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.

Biodiversity transformations in the global ocean: A climate change and conservation management perspective.

Understanding the biological diversity of different communities and evaluating the risks to biological sustainability in a time of rapid environmental change is a key challenge for providing an adapting management approach for biodiversity transformations in the ocean linked to human well-being. (Photo credit: Andrea Belgrano).

Mechanistic Temperature-Size Rule Explanation Should Reconcile Physiological and Mortality Responses to Temperature.

AbstractThe temperature-size rule is one of the universal rules in ecology and states that ectotherms in warmer waters will grow faster as juveniles, mature at smaller sizes and younger ages, and reach smaller maximum body sizes. Many models have unsuccessfully attempted to reproduce temperature-size rule-consistent life histories by using two-term (anabolism and catabolism) Pütter-type growth models, such as the von Bertalanffy. Here, we present a physiologically structured individual growth model, which incorporates an energy budget and optimizes energy allocation to growth, reproduction, and reserves. Growth, maturation, and reproductive output emerge as a result of life-history optimization to specific physiological rates and mortality conditions. To assess which processes can lead to temperature-size rule-type life histories, we simulate 42 scenarios that differ in temperature and body size dependencies of intake, metabolism, and mortality rates. Results show that the temperature-size rule can emerge in two ways. The first way requires both intake and metabolism to increase with temperature, but the temperature-body size interaction of the two rates must lead to relatively faster intake increase in small individuals and relatively larger metabolism increase in large ones. The second way requires only higher temperature-driven natural mortality and faster intake rates in early life (no change in metabolic rates is needed). This selects for faster life histories with earlier maturation and increased reproductive output. Our model provides a novel mechanistic and evolutionary framework for identifying the conditions necessary for the temperature-size rule. It shows that the temperature-size rule is likely to reflect both physiological changes and life-history optimization and that use of von Bertalanffy-type models, which do not include reproduction processes, can hinder our ability to understand and predict ectotherm responses to climate change.

Integrative Approaches to Understanding Organismal Responses to Aquatic Deoxygenation.

AbstractOxygen bioavailability is declining in aquatic systems worldwide as a result of climate change and other anthropogenic stressors. For aquatic organisms, the consequences are poorly known but are likely to reflect both direct effects of declining oxygen bioavailability and interactions between oxygen and other stressors, including two-warming and acidification-that have received substantial attention in recent decades and that typically accompany oxygen changes. Drawing on the collected papers in this symposium volume ("An Oxygen Perspective on Climate Change"), we outline the causes and consequences of declining oxygen bioavailability. First, we discuss the scope of natural and predicted anthropogenic changes in aquatic oxygen levels. Although modern organisms are the result of long evolutionary histories during which they were exposed to natural oxygen regimes, anthropogenic change is now exposing them to more extreme conditions and novel combinations of low oxygen with other stressors. Second, we identify behavioral and physiological mechanisms that underlie the interactive effects of oxygen with other stressors, and we assess the range of potential organismal responses to oxygen limitation that occur across levels of biological organization and over multiple timescales. We argue that metabolism and energetics provide a powerful and unifying framework for understanding organism-oxygen interactions. Third, we conclude by outlining a set of approaches for maximizing the effectiveness of future work, including focusing on long-term experiments using biologically realistic variation in experimental factors and taking truly cross-disciplinary and integrative approaches to understanding and predicting future effects.

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.

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.

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.

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.

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.

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.