A lake as a microcosm: reflections on developments in aquatic ecology

In the present study, we aim at relating Forbes' remarkable paper on "The lake as a microcosm", published 125 years ago, to the present status of knowledge in our own research group. Hence, we relate the observations Forbes made to our own microcosm, Lake Krankesjon in southern Sweden, that has been intensively studied by several research groups for more than three decades. Specifically, we focus on the question: Have we made any significant progress or did Forbes and colleagues blaze the trail through the unknown wilderness and we are mainly paving that intellectual road? We conclude that lakes are more isolated than many other biomes, but have, indeed, many extensions, for example, input from the catchment, fishing and fish migration. We also conclude that irrespective of whether lakes should be viewed as microcosms or not, the paper by Forbes has been exceptionally influential and still is, especially since it touches upon almost all aspects of the lake ecosystem, from individual behaviour to food web interactions and environmental issues. Therefore, there is no doubt that even if 125 years have passed, Forbes' paper still is a source of inspiration and deserves to be read. Hence, although aquatic ecology has made considerable progress over the latest century, Forbes might be viewed as one of the major pioneers and visionary scientists of limnology

Causes and consequences of individual variation in anti-predator traits

Predation imposes a potent evolutionary force on prey, moulding the evolution of traits and diversification of species, and can furthermore have powerful ecological consequences. We know that different species vary in how they cope with their natural enemies, and, consequently, a huge range of anti-predator defences are displayed in nature. Yet there is a growing recognition that, if we zoom into a certain species, or even into a single population of animals, there is still a huge and intriguing amount of individual trait variation. In this thesis I investigate what drives individual variation in anti-predator traits, and the implications of this variation for individual animals in two contrasting systems. Specifically, I explore what underlies inter-individual variation in an induced morphological defence in crucian carp and additionally investigate individuality in migratory strategy, risk-taking behaviour and morphology in another common freshwater fish, the roach. I document links between personality-trait variation and anti-predator strategies suggesting that some individuals engage in compensatory strategies to offset some of the costs associated with one trait with the benefits of another. Individuals with a risk-prone personality type (bold individuals) express a greater morphological defence (crucian carp) and are more likely to undertake a winter migration away from predator-rich lakes (roach) as compared to shyer ones. I also show that bold individuals pay a higher predation cost than individuals that adopt a risk-averse behavioural strategy. Furthermore, roach individuals exposed to perceived predation risk (i.e. to a live predator) prior to the migratory period have a higher migration propensity as compared to roach not experiencing experimental predation risk. I also show that variation in migratory timing differs seasonally, and that, at an individual level, survival is strongly linked with the timing of spring but not with autumn migration. Hence, individual variation in the timing of the migratory journey has powerful fitness consequences. Finally, I explore the morphological correlates of migratory behaviour. I show that body morphology is related to migratory life history, as fish from open lakes (with migration opportunity) and migratory individuals from a partially migratory population have more slender, hydrodynamic morphologies as compared to specimens from closed lakes (no migration opportunity) and residents. In summary, my results highlight the powerful role that ecological forces, such as predation, can have in shaping patterns of individual variation in wild populations of animals, and, importantly, that these different behavioural strategies can have profound consequences for survival and thereby individual fitness. Individual variation in survival as a function of phenotype is the raw material upon which natural selection acts, and yet the ecological drivers of evolution remain poorly studied in many wild populations. Working at the individual level in the wild poses significant challenges, but can provide rich insights into the mechanisms of the interplay between ecosystem dynamics and evolutionary processes

Taking turns: some aspects of behavioural lateralization in schooling fish

Lateralization of cognitive functions seems to be exceptionally widespread in nature and have been demonstrated to occur in multiple taxa. Previous studies using fish as models have suggested that social behaviours such as schooling may covary with behavioural lateralization at the population-level. Here, we assess the strength, degree and repeatability of behavioural lateralization in schooling fish. Two of the species studied (Aulorhynchus flavidus and Gasterosteus aculeatus) were found to express population-level symmetry in the direction of lateralization whereas one species (Ammodytes hexapterus) showed no indication of population-level lateralization. We also provide evidence that behavioral lateralization is repeatable over time. From our cross-species comparisons we conclude that population-level lateralization is not necessarily related to a gregarious life-style. Further studies should test repeatability over longer periods of time and the role of lateralization in schooling behavior

Roach partial migration-causes and consequences of individual variation in migratory timing

