Ponds as experimental arenas for studying animal movement: current research and future prospects.

Animal movement is a multifaceted process that occurs for multiple reasons with powerful consequences for food web and ecosystem dynamics. New paradigms and technical innovations have recently pervaded the field, providing increasingly powerful means to deliver fine-scale movement data, attracting renewed interest. Specifically in the aquatic environment, tracking with acoustic telemetry now provides integral spatiotemporal information to follow individual movements in the wild. Yet, this technology also holds great promise for experimental studies, enhancing our ability to truly establish cause-and-effect relationships. Here, we argue that ponds with well-defined borders (i.e. "islands in a sea of land") are particularly well suited for this purpose. To support our argument, we also discuss recent experiences from studies conducted in an innovative experimental infrastructure, composed of replicated ponds equipped with modern aquatic telemetry systems that allow for unparalleled insights into the movement patterns of individual animals.

Sex matters: predator presence induces sexual dimorphism in a monomorphic prey, from stress genes to morphological defences.

Inducible defences allow prey to increase survival chances when predators are present while avoiding unnecessary costs in their absence. Many studies report considerable inter-individual variation in inducible defence expression, yet what underlies this variation is poorly understood. A classic vertebrate example of a predator-induced morphological defence is the increased body depth in crucian carp (Carassius carassius), which reduces the risk of predation from gape-size limited predators. Here, we report that among-individual variation in morphological defence expression can be linked to sex. We documented sexual dimorphism in lakes in which crucian carp coexisted with predators, where females showed shallower relative body depths than males, but not in a predator-free lake. When exposing crucian carp from a population without predators to perceived predation risk in a laboratory environment (presence/absence of pike, Esox lucius), we found that males expressed significantly greater morphological defence than females, causing sexual dimorphism only in the presence of predators. We uncovered a correlative link between the sex-specific inducible phenotypic response and gene expression patterns in major stress-related genes (POMC, MC3R, and MC4R). Together, our results highlight that sex-specific responses may be an important, yet underappreciated, component underlying inter-individual differences in the expression of inducible defences, even in species without pronounced sexual dimorphism.

Effects of parasitic freshwater mussels on their host fishes: a review.

Freshwater mussels in the order Unionida are highly adapted to parasitize fish for the primary purpose of dispersal. The parasitic larval stage affixes itself to the gills or fins of the host where it becomes encysted in the tissue, eventually excysting to develop into a free-living adult. Research on the parasitic interactions between unionids and their host fishes has garnered attention recently due to the increase in worldwide preservation efforts surrounding this highly endangered and ecologically significant order. With the exception of heavy infestation events, these mussels cause minor effects to their hosts, typically only observable effect in combination with other stressors. Moreover, the range of effect intensities on the host varies greatly with the species involved in the interaction, an effect that may arise from different evolutionary strategies between long- and short-infesting mussels; a distinction not typically made in conservation practices. Lower growth and reduced osmotic potential in infested hosts are commonly observed and correlated with infestation load. These effects are typically also associated with increases in metabolic rate and behaviour indicative of stress. Host fish seem to compensate for this through a combination of rapid wound healing in the parasitized areas and higher ventilation rates. The findings are heavily biased towards Margaritifera margaritifera, a unique mussel not well suited for cross-species generalizations. Furthermore, the small body of molecular and genetic studies should be expanded as many conclusions are drawn from studies on the ultimate effects of glochidiosis rather than proximate studies on the underlying mechanisms.

Timing and synchrony of migration in a freshwater fish: Consequences for survival.

Animal migration is one of the most spectacular and visible behavioural phenomena in nature with profound implications for a range of ecological and evolutionary processes. Successful migration hinges on the ability to exploit temporary resources (e.g. food) and evade threats (e.g. predators) as they arise, and thus the timing of migration is often regarded as a dominant predictor of individual migratory success. However, with the exception of intensively studied taxa (mainly birds), relatively few studies have investigated inter-individual annual and seasonal variation in migratory timing and performance, or tested predictions on how migration across high and low predation-risk habitats may exert selection on migratory timing. In particular, studies that assess the survival consequences of variation in migratory timing remain rare, which is most likely due to the logistical challenges associated with monitoring survival success and population-level characteristics simultaneously. Here, we address the above-mentioned questions using roach Rutilus rutilus, a fish that migrates from lakes characterised by high predation risk into low-risk streams during winter. Specifically, we used individual-based tracking of roach in two European lake systems over multiple migration periods (9 and 7 years respectively), to obtain highly detailed (year-round scheduling, repeat journeys and the fate of individuals) data on the variability/synchrony of migratory timing in spring and autumn respectively. We report seasonal differences in the variability of migratory timing, with lower variance and higher migration synchrony in spring lake arrival timing as compared to autumn lake departure timing. Furthermore, the timing of autumn migration is more variable across years than the timing of spring migration. Second, we find that later arrival to the lake habitat is positively associated with apparent survival from 1 year to the next, whereas we found no effect of lake departure timing on survival probability. These findings represent rare evidence showing how intraspecific variation in timing in migratory fish differs across years and seasons, and how variation in timing can translate into survival consequences for prey in systems characterised by high predation risk.

