Feeding specialists on fatty acid-rich prey have higher gonad weights: Pay-off in Baltic perch?

Individual specialization is a common phenomenon throughout the animal kingdom. Many studies have identified intraspecific competition as one of the main drivers for individual feeding specialization. These studies have mainly considered the quantity of resources, commonly overlooking qualitative aspects of the diet. For example, highly unsaturated fatty acids of the omega-3 class (omega-3 HUFAs) are related to optimal health and growth in consumers. However, little is known on direct fitness consequences for consumers of natural populations that specialize on high-quality resources, such as those rich in omega-3 HUFAs. Despite being such an important qualitative aspect of the diet, it is still unknown whether natural populations show among-individual variation in their choice on prey items that are either rich or poor in HUFAs, and how it affects individual performances. In this study, we investigated whether there is individual feeding specialization and whether it is related to fitness benefits, in a population of perch (Perca fluviatilis) in the Baltic Sea. The contribution of pelagic planktivorous fish to the diet varied from 17% to 61% among perch individuals, as depicted by stable isotope mixing models. This variation in diet was also qualitative, as the omega-3 HUFA content differed among prey types. Specialization on the high-quality resource pelagic planktivorous fish was associated with the proportions of omega-3 HUFA in the individuals' muscles and individuals among those with the highest proportions of omega-3 HUFAs had the greatest relative gonad weight (gonadosomatic index, GSI), a proxy for reproductive investment. Thus, our results highlight the function of food quality for individual specialization and its potential to have direct fitness benefits, playing a major role in shaping ecological interactions

Life-history evolution in harvested populations: the role of natural predation

Models and experiments of the evolution of age- and/or size-at-maturation in response to population harvesting have consistently shown that selective harvesting of older and larger individuals can cause earlier maturation. These predictions, however, are all based on single-species considerations and thus crucially neglect the selective forces caused or mediated by species interactions. Here we develop simple models of phenotypic evolution of age-at-first-reproduction in a prey population subject to different types of predation and harvesting. We show that, in the presence of natural predation, the potential evolutionary response of age-at-first-reproduction to population harvesting is ambiguous: harvesting can cause either earlier or later maturation depending on the type of predator interaction and its strength relative to the fishing pressure. The counterintuitive consequences of harvesting result from the indirect effects that harvesting of a prey population has on the selection pressure exerted by its natural predator, since this selection pressure itself typically depends on prey density. If harvest rates are high, the direct selection pressures considered in classical analyses prevail and harvesting decreases the age-at-first-reproduction, whereas at lower harvest rates the indirect, inter-specifically mediated effects of harvesting can qualitatively overturn predictions based on simpler single-species models

Smaller species but larger stages: Warming effects on inter- and intraspecific community size structure

Global warming can alter size distributions of animal communities, but the contribution of size shifts within versus between species to such changes remains unknown. In particular, it is unclear if expected body size shrinkage in response to warming, observed at the interspecific level, can be used to infer similar size shifts within species. In this study, we compare warming effects on interspecific (relative species abundance) versus intraspecific (relative stage abundance) size structure of competing consumers by analyzing stage-structured bioenergetic food web models consisting of one or two consumer species and two resources, parameterized for pelagic plankton. Varying composition and temperature and body size dependencies in these models, we predicted interspecific versus intraspecific size structure across temperature. We found that warming shifted community size structure toward dominance of smaller species, in line with empirical evidence summarized in our review of 136 literature studies. However, this result emerged only given a size-temperature interaction favoring small over large individuals in warm environments. In contrast, the same mechanism caused an intraspecific shift toward dominance of larger (adult) stages, reconciling disparate observations of size responses within and across zooplankton species in the literature. As the empirical evidence for warming-driven stage shifts is scarce and equivocal, we call for more experimental studies on intraspecific size changes with warming. Understanding the global warming impacts on animal communities requires that we consider and quantify the relative importance of mechanisms concurrently shaping size distributions within and among species

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

Ecosystem heating experiment reveals sex-specific growth responses in fish

Size-specific body growth responses to warming are common among animal taxa, but sex-specific responses are poorly known. Here we ask if body growth responses to warming are sex-dependent, and if such sex-specific responses vary with size and age. This was tested with sex-specific data of back-calculated individual growth trajectories, in European perch (Perca fluviatilis) from a long-term whole-ecosystem warming experiment (6.3 C above the surrounding sea). Warming led to both size- and sex-specific differences in growth responses. Warming had a consistent positive effect on body growth of females, but negative effects on male growth at size > 10 cm and age > 2 years. These sex-specific growth responses translate to an increased degree of female-biased sexual size dimorphism (in length-at-age) with warming. Although the exact temperature-mediated effects underlying differential growth responses could not be resolved, results imply global warming may have highly different effects during ontogeny of male and female perch. Such effects should be considered in climate warming scenarios concerning fish growth, population size-structure, and dynamics of aquatic food webs that include fish exhibiting sexual size dimorphism

Effects of Warming on Intraguild Predator Communities with Ontogenetic Diet Shifts

Species 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

Decades of warming alters maturation and reproductive investment in fish

How does warming affect maturation and reproductive investment in ectotherms? Younger age and smaller size at maturation, as well as altered reproduction processes, have been found in a few species subjected to elevated temperatures. These observations, however, come from studies that do not distinguish effects of warming on maturation from those on growth, are also restricted to single generation responses to warming, or have additional stressors besides warming in the study system. Here, we study warming effects on maturation and reproductive investment in wild, unexploited fish populations using a whole-ecosystem heating experiment. The experiment is conducted on Eurasian perch (Perca fluviatilis) in a heated and control area (with > 5 degrees C temperature difference) in the Baltic Sea. We compare female perch size at maturation using estimated probabilistic maturation reaction norms (PMRNs) and the gonado-somatic index over 17 years of heating, spanning approximately five to eight perch generations. Using the PMRN approach, we show that warming has substantial effects on maturation size independent of warming-induced changes in body growth. We found that young fish mature at a smaller size and invest more in developing their gonads in the heated population than in the unheated population. Our findings suggest that warming effects on reproductive investment may initially compensate for the cost of warming-induced decrease in maturation size caused by the trade-off between early maturation and size-dependent fecundity. After multiple additional generations of warming, maturation and reproduction traits in perch differed from those in the first generations following the onset of warming, which suggests that warming-induced evolution may have occurred. Our study is particularly relevant in the context of climate change because of the unusually large temperature difference between the areas and the fact that the heating occurred on an ecosystem level. We call for experimental studies resolving mechanisms of trait responses to warming across generations, complemented with genomic analyses, to aid understanding of organisms' long-term responses to climate change

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