Patterns of animal migration often vary dramatically within species. Understanding the mechanisms, which shape this variation, is important due to the powerful impacts migratory species can have upon ecosystem processes. Migratory timing is thought to be especially critical for survival and reproductive success and variance in migratory timing has been shown to differ between individuals and seasons across a wide range of taxa. Here we investigate the ecological and evolutionary mechanisms, which drive this commonly observed phenomenon. By individual based tracking of roach, a common migratory freshwater fish, in European lakes over multiple migration periods we obtained highly detailed (year-round scheduling and repeat journeys) information on the migratory patterns of both populations and individuals. Our analyses show that individuals exhibit strong site fidelity and consistency in timing if migration. Furthermore, variation in migratory timing differed seasonally with less variance and more pronounced migration synchrony in spring as compared to autumn. We then show that at an individual level, survival is strongly linked with the timing of spring migration, but not to autumn migration. Hence, natural selection acts to reduce variance in spring migratory timing via survival costs to individuals that deviate from an optimal migratory schedule in spring but not autumn. Our data provides a detailed insight from a longitudinally monitored, wild population into intrapopulation variability in migration strategies and fitness correlates of individual variation in migratory timing

Express yourself: bold individuals induce enhanced morphological defences.

Organisms display an impressive array of defence strategies in nature. Inducible defences (changes in morphology and/or behaviour within a prey's lifetime) allow prey to decrease vulnerability to predators and avoid unnecessary costs of expression. Many studies report considerable interindividual variation in the degree to which inducible defences are expressed, yet what underlies this variation is poorly understood. Here, we show that individuals differing in a key personality trait also differ in the magnitude of morphological defence expression. Crucian carp showing risky behaviours (bold individuals) expressed a significantly greater morphological defence response when exposed to a natural enemy when compared with shy individuals. Furthermore, we show that fish of different personality types differ in their behavioural plasticity, with shy fish exhibiting greater absolute plasticity than bold fish. Our data suggest that individuals with bold personalities may be able to compensate for their risk-prone behavioural type by expressing enhanced morphological defences

Linking behavioural type with cannibalism in Eurasian perch

The propensity to kill and consume conspecifics (cannibalism) varies greatly between and within species, but the underlying mechanisms behind this variation remain poorly understood. A rich literature has documented that consistent behavioural variation is ubiquitous across the animal kingdom. Such inter-individual behavioural differences, sometimes referred to as personality traits, may have far-reaching ecological consequences. However, the link between predator personality traits and the propensity to engage in cannibalistic interactions remains understudied. Here, we first quantified personality in Eurasian perch (Perca fluviatilis), measured as activity (time spent moving) and sociability (time spent near conspecifics). We then gave perch of contrasting behavioural types the option to consume either conspecific or heterospecific (roach, Rutilus rutilus) prey. Individual perch characterized by a social-active behavioural phenotype (n = 5) selected roach before being cannibalistic, while asocial-inactive perch (n = 17) consumed conspecific and heterospecific prey evenly. Thus, asocial-inactive perch expressed significantly higher rates of cannibalism as compared to social-active individuals. Individual variation in cannibalism, linked to behavioural type, adds important mechanistic understanding to complex population and community dynamics, and also provides insight into the diversity and maintenance of animal personality

Experimental manipulation of perceived predation risk and cortisol generates contrasting trait trajectories in plastic crucian carp

Most animals constitute potential prey and must respond appropriately to predator-mediated stress in order to survive. Numerous prey also adaptively tailor their response to the prevailing level of risk and stress imposed by their natural enemies, i.e. they adopt an inducible defence strategy. Predator exposure may activate the stress axis, and drive the expression of anti-predator traits that facilitate survival in a high-risk environment (the predation-stress hypothesis). Here, we quantified two key morphological anti-predator traits, body morphology and coloration, in crucian carp reared in the presence or absence of a predator (pike) in addition to experimental manipulation of physiological stress via implants containing either cortisol or a cortisol inhibitor. We found that predator-exposed fish expressed a deeper-bodied phenotype and darker body coloration as compared with non-exposed individuals. Skin analyses revealed that an increase in the amount of melanophores caused the dramatic colour change in predator-exposed fish. Increased melanization is costly, and the darker body coloration may act as an inducible defence against predation, via a conspicuous signal of the morphological defence or by crypsis towards dark environments and a nocturnal lifestyle. By contrast, the phenotype of individuals carrying cortisol implants did not mirror the phenotype of predator-exposed fish but instead exhibited opposite trajectories of trait change: a shallow-bodied morphology with a lighter body coloration as compared with sham-treated fish. The cortisol inhibitor did not influence the phenotype of fish i.e. neither body depth nor body coloration differed between this group and predator-exposed fish with a sham implant. However, our results illuminate a potential link between stress physiology and morphological defence expression

Data from: Express yourself: bold individuals induce enhanced morphological defences