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.

Antipredator phenotype in crucian carp altered by a psychoactive drug.

Predator-inducible defenses constitute a widespread form of adaptive phenotypic plasticity, and such defenses have recently been suggested linked with the neuroendocrine system. The neuroendocrine system is a target of endocrine disruptors, such as psychoactive pharmaceuticals, which are common aquatic contaminants. We hypothesized that exposure to an antidepressant pollutant, fluoxetine, influences the physiological stress response in our model species, crucian carp, affecting its behavioral and morphological responses to predation threat. We examined short- and long-term effects of fluoxetine and predator exposure on behavior and morphology in crucian carp. Seventeen days of exposure to a high dose of fluoxetine (100 µg/L) resulted in a shyer phenotype, regardless of the presence/absence of a pike predator, but this effect disappeared after long-term exposure. Fluoxetine effects on morphological plasticity were context-dependent as a low dose (1 µg/L) only influenced crucian carp body shape in pike presence. A high dose of fluoxetine strongly influenced body shape regardless of predator treatment. Our results highlight that environmental pollution by pharmaceuticals could disrupt physiological regulation of ecologically important inducible defenses.

Personality-dependent inter- and intraspecific foraging competition in the invasive round goby, Neogobius melanostomus.

This study examines the impact of boldness on foraging competition of the highly invasive round goby Neogobius melanostomus Pallas 1815. Individual risk tolerance, or boldness, was measured as the time to resume movement after a simulated predation strike. Fish that resumed movement faster were categorized as "bold," fish that took more time to resume movement were categorized as "shy" and those that fell in between these two categories were determined to have "intermediate" boldness. Competitive impacts of boldness in N. melanostomus were determined in a laboratory foraging experiment in which interspecific (juvenile Atlantic cod Gadus morhua Linnaeus 1758) and intraspecific (intermediate N. melanostomus) individuals were exposed to either bold or shy N. melanostomus competitors. G. morhua consumed fewer prey when competing with bold N. melanostomus than when competing with shy N. melanostomus, whereas intermediately bold N. melanostomus foraging was not affected by competitor boldness. Bold and shy N. melanostomus consumed similar amounts of prey, and the number of interactions between paired fish did not vary depending on the personality of N. melanostomus individuals. Therefore, intraspecific foraging competition was not found to be personality dependent. This study provides evidence that individual differences in boldness can mediate competitive interactions in N. melanostomus; nonetheless, results also show that competition is also governed by other mechanisms that require further study.

Substrate-size choice in European eel (Anguilla anguilla) elvers is not altered by piscivore chemical cues.

The European eel Anguilla anguilla Linnaeus 1758 is critically endangered with recruitment estimated at 5-10% of historical levels. Enhancing survival of recruits is pivotal for conservation, and restoration should consider habitat choice of elvers ascending river systems. We experimentally show that newly ascended elvers choose small pebble habitat over finer and larger substrates, regardless of the presence or absence of piscivore chemical cues, indicating no predator-induced change in substrate choice. Enriching habitats with this substrate fraction should enhance eel recruitment as well as biodiversity at large.

A field evaluation of long-term effects of PIT tagging.

Passive integrated transponder (PIT)-tagging is commonly used in behavioural studies of fish, although long-term evaluations of effects from tagging under natural conditions are scarce. We PIT-tagged common bream Abramis brama, European perch Perca fluviatilis, pike Esox lucius and roach Rutilus rutilus, released them in their lakes of origin and recaptured them after 103-3269 days. Overall, tagged fish did not differ in condition from non-tagged fish, except for small R. rutilus that had a lower length-specific body mass in one lake in 1 year. We conclude that PIT-tagging in general has negligible long-term effects on fish condition.

