Food, Fear and Defence - Behavioral and morphological adaptation of juvenile perch under the risk of predation

Predation is one of the major structuring forces in animal communities, because most predators hunt selectively. This favors characteristics in prey that facilitate the avoidance of predation. Correspondingly, various and often plastic morphological and behavioral defense strategies have been found throughout numerous taxa. However, the expression of defense traits often confronts prey with time and/or resource allocation trade-offs. Thus behavioral defenses, like watching out for potential threats, inactivity and hiding largely are incompatible with foraging and the energy expenditure to build up morphological defenses cannot be allocated into e.g. growth, storage or reproduction. Therefore, additional effects, like an individual’s nutritional status, resource use, size and/or age balance, often influenced of these trade-offs. Furthermore, theoretical results indicate that the plasticity of a trait is per se determined by the adaptiveness of a given phenotype, its associated costs and the variability of the selective environmental agent. This illustrates the complexity of patterns shaping animal behavioral and morphological defense expression under predation risk. Eurasian perch (Perca fluviatilis L.) is a common freshwater species throughout Europe, where juvenile perch display consistent variation in morphology and behavior and both traits are sensitive to the environment and especially to predation risk. Therefore perch is an optimal model organism to study the complex defense trait dynamics in predator-prey interactions. In the first study, a common garden setup was used to examine the genetic and environmental components of the morphological variation from two lake populations with differences in size-specific predation risk. We found differences in head and jaw length and slight differences in body depth between the wild young-of-the-year perch from Lake Ängersjön and Lake Fisksjön. The differences found between the wild fish from the two lakes were, however, not maintained under common garden rearing. The observed morphological divergence between the wild juvenile perch from Lake Ängersjön and Lake Fisksjön seems to stem mainly from a plastic response to different conditions in the two lakes. Morphological traits are not influenced by direct reaction to the size-specific risk of cannibalism, but probably stem from a combination of different environmental characteristics, including resource and habitat use, and the density of other piscivores such as pike. In the second chapter young-of-the-year perch were reared on either fish larvae or zooplankton to investigate whether the use of divergent resources changes the reaction to a novel surrounding and the behavior under the threat of predation. Both phenotypes reacted differently under predation risk and inspected the predator more frequently when their familiar prey was presented during the trials, indicating that resource polymorphism may influence risk-taking behavior in juvenile fish. The third study used juvenile 0+ and 1+ perch in an experimental approach to vary the factor of predation risk. Predators were able to feed on perch during a mesocosm period. Perceived predation risk affected the behavior and the morphology of both age classes of perch. Boldness decreased with the intensity of predation, while morphology of perch changed towards deeper bodied individuals. Although it remains unanswered if these changes are a result of selective predation or phenotypic response of the prey, the latter explanation is assumed to be conclusive because there was no correlation between the observed changes in the length-frequency distributions and the predation risk of perch. In the final study, we measured behavioral and morphological traits in 0+ perch and compared their selective values in response to the two most common predators, adult perch and pike. Selection on behavioral traits was higher than on morphological traits and perch predators preyed overall more selectively than pike. Pike tended to positively choose shallow bodied and non-vigilant individuals. In contrast, perch predators selected mainly for bolder juvenile perch. These results indicate that shyness and increased body depth might be adaptive for juvenile perch under predation risk. However, the relative specific predation intensity for the divergent traits differed between the predators, providing some additional ideas why juvenile perch display such a high degree of phenotypic plasticity

Facing different predators: adaptiveness of behavioral and morphological traits under predation

Predation is thought to be one of the main structuring forces in animal communities. However, selective predation is often measured on isolated traits in response to a single predatory species, but only rarely are selective forces on several traits quantified or even compared between different predators naturally occurring in the same system. In the present study, we therefore measured behavioral and morphological traits in young-of-the-year Eurasian perch Perca fluviatilis and compared their selective values in response to the 2 most common predators, adult perch and pike Esox lucius. Using mixed effects models and model averaging to analyze our data, we quantified and compared the selectivity of the 2 predators on the different morphological and behavioral traits. We found that selection on the behavioral traits was higher than on morphological traits and perch predators preyed overall more selectively than pike predators. Pike tended to positively select shallow bodied and nonvigilant individuals (i.e. individuals not performing predator inspection). In contrast, perch predators selected mainly for bolder juvenile perch (i.e. individuals spending more time in the open, more active), which was most important. Our results are to the best of our knowledge the first that analyzed behavioral and morphological adaptations of juvenile perch facing 2 different predation strategies. We found that relative specific predation intensity for the divergent traits differed between the predators, providing some additional ideas why juvenile perch display such a high degree of phenotypic plasticity

