and this effect may be stronger than caused by increased temperature or water color alone.

Four decades of functional community change reveals gradual trends and low interlinkage across trophic groups in a large marine ecosystem.

The rate at which biological diversity is altered on both land and in the sea, makes temporal community development a critical and fundamental part of understanding global change. With advancements in trait-based approaches, the focus on the impact of temporal change has shifted towards its potential effects on the functioning of the ecosystems. Our mechanistic understanding of and ability to predict community change is still impeded by the lack of knowledge in long-term functional dynamics that span several trophic levels. To address this, we assessed species richness and multiple dimensions of functional diversity and dynamics of two interacting key organism groups in the marine food web: fish and zoobenthos. We utilized unique time series-data spanning four decades, from three environmentally distinct coastal areas in the Baltic Sea, and assembled trait information on six traits per organism group covering aspects of feeding, living habit, reproduction and life history. We identified gradual long-term trends, rather than abrupt changes in functional diversity (trait richness, evenness, dispersion) trait turnover, and overall multi-trait community composition. The linkage between fish and zoobenthic functional community change, in terms of correlation in long-term trends, was weak, with timing of changes being area and trophic group specific. Developments of fish and zoobenthos traits, particularly size (increase in small size for both groups) and feeding habits (e.g. increase in generalist feeding for fish and scavenging or predation for zoobenthos), suggest changes in trophic pathways. We summarize our findings by highlighting three key aspects for understanding functional change across trophic groups: (a) decoupling of species from trait richness, (b) decoupling of richness from density and (c) determining of turnover and multi-trait dynamics. We therefore argue for quantifying change in multiple functional measures to help assessments of biodiversity change move beyond taxonomy and single trophic groups.

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.

The importance of benthic-pelagic coupling for marine ecosystem functioning in a changing world.

Benthic-pelagic coupling is manifested as the exchange of energy, mass, or nutrients between benthic and pelagic habitats. It plays a prominent role in aquatic ecosystems, and it is crucial to functions from nutrient cycling to energy transfer in food webs. Coastal and estuarine ecosystem structure and function are strongly affected by anthropogenic pressures; however, there are large gaps in our understanding of the responses of inorganic nutrient and organic matter fluxes between benthic habitats and the water column. We illustrate the varied nature of physical and biological benthic-pelagic coupling processes and their potential sensitivity to three anthropogenic pressures - climate change, nutrient loading, and fishing - using the Baltic Sea as a case study and summarize current knowledge on the exchange of inorganic nutrients and organic material between habitats. Traditionally measured benthic-pelagic coupling processes (e.g., nutrient exchange and sedimentation of organic material) are to some extent quantifiable, but the magnitude and variability of biological processes are rarely assessed, preventing quantitative comparisons. Changing oxygen conditions will continue to have widespread effects on the processes that govern inorganic and organic matter exchange among habitats while climate change and nutrient load reductions may have large effects on organic matter sedimentation. Many biological processes (predation, bioturbation) are expected to be sensitive to anthropogenic drivers, but the outcomes for ecosystem function are largely unknown. We emphasize how improved empirical and experimental understanding of benthic-pelagic coupling processes and their variability are necessary to inform models that can quantify the feedbacks among processes and ecosystem responses to a changing world.

Predator transitory spillover induces trophic cascades in ecological sinks.

Understanding the effects of cross-system fluxes is fundamental in ecosystem ecology and biological conservation. Source-sink dynamics and spillover processes may link adjacent ecosystems by movement of organisms across system boundaries. However, effects of temporal variability in these cross-system fluxes on a whole marine ecosystem structure have not yet been presented. Here we show, using 35 y of multitrophic data series from the Baltic Sea, that transitory spillover of the top-predator cod from its main distribution area produces cascading effects in the whole food web of an adjacent and semi-isolated ecosystem. At varying population size, cod expand/contract their distribution range and invade/retreat from the neighboring Gulf of Riga, thereby affecting the local prey population of herring and, indirectly, zooplankton and phytoplankton via top-down control. The Gulf of Riga can be considered for cod a "true sink" habitat, where in the absence of immigration from the source areas of the central Baltic Sea the cod population goes extinct due to the absence of suitable spawning grounds. Our results add a metaecosystem perspective to the ongoing intense scientific debate on the key role of top predators in structuring natural systems. The integration of regional and local processes is central to predict species and ecosystem responses to future climate changes and ongoing anthropogenic disturbances.

