Effects of pre-winter cortisol exposure on condition, diet, and morphology of wild juvenile brown trout (Salmo trutta).

Winter is an energetically challenging period for many animals in temperate regions because of the relatively harsh environmental conditions and reduction in food availability during this season. Moreover, stressors experienced by individuals in the fall can affect their subsequent foraging strategy and energy stores after exposure has ended, referred to as carryover effects. We used exogenous cortisol manipulation of wild juvenile brown trout (Salmo trutta) in the fall to simulate a physiological stress response and then investigated short-term (2 weeks) and long-term (4 months) effects on condition metrics (hepatosomatic index and water muscle content), diet (stomach contents and stable isotopes), and morphology during growth in freshwater. We revealed some short-term impacts, likely due to handling stress, and long-term (seasonal) changes in diet, likely reflecting prey availability. Unfortunately, we had very few recaptures of cortisol-treated fish at long-term sampling, limiting detailed analysis about cortisol effects at that time point. Nonetheless, the fish that were sampled showed elevated stable isotopes, suggestive of a cortisol effect long after exposure. This is one of few studies to investigate whether cortisol influences foraging and morphology during juvenile growth, thus extending the knowledge of proximate mechanisms influencing ecologically-relevant phenotypes.

No Evidence for Long-Term Carryover Effects in a Wild Salmonid Fish.

AbstractEarly-life experiences can shape life histories and population dynamics of wild animals. To examine whether stressful stimuli experienced in early life resulted in carryover effects in later life stages, we conducted several experimental manipulations and then monitored wild fish with passive integrated transponder tags during juvenile out-migration and adult return migration. In total, 3,217 juvenile brown trout (Salmo trutta) were subjected to one of six manipulations: chase to exhaustion, thermal challenge, food deprivation, low-concentration cortisol injection, high-concentration cortisol injection, and sham injection, plus a control group. Cortisol and food deprivation treatments were previously shown to have short-term effects on juveniles, such as lower survival to out-migration and changes in migration timing. However, it remained unknown whether any of the six manipulations had effects that carried over into the adult phase. We therefore investigated whether these extrinsic manipulations, as well as intrinsic factors (size and condition), affected probability of return as adults and time spent at sea. Of the 1,273 fish that out-migrated, 146 returned as adults. We failed to detect any effect of treatments on return rates, while high-concentration cortisol weakly affected time spent at sea in one tagging event. We also found that juvenile condition was positively correlated to likelihood of adult return in only one tagging event. Overall, our findings did not identify either intrinsic factors or extrinsic stressful early-life experiences that have strong effects on fish that survive to adulthood. This suggests that some species may be more resilient than others to stressful stimuli encountered early in life.

Comparative Analyses of Phenotypic Trait Covariation within and among Populations.

Many morphological, behavioral, physiological, and life-history traits covary across the biological scales of individuals, populations, and species. However, the processes that cause traits to covary also change over these scales, challenging our ability to use patterns of trait covariance to infer process. Trait relationships are also widely assumed to have generic functional relationships with similar evolutionary potentials, and even though many different trait relationships are now identified, there is little appreciation that these may influence trait covariation and evolution in unique ways. We use a trait-performance-fitness framework to classify and organize trait relationships into three general classes, address which ones more likely generate trait covariation among individuals in a population, and review how selection shapes phenotypic covariation. We generate predictions about how trait covariance changes within and among populations as a result of trait relationships and in response to selection and consider how these can be tested with comparative data. Careful comparisons of covariation patterns can narrow the set of hypothesized processes that cause trait covariation when the form of the trait relationship and how it responds to selection yield clear predictions about patterns of trait covariation. We discuss the opportunities and limitations of comparative approaches to evaluate hypotheses about the evolutionary causes and consequences of trait covariation and highlight the importance of evaluating patterns within populations replicated in the same and in different selective environments. Explicit hypotheses about trait relationships are key to generating effective predictions about phenotype and its evolution using covariance data.

Morphological, physiological and dietary covariation in migratory and resident adult brown trout (Salmo trutta).

The causes and consequences of trait relationships within and among the categories of physiology, morphology, and life-history remain poorly studied. Few studies cross the boundaries of these categories, and recent reviews have pointed out not only the dearth of evidence for among-category correlations but that trait relationships may change depending on the ecological conditions a population faces. We examined changes in mean values and correlations between traits in a partially migrant population of brown trout when migrant sea-run and resident stream forms were breeding sympatrically. Within each sex and life-history strategy group, we used carbon and nitrogen stable isotopes to assess trophic level and habitat use; assessed morphology which reflects swimming and foraging ability; measured circulating cortisol as it is released in response to stressors and is involved in the transition from salt to freshwater; and determined oxidative status by measuring oxidative stress and antioxidants. We found that sea-run trout were larger and had higher values of stable isotopes, cortisol and oxidative stress compared to residents. Most groups showed some correlations between morphology and diet, indicating individual resource specialization was occurring, and we found consistent correlations between morphology and cortisol. Additionally, relationships differed between the sexes (cortisol and oxidative status were related in females but not males) and between life-history strategies (habitat use was related to oxidative status in male sea-run trout but not in either sex of residents). The differing patterns of covariation between the two life-history strategies and between the sexes suggest that the relationships among phenotypic traits are subjected to different selection pressures, illustrating the importance of integrating multiple phenotypic measures across different trait categories and contrasting life-history strategies.