Plasticity and consistency of behavioural responses to predation risk in laboratory environments

The individual animal is currently a major focus of behavioural research and an increasing number of studies raise the question of how between-individual behavioural consistency and behavioural plasticity interact. Applying the reaction norm concept on groups, our study addresses both of these aspects in one framework and within an animal's natural social environment. Risk-taking behaviour in 1-year-old perchPerca fluviatiliswas assayed in aquarium experiments before and after the fish were subjected to the presence or absence of a piscivorous predator for 3weeks. To analyse the inter-individual behavioural variation across the repeated measurements, we dissected the behavioural change across the predator treatment into individual constant and plastic components using hierarchical mixed-effects models. During the predator treatment, juvenile perch increased in boldness and decreased in vigilance, the magnitude of these behavioural changes was influenced by group composition. However, the behavioural changes were not influenced by the presence of a predator, indicating the difficulties in generating realistic long-term predation pressure in the laboratory. Individuals differed in the relative increase in boldness across the predator treatment and, thus, varied in the shape of their reaction norms. In accordance, the best linear unbiased predictors, extracted from the random effects of separate linear mixed-effects models for the data before and after the predator treatment were only weakly correlated. Hence, between-individual variation seems to change under laboratory conditions and therewith not necessarily represents the initially present ‘natural’ variation, giving important implications for the conduction and interpretation of behavioural experiments

The effect of anesthetics on carotenoid pigmentation and behavior in Arctic char (Salvelinus alpinus)

Status of individual animals is often shown in pigmentation. For instance, stress responsiveness is associated with melanin-based pigmentation in vertebrates in general. This pattern is evident in Atlantic salmon (Salmo salar) and rainbow trout (Oncorhynchus mykiss), with melanin-based spots indicating stress coping style. Arctic char (Salvelinus alpinus) differ from other salmonids in pigmentation but have an association between carotenoid-based pigmentation and stress coping style. These pigmentation differences could be used as a fast and simple tool for improving breeding programs. However, the procedure for photographing individuals is stressful. Therefore, we wanted to investigate if 3 common inhalation anesthetics could be used to reduce the stress involved in the procedure compared to a no-anesthetics group. Behavior was also monitored during the anesthetization. All 3 anesthetics (Aquacalm, Benzocaine, and MS-222) differed in pigmentation compared to the no-anesthetics group by having a higher number of spots. In the anesthetic treatments as well as the no-anesthetics group, the fish had elevated plasma cortisol levels. In fact, the no-anesthetics group had higher cortisol than treated fish. This was probably because of procedural differences such as time affecting the stress response. Furthermore, in a long-term experiment, all fish survived and had similar condition factors 1 week after photographing as before. Therefore, the method for photographing Arctic char is deemed safe and could be used as a tool for estimating stress coping style, but careful planning is needed for experiments using i

Dominance and stress signalling of carotenoid pigmentation in Arctic charr (Salvelinus alpinus): Lateralization effects?

Social conflicts are usually solved by agonistic interactions where animals use cues to signal dominance or subordinance. Pigmentation change is a common cue used for signalling. In our study, the involvement of carotenoid-based pigmentation in signalling was investigated in juvenile Arctic charr (Salvelinus alpinus). Size-matched pairs were analysed for pigmentation both before and after being tested for competitive ability. We found that dominant individuals had fewer carotenoid-based spots on the right and left sides as well as lower plasma cortisol levels compared to subordinate individuals. Further, the number of spots on both sides was positively associated with plasma cortisol levels. These results indicate that carotenoid-based pigmentation in Arctic charr signals dominance and stress coping style. Further, it also appears as if carotenoid-based pigmentation is lateralized in Arctic charr, and that the right side signals aggression and dominance whereas the left side signals stress responsiveness