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.

Personality- and size-related metabolic performance in invasive round goby (Neogobius melanostomus).

Differences between individuals in behavioral type (i.e. animal personality) are ecologically and evolutionarily important because they can have significant effects on fitness components such as growth and predation risk. In the present study we are used the invasive round goby (Neogobius melanostomus) from an established population in controlled experiments to examine the relationships among personality, metabolic performance, and growth rate (inferred as size-at-age). Boldness was measured as the time to return to normal behavior after a simulated predator attack, where fish with shorter freezing times were categorized as "bold" and fish with longer times were categorized as "shy." We show that bold fish have significantly higher standard metabolic rate (SMR) than their shy conspecifics, whereas there was no difference between personality types in their maximum metabolic rate (MMR) or aerobic scope (AS). Bold fish furthermore had a smaller size-at-age as compared to shy fish. Together this provides evidence of a metabolic underpinning of personality where the high-SMR bold fish require more resources to sustain basic life functions than their low-SMR shy conspecifics, indicating that bold round goby from established populations with high densities (and high competition for food) pay a price of reduced growth rate.

Low-latitude zooplankton pigmentation plasticity in response to multiple threats.

Crustacean copepods in high-latitude lakes frequently alter their pigmentation facultatively to defend themselves against prevailing threats, such as solar ultraviolet radiation (UVR) and visually oriented predators. Strong seasonality in those environments promotes phenotypic plasticity. To date, no one has investigated whether low-latitude copepods, experiencing continuous stress from UVR and predation threats, exhibit similar inducible defences. We here investigated the pigmentation levels of Bahamian 'blue hole' copepods, addressing this deficit. Examining several populations varying in predation risk, we found the lowest levels of pigmentation in the population experiencing the highest predation pressure. In a laboratory experiment, we found that, in contrast with our predictions, copepods from these relatively constant environments did show some changes in pigmentation subsequent to the removal of UVR; however, exposure to water from different predation regimes induced minor and idiosyncratic pigmentation change. Our findings suggest that low-latitude zooplankton in inland environments may exhibit reduced, but non-zero, levels of phenotypic plasticity compared with their high-latitude counterparts.

Species integrity enhanced by a predation cost to hybrids in the wild.

Species integrity can be challenged, and even eroded, if closely related species can hybridize and produce fertile offspring of comparable fitness to that of parental species. The maintenance of newly diverged or closely related species therefore hinges on the establishment and effectiveness of pre- and/or post-zygotic reproductive barriers. Ecological selection, including predation, is often presumed to contribute to reduced hybrid fitness, but field evidence for a predation cost to hybridization remains elusive. Here we provide proof-of-concept for predation on hybrids being a postzygotic barrier to gene flow in the wild. Cyprinid fishes commonly produce fertile, viable hybrid offspring and therefore make excellent study organisms to investigate ecological costs to hybrids. We electronically tagged two freshwater cyprinid fish species (roach Rutilus rutilus and bream Abramis brama) and their hybrids in 2005. Tagged fish were returned to their lake of origin, exposing them to natural predation risk from apex avian predators (great cormorant, Phalacrocorax carbo). Scanning for regurgitated tags under cormorant roosts 3-4 years later identified cormorant-killed individual fish and allowed us to directly test for a predation cost to hybrids in the wild. Hybrid individuals were found significantly more susceptible to cormorant predation than individuals from either parental species. Such ecological selection against hybrids contributes to species integrity, and can enhance species diversification.

A predation cost to bold fish in the wild.

Studies of predator-mediated selection on behaviour are critical for our understanding of the evolution and maintenance of behavioural diversity in natural populations. Consistent individual differences in prey behaviour, especially in the propensity to take risks ("boldness"), are widespread in the animal kingdom. Theory predicts that individual behavioural types differ in a cost-benefit trade-off where bolder individuals benefit from greater access to resources while paying higher predation-risk costs. However, explicitly linking predation events to individual behaviour under natural conditions is challenging and there is currently little data from the wild. We assayed individual behaviour and electronically tagged hundreds of fish (roach, Rutilus rutilus) before releasing them into their lake of origin, thereby exposing them to predation risk from avian apex predators (cormorants, Phalacrocorax carbo). Scanning for regurgitated tags at the cormorant roosting site provided data on individual predation events. We found that fish with higher boldness have a greater susceptibility to cormorant predation compared to relatively shy, risk-averse individuals. Our findings hereby provide unique and direct evidence of behavioural type-dependent predation vulnerability in the wild, i.e. that there is a predation cost to boldness, which is critical for our understanding of the evolution and maintenance of behavioural diversity in natural populations.