Cohort dynamics give rise to alternative stable community states.

Many ecological systems can exhibit alternative stable states (ASS), which implies that ecological communities may diverge depending on their initial state, despite identical environmental conditions. Here we present a new mechanism that can cause ASS in competition systems. Using a physiologically structured model of competing populations, representing Baltic Sea sprat and herring and their resources, we show how cohort-driven population cycles may result in priority effects leading to ASS. Similar mechanisms could, depending on mortality level, also result in a "resident strikes back" phenomenon. We argue that the prerequisites for the occurrence of ASS in our model system, that is, communities with competing populations exhibiting cohort cycles and variation in size at maturation, may be common in ecological systems.

Predators with multiple ontogenetic niche shifts have limited potential for population growth and top-down control of their prey.

Catastrophic collapses of top predators have revealed trophic cascades and community structuring by top-down control. When populations fail to recover after a collapse, this may indicate alternative stable states in the system. Overfishing has caused several of the most compelling cases of these dynamics, and in particular Atlantic cod stocks exemplify such lack of recovery. Often, competition between prey species and juvenile predators is hypothesized to explain the lack of recovery of predator populations. The predator is then considered to compete with its prey for one resource when small and to subsequently shift to piscivory. Yet predator life history is often more complex than that, including multiple ontogenetic diet shifts. Here we show that no alternative stable states occur when predators in an intermediate life stage feed on an additional resource (exclusive to the predator) before switching to piscivory, because predation and competition between prey and predator do not simultaneously structure community dynamics. We find top-down control by the predator only when there is no feedback from predator foraging on the additional resource. Otherwise, the predator population dynamics are governed by a bottleneck in individual growth occurring in the intermediate life stage. Therefore, additional resources for predators may be beneficial or detrimental for predator population growth and strongly influence the potential for top-down community control.

Biological ensemble modeling to evaluate potential futures of living marine resources.

Natural resource management requires approaches to understand and handle sources of uncertainty in future responses of complex systems to human activities. Here we present one such approach, the "biological ensemble modeling approach," using the Eastern Baltic cod (Gadus morhua callarias) as an example. The core of the approach is to expose an ensemble of models with different ecological assumptions to climate forcing, using multiple realizations of each climate scenario. We simulated the long-term response of cod to future fishing and climate change in seven ecological models ranging from single-species to food web models. These models were analyzed using the "biological ensemble modeling approach" by which we (1) identified a key ecological mechanism explaining the differences in simulated cod responses between models, (2) disentangled the uncertainty caused by differences in ecological model assumptions from the statistical uncertainty of future climate, and (3) identified results common for the whole model ensemble. Species interactions greatly influenced the simulated response of cod to fishing and climate, as well as the degree to which the statistical uncertainty of climate trajectories carried through to uncertainty of cod responses. Models ignoring the feedback from prey on cod showed large interannual fluctuations in cod dynamics and were more sensitive to the underlying uncertainty of climate forcing than models accounting for such stabilizing predator-prey feedbacks. Yet in all models, intense fishing prevented recovery, and climate change further decreased the cod population. Our study demonstrates how the biological ensemble modeling approach makes it possible to evaluate the relative importance of different sources of uncertainty in future species responses, as well as to seek scientific conclusions and sustainable management solutions robust to uncertainty of food web processes in the face of climate change.

Larger but younger fish when growth outpaces mortality in heated ecosystem.