Organisms display an impressive array of defence strategies in nature. Inducible defences (changes in morphology and/or behaviour within a prey's lifetime) allow prey to decrease vulnerability to predators and avoid unnecessary costs of expression. Many studies report considerable interindividual variation in the degree to which inducible defences are expressed, yet what underlies this variation is poorly understood. Here, we show that individuals differing in a key personality trait also differ in the magnitude of morphological defence expression. Crucian carp showing risky behaviours (bold individuals) expressed a significantly greater morphological defence response when exposed to a natural enemy when compared with shy individuals. Furthermore, we show that fish of different personality types differ in their behavioural plasticity, with shy fish exhibiting greater absolute plasticity than bold fish. Our data suggest that individuals with bold personalities may be able to compensate for their risk-prone behavioural type by expressing enhanced morphological defences

Conspecific boldness and predator species determine predation-risk consequences of prey personality

Abstract: Individual variation in the behavior of prey can influence predation risk in complex ways. We ran individual roach (Rutilus rutilus), a common freshwater fish, through a standard refuge emergence protocol to characterize their boldness, a key animal personality trait. We then paired a bold and a shy roach and exposed the pair to one of two predator species that have contrasting hunting modes to ascertain how personality traits shaped their survival during predator encounters. When a paired bold and shy prey fish interacted with a perch predator (active foraging mode), bold and shy prey were consumed in almost equal numbers. However, pike predators (ambush foraging mode) selectively consumed more shy prey, and prey body size and boldness score both contributed significantly to which prey fish was eaten. Our findings support the idea that multiple predators with different foraging modes, and hence differential selection on prey personality, could contribute to maintaining variation in personality in prey populations. Furthermore, for social species, including shoaling fish, the ultimate consequences of an individual’s personality may depend upon the personality of its nearby conspecifics. Significance statement: Animals of the same species often look similar, but individuals show differences in their behavior that can have important consequences, for instance when these individuals interact with predators. The common roach is a freshwater fish that shows inter-individual variation in its propensity to take risks, a key personality trait often termed boldness. Variation in boldness may affect the outcome when roach interact with predators, i.e., if they get eaten or survive. However, we found the impact of roachs’ personality type depends on what species of predatory fish they face. When we put a shy and a bold roach together with predatory perch, the roachs’ personality did not significantly affect which individual was eaten. But when the predator was a pike, the predators selectively ate more shy roach, and the likelihood an individual would be eaten depended on their body size

Natural and anthropogenic sources of habitat variation influence exploration behaviour, stress response, and brain morphology in a coastal fish

1. Evolutionary ecology aims to better understand how ecologically important traits respond to environmental heterogeneity. Environments vary both naturally and as a result of human activities, and investigations that simultaneously consider how natural and human-induced environmental variation affect diverse trait types grow increasingly important as human activities drive species endangerment. 2. Here, we examine how habitat fragmentation and structural habitat complexity, affect disparate trait types in Bahamas mosquitofish (Gambusia hubbsi) inhabiting tidal creeks. We tested a priori predictions for how these factors might influence exploratory behaviour, stress reactivity, and brain anatomy. 3. We examined approximately 350 adult Bahamas mosquitofish from seven tidal creek populations across Andros Island, The Bahamas that varied in both human-caused fragmentation (three fragmented, four unfragmented) and natural habitat complexity (e.g. 5-fold variation in rock habitat). 4. Populations that had experienced severe human-induced fragmentation, and thus restriction of tidal exchange from the ocean, exhibited greater exploration of a novel environment, stronger physiological stress responses to a mildly stressful event, and smaller telencephala (relative to body size). These changes matched adaptive predictions based mostly on 1) reduced chronic predation risk and 2) decreased demands for navigating tidally dynamic habitats. Populations from sites with greater structural habitat complexity showed a higher propensity for exploration and a relatively larger optic tectum and cerebellum. These patterns matched adaptive predictions related to increased demands for navigating complex environments. 5. Our findings demonstrate environmental variation, including recent anthropogenic impacts (<50 years), can significantly affect complex, ecologically important traits. Yet trait-specific patterns may not be easily predicted, as we found strong support for only six of 12 predictions. Our results further highlight the utility of simultaneously quantifying multiple environmental factors—e.g. had we failed to account for habitat complexity, we would not have detected effects of fragmentation on exploratory behaviours. These responses, and their ecological consequences, may be complex: rapid and adaptive phenotypic responses to anthropogenic impacts can facilitate persistence in human-altered environments, but may come at a cost of population vulnerability if ecological restoration were to occur without consideration of the altered traits.The first sheet of the Excel file provides information for labels/terms. A small number of individuals have missing data for at least one of the three phenotypic categories owing to problems encountered in the field (e.g. video recording error). Funding provided by: North Carolina State UniversityCrossref Funder Registry ID: http://dx.doi.org/10.13039/100007703Award Number: Funding provided by: Helge Ax:son Johnsons StiftelseCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100003788Award Number: Funding provided by: VetenskapsrådetCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100004359Award Number: 2015-00300All methodological details are provided in the article. Briefly, digital videos and photographs were taken in the field and analyzed to quantify exploration behaviour, ventilation frequency, and brain morphology