Marine ecosystem connectivity mediated by migrant-resident interactions and the concomitant cross-system flux of lipids.

Accumulating research argues that migrants influence the functioning and productivity of local habitats and ecosystems along migration routes and potentially drive cross-system energy fluxes of considerable magnitude, yet empirical documentation of local ecological effects and descriptions of the underlying mechanisms are surprisingly rare. In this study, we discovered migrant-resident interactions and substantial cross-system lipid transportation in the transition zone between the Baltic Sea and the North Sea where a resident cod population (predators) was found to interact with a herring population (prey) on a seasonal basis. We traced the lipids, using fatty acid trophic markers (FATM), from the herring feeding grounds in the North Sea to the cod livers in the Western Baltic Sea. Time series analysis of population dynamics indicated that population-level production of cod is positively affected by the herring subsidies. However, the underlying mechanisms were more complicated than anticipated. During the herring season, large cod received most of its dietary lipids from the herring, whereas smaller cod were prevented from accessing the lipid pool due to a mismatch in predator-prey size ratio. Furthermore, while the herring were extremely rich in bulk energy, they were surprisingly poor in a specific functional fatty acid. Hence, our study was the first to illustrate how the magnitude cross-system fluxes of subsidies in migrant-resident systems are potentially constrained by the size structure of the resident predator population and the nutritional quality of the migrants.

Escaping peril: perceived predation risk affects migratory propensity.

Although migratory plasticity is increasingly documented, the ecological drivers of plasticity are not well understood. Predation risk can influence migratory dynamics, but whether seasonal migrants can adjust their migratory behaviour according to perceived risk is unknown. We used electronic tags to record the migration of individual roach (Rutilus rutilus), a partially migratory fish, in the wild following exposure to manipulation of direct (predator presence/absence) and indirect (high/low roach density) perceived predation risk in experimental mesocosms. Following exposure, we released fish in their lake summer habitat and monitored individual migration to connected streams over an entire season. Individuals exposed to increased perceived direct predation risk (i.e. a live predator) showed a higher migratory propensity but no change in migratory timing, while indirect risk (i.e. roach density) affected timing but not propensity showing that elevated risk carried over to alter migratory behaviour in the wild. Our key finding demonstrates predator-driven migratory plasticity, highlighting the powerful role of predation risk for migratory decision-making and dynamics.

Individual boldness is linked to protective shell shape in aquatic snails.

The existence of consistent individual differences in behaviour ('animal personality') has been well documented in recent years. However, how such individual variation in behaviour is maintained over evolutionary time is an ongoing conundrum. A well-studied axis of animal personality is individual variation along a bold-shy continuum, where individuals differ consistently in their propensity to take risks. A predation-risk cost to boldness is often assumed, but also that the reproductive benefits associated with boldness lead to equivalent fitness outcomes between bold and shy individuals over a lifetime. However, an alternative or complementary explanation may be that bold individuals phenotypically compensate for their risky lifestyle to reduce predation costs, for instance by investing in more pronounced morphological defences. Here, we investigate the 'phenotypic compensation' hypothesis, i.e. that bold individuals exhibit more pronounced anti-predator defences than shy individuals, by relating shell shape in the aquatic snail Radix balthica to an index of individual boldness. Our analyses find a strong relationship between risk-taking propensity and shell shape in this species, with bolder individuals exhibiting a more defended shell shape than shy individuals. We suggest that this supports the 'phenotypic compensation' hypothesis and sheds light on a previously poorly studied mechanism to promote the maintenance of personality variation among animals.

Shape up or ship out: migratory behaviour predicts morphology across spatial scale in a freshwater fish.

1. Migration is a widespread phenomenon, with powerful ecological and evolutionary consequences. Morphological adaptations to reduce the energetic costs associated with migratory transport are commonly documented for migratory species. However, few studies have investigated whether variation in body morphology can be explained by variation in migratory strategy within a species. 2. We address this question in roach Rutilus rutilus, a partially migratory freshwater fish that migrates from lakes into streams during winter. We both compare body shape between populations that differ in migratory opportunity (open vs. closed lakes), and between individuals from a single population that vary in migratory propensity (migrants and residents from a partially migratory population). Following hydrodynamic theory, we posit