Anaesthesia and handling stress effects on pigmentation and monoamines in Arctic charr

Stress responsiveness differs between individuals and is often categorized into different stress coping styles. Using these stress coping styles for selection in fish farming could be beneficial, since stress is one main factor affecting welfare. In Arctic charr (Salvelinus alpinus) carotenoid pigmentation is associated with stress responsiveness and stress coping styles. Thus this could be an important tool to use for selection of stress resilient charr. However, anaesthetics seem to affect carotenoid pigmentation, and it would be better if the method for selection could be implemented during normal maintenance, which usually includes anaesthetics. Therefore, this study investigated how the use of anaesthetics affected carotenoid pigmentation, i.e. number of spots, over time compared to no-anaesthetic treatment. Additionally, the stress indicators monoamines and glucocorticoids were investigated. The results indicate that the anaesthetic MS-222 affects number of spots on the right side. This anaesthetic also increased dopaminergic activity in the telencephalon. Both brain dopaminergic and serotonergic activity was associated with spottiness. Further, behaviour during anaesthetization was associated with spots on the left side, but not the right side. Repetition of the same treatment seemed to affect spot numbers on the right side. In conclusion, this study shows that inducing stress in charr affects the carotenoid spots. Thus, it is possible to use anaesthetics when evaluating spottiness although careful planning is needed

Screening of benzodiazepines in thirty European rivers

Pharmaceuticals as environmental contaminants have received a lot of interest over the past decade but, for several pharmaceuticals, relatively little is known about their occurrence in European surface waters. Benzodiazepines, a class of pharmaceuticals with anxiolytic properties, have received interest due to their behavioral modifying effect on exposed biota. In this study, our results show the presence of one or more benzodiazepine(s) in 86% of the analyzed surface water samples (n = 138) from 30 rivers, representing seven larger European catchments. Of the 13 benzodiazepines included in the study, we detected 9, which together showed median and mean concentrations (of the results above limit of quantification) of 5.4 and 9.6 ng L−1, respectively. Four benzodiazepines (oxazepam, temazepam, clobazam, and bromazepam) were the most commonly detected. In particular, oxazepam had the highest frequency of detection (85%) and a maximum concentration of 61 ng L−1. Temazepam and clobazam were found in 26% (maximum concentration of 39 ng L−1) and 14% (maximum concentration of 11 ng L−1) of the samples analyzed, respectively. Finally, bromazepam was found only in Germany and in 16 out of total 138 samples (12%), with a maximum concentration of 320 ng L−1. This study clearly shows that benzodiazepines are common micro-contaminants of the largest European river systems at ng L−1 levels. Although these concentrations are more than a magnitude lower than those reported to have effective effects on exposed biota, environmental effects cannot be excluded considering the possibility of additive and sub-lethal effects

Balancing the response to predation-the effects of shoal size, predation risk and habituation on behaviour of juvenile perch

Group size, predation risk and habituation are key drivers of behaviour and evolution in gregarious prey animals. However, the extent to which they interact in shaping behaviour is only partially understood. We analyzed their combined effects on boldness and vigilance behaviour in juvenile perch (Perca fluviatilis) by observing individuals in groups of one, two, three and five faced with four different levels of predation risk in a repeated measures design. The perch showed an asymptotic increase in boldness with increasing group size and the highest per capita vigilance in groups of two. With increasing predation risk, individuals reduced boldness and intensified vigilance. The interaction between group size and predation risk influenced vigilance but not boldness. In this context, individuals in groups of two elevated their vigilance compared to individuals in larger groups only when at higher risk of predation. Further, as only group size, they significantly reduced vigilance at the highest level of risk. With increasing habituation, solitary individuals became considerably bolder. Also, predation risk affected boldness only in the more habituated situation. Hence, repeated measures may be essential to correctly interpret certain relationships in behaviour. Our results suggest that perch may adjust boldness behaviour to group size and predation risk independently. This is rather unexpected since in theory, natural selection would strongly favour an interactive adjustment. Finally, vigilance might be particularly effective in groups of two due to the intense monitoring and detailed response to changing levels of risk