Causes and Consequences of Behavioral Interference between Species.

Behavioral interference between species, such as territorial aggression, courtship, and mating, is widespread in animals. While aggressive and reproductive forms of interspecific interference have generally been studied separately, their many parallels and connections warrant a unified conceptual approach. Substantial evidence exists that aggressive and reproductive interference have pervasive effects on species coexistence, range limits, and evolutionary processes, including divergent and convergent forms of character displacement. Alien species invasions and climate change-induced range shifts result in novel interspecific interactions, heightening the importance of predicting the consequences of species interactions, and behavioral interference is a fundamental but neglected part of the equation. Here, we outline priorities for further theoretical and empirical research on the ecological and evolutionary consequences of behavioral interference.

Nutritional physiology and ecology of wildlife in a changing world.

Over the last century, humans have modified landscapes, generated pollution and provided opportunities for exotic species to invade areas where they did not evolve. In addition, humans now interact with animals in a growing number of ways (e.g. ecotourism). As a result, the quality (i.e. nutrient composition) and quantity (i.e. food abundance) of dietary items consumed by wildlife have, in many cases, changed. We present representative examples of the extent to which vertebrate foraging behaviour, food availability (quantity and quality) and digestive physiology have been modified due to human-induced environmental changes and human activities. We find that these effects can be quite extensive, especially as a result of pollution and human-provisioned food sources (despite good intentions). We also discuss the role of nutrition in conservation practices, from the perspective of both in situ and ex situ conservation. Though we find that the changes in the nutritional ecology and physiology of wildlife due to human alterations are typically negative and largely involve impacts on foraging behaviour and food availability, the extent to which these will affect the fitness of organisms and result in evolutionary changes is not clearly understood, and requires further investigation.

If and when: intrinsic differences and environmental stressors influence migration in brown trout (Salmo trutta).

Partial migration is a common phenomenon, yet the causes of individual differences in migratory propensity are not well understood. We examined factors that potentially influence timing of migration and migratory propensity in a wild population of juvenile brown trout (Salmo trutta) by combining experimental manipulations with passive integrated transponder telemetry. Individuals were subjected to one of six manipulations: three designed to mimic natural stressors (temperature increase, food deprivation, and chase by a simulated predator), an injection of exogenous cortisol designed to mimic an extreme physiological challenge, a sham injection, and a control group. By measuring length and mass of 923 individuals prior to manipulation and by monitoring tagged individuals as they left the stream months later, we assessed whether pre-existing differences influenced migratory tendency and timing of migration, and whether our manipulations affected growth, condition, and timing of migration. We found that pre-existing differences predicted migration, with smaller individuals and individuals in poor condition having a higher propensity to migrate. Exogenous cortisol manipulation had the largest negative effect on growth and condition, and resulted in an earlier migration date. Additionally, low-growth individuals within the temperature and food deprivation treatments migrated earlier. By demonstrating that both pre-existing differences in organism state and additional stressors can affect whether and when individuals migrate, we highlight the importance of understanding individual differences in partial migration. These effects may carry over to influence migration success and affect the evolutionary dynamics of sub-populations experiencing different levels of stress, which is particularly relevant in a changing world.

Size-Dependent Consequences of Exogenous Cortisol Manipulation on Overwinter Survival and Condition of Largemouth Bass.

Little is known about the size-dependent consequences of stressors on wild animals, which is particularly relevant during winter where size-specific trends in survival are common. Here, exogenous cortisol manipulation was used to investigate the effect of a physiological challenge on overwinter mortality and spring condition of largemouth bass (Micropterus salmoides) across a range of body sizes. Fish were wild-caught in the fall, assigned into either control or cortisol manipulated treatments, and held in replicated experimental ponds. For bass that survived the winter, length, mass, and health metrics (e.g., gonadosomatic index [GSI], hepatosomatic index [HSI], and water content) were determined in the spring. Winter survival was marginally lower for cortisol treated bass; however, there was no influence of initial length, mass, or condition on overwinter survival. When bass were grouped by size, survival was significantly higher for bass 300-350 mm in length compared to those <200 mm. The treatment did not strongly influence spring health metrics, suggesting that largemouth bass that survived the winter were able to recover from the effects of the cortisol elevation. Initial size and sex were linked to some spring health metrics, with large females having the highest GSI and HSI scores. Overall, results from this study do not support the notion that there are size-dependent responses to cortisol manipulation in a teleost fish. Rather, this type of physiological challenge may modulate the natural rates of winter mortality that are primarily driven by starvation and predation, independent of body size, in subadult and adult largemouth bass.

Short-term and long-term effects of transient exogenous cortisol manipulation on oxidative stress in juvenile brown trout.