Ectotherms are predicted to 'shrink' with global warming, in line with general growth models and the temperature-size rule (TSR), both predicting smaller adult sizes with warming. However, they also predict faster juvenile growth rates and thus larger size-at-age of young organisms. Hence, the result of warming on the size-structure of a population depends on the interplay between how mortality rate, juvenile- and adult growth rates are affected by warming. Here, we use two-decade long time series of biological samples from a unique enclosed bay heated by cooling water from a nearby nuclear power plant to become 5-10 °C warmer than its reference area. We used growth-increment biochronologies (12,658 reconstructed length-at-age estimates from 2426 individuals) to quantify how >20 years of warming has affected body growth, size-at-age, and catch to quantify mortality rates and population size- and age structure of Eurasian perch (Perca fluviatilis). In the heated area, growth rates were faster for all sizes, and hence size-at-age was larger for all ages, compared to the reference area. While mortality rates were also higher (lowering mean age by 0.4 years), the faster growth rates lead to a 2 cm larger mean size in the heated area. Differences in the size-spectrum exponent (describing how the abundance declines with size) were less clear statistically. Our analyses reveal that mortality, in addition to plastic growth and size-responses, is a key factor determining the size structure of populations exposed to warming. Understanding the mechanisms by which warming affects the size- and the age structure of populations is critical for predicting the impacts of climate change on ecological functions, interactions, and dynamics.

Optimal energy allocation trade-off driven by size-dependent physiological and demographic responses to warming.

Body size-dependent physiological effects of temperature influence individual growth, reproduction, and survival, which govern animal population responses to global warming. Considerable knowledge has been established on how such effects can affect population growth and size structure, but less is known of their potential role in temperature-driven adaptation in life-history traits. In this study, we ask how warming affects the optimal allocation of energy between growth and reproduction and disentangle the underlying fitness trade-offs. To this end, we develop a novel dynamic energy budget integral projection model (DEB-IPM), linking individuals' size- and temperature-dependent consumption and maintenance via somatic growth, reproduction, and size-dependent energy allocation to emergent population responses. At the population level, we calculate the long-term population growth rate (fitness) and stable size structure emerging from demographic processes. Applying the model to an example of pike (Esox lucius), we find that optimal energy allocation to growth decreases with warming. Furthermore, we demonstrate how growth, fecundity, and survival contribute to this change in optimal allocation. Higher energy allocation to somatic growth at low temperatures increases fitness through survival of small individuals and through the reproduction of larger individuals. In contrast, at high temperatures, increased allocation to reproduction is favored because warming induces faster somatic growth of small individuals and increased fecundity but reduced growth and higher mortality of larger individuals. Reduced optimum allocation to growth leads to further reductions in body size and an increasingly truncated population size structure with warming. Our study demonstrates how, by incorporating general physiological mechanisms driving the temperature dependence of life-history traits, the DEB-IPM framework is useful for investigating the adaptation of size-structured organisms to warming.

Size- and food-dependent growth drives patterns of competitive dominance along productivity gradients.

Patterns of coexistence among competing species exhibiting size- and food-dependent growth remain largely unexplored. Here we studied mechanisms behind coexistence and shifts in competitive dominance in a size-structured fish guild, representing sprat and herring stocks in the Baltic Sea, using a physiologically structured model of competing populations. The influence of degree of resource overlap and the possibility of undergoing ontogenetic diet shifts were studied as functions of zooplankton and zoobenthos productivity. By imposing different size-dependent mortalities, we could study the outcome of competition under contrasting environmental regimes representing poor and favorable growth conditions. We found that the identity of the dominant species shifted between low and high productivity. Adding a herring-exclusive benthos resource only provided a competitive advantage over sprat when size-dependent mortality was high enough to allow for rapid growth in the zooplankton niche. Hence, the importance of a bottom-up effect of varying productivity was dependent on a strong top-down effect. Although herring could depress shared resources to lower levels than could sprat and also could access an exclusive resource, the smaller size at maturation of sprat allowed it to coexist with herring and, in some cases, exclude it. Our model system, characterized by interactions among size cohorts, allowed for consumer coexistence even at full resource overlap at intermediate productivities when size-dependent mortality was low. Observed shifts in community patterns were crucially dependent on the explicit consideration of size- and food-dependent growth. Accordingly, we argue that accounting for food-dependent growth and size-dependent interactions is necessary to better predict changes in community structure and dynamics following changes in major ecosystem drivers such as resource productivity and mortality, which are fundamental for our ability to manage exploitation of living resources in, e.g., fisheries.