In the wild, animals are exposed to a growing number of stressors with increasing frequency and intensity, as a result of human activities and human-induced environmental change. To fully understand how wild organisms are affected by stressors, it is crucial to understand the physiology that underlies an organism's response to a stressor. Prolonged levels of elevated glucocorticoids are associated with a state of chronic stress and decreased fitness. Exogenous glucocorticoid manipulation reduces an individual's ability to forage, avoid predators and grow, thereby limiting the resources available for physiological functions like defence against oxidative stress. Using brown trout (Salmo trutta), we evaluated the short-term (2 weeks) and long-term (4 months over winter) effects of exogenous cortisol manipulations (versus relevant shams and controls) on the oxidative status of wild juveniles. Cortisol caused an increase in glutathione over a 2 week period and appeared to reduce glutathione over winter. Cortisol treatment did not affect oxidative stress levels or low molecular weight antioxidants. Cortisol caused a significant decrease in growth rates but did not affect predation risk. Over-winter survival in the stream was associated with low levels of oxidative stress and glutathione. Thus, oxidative stress may be a mechanism by which elevated cortisol causes negative physiological effects.

The ecological and evolutionary stability of interspecific territoriality.

Interspecific territoriality may play an important role in structuring ecological communities, but the causes of this widespread form of interference competition remain poorly understood. Here, we investigate the phenotypic, ecological and phylogenetic correlates of interspecific territoriality in wood warblers (Parulidae). Interspecifically territorial species have more recent common ancestors and are more similar phenotypically, and are more likely to hybridise, than sympatric, non-interspecifically territorial species. After phylogenetic corrections, however, similarity in plumage and territorial song are the only significant predictors of interspecific territoriality besides syntopy (fine-scale geographic overlap). Our results do not support the long-standing hypothesis that interspecific territoriality occurs only under circumstances in which niche divergence is restricted, which combined with the high incidence of interspecific territoriality in wood warblers (39% of species), suggests that this interspecific interaction is more stable, ecologically and evolutionarily, than commonly assumed.

The evolutionary consequences of interspecific aggression.

Competition has always been a cornerstone of evolutionary biology, and aggression is the predominant form of direct competition in animals, but the evolutionary effects of aggression between species are curiously understudied. Only in the past few years, existing theoretical frameworks have been extended to include interspecific aggression, and significant empirical advances have been made. After arguing that agonistic character displacement (ACD) theory provides the most suitable theoretical framework, we review new empirical evidence for ACD and the results of mathematical models of the process. We consider how ACD can be distinguished empirically from ecological and reproductive character displacement and the additional challenges posed by developmental plasticity. We also provide the first taxonomically broad review of theoretical and empirical work on the effects of interspecific aggression on species coexistence and range limits. We conclude by highlighting promising directions for future research on the evolutionary effects of interspecific aggression.

Diversifying and correlational selection on behavior toward conspecific and heterospecific competitors in brook stickleback (Culaea inconstans).

Behaviors toward heterospecifics and conspecifics may be correlated because of shared mechanisms of expression in both social contexts (nonadaptive covariation) or because correlational selection favors adaptive covariation. We evaluated these hypotheses by comparing behavior toward conspecifics and heterospecifics in brook stickleback (Culaea inconstans) from three populations sympatric with and three allopatric from a competitor, the ninespine stickleback (Pungitius pungitius). Behavioral traits were classified into three multivariate components: overt aggression, sociability, and activity. The correlation of behavior between social contexts for both overt aggression and activity varied among populations in a way unrelated to sympatry with ninespine stickleback, while mean aggression was reduced in sympatry. Correlations in allopatric populations suggest that overt aggression and activity may genetically covary between social contexts for nonadaptive reasons. Sociability was rarely correlated in allopatry but was consistently correlated in sympatry despite reduced mean sociability, suggesting that correlational selection may favor a sociability syndrome in brook stickleback when they coexist with ninespine stickleback. Thus, interspecific competition may impose diversifying selection on behavior among populations, although the causes of correlated behavior toward conspecifics and heterospecifics and whether it can evolve in one social context independent of the other may depend on the type of behavior.

Ecology and evolution of resource-related heterospecific aggression.

Direct interactions among conspecific and heterospecific animals are often mediated by aggressive behavior. We analyze the ecology and evolution of resourc-related heterospecific aggression (HA) by reviewing and meta-analysing 126 studies, contrasting HA with conspecfic aggression (CA), and discussing terminological confusions and conceptual models. HA occurred in 78% of tests (n = 459), suggesting a high prevalence and potential effect on niche use and community structure. The benefits of both CA and HA are linked to resource defensibility and abundance, yet HA can change independently of CA. Ecological inferences about HA are often weak because they assume that interference always results from resource competition, and evolutionary inferences made by comparing HA to CA are also weak because they usually ignore history. We believe that comparisons between situations where a focal species is allopatric from and sympatric with a heterospecfic competitor provide better opportunities to test hypotheses about HA. In general, according to our data set, aggression was higher with increased resource overlap as expected, both because CA was greater than HA, and HA was greater within compared to between genera. Progress in understanding HA requires distinguishing traits (aggressive behavior) from interactions (agonism, interference), as well as from the ecological and evolutionary causer (competition, ancestry) and consequences (dominance, territoriality, exclusion) of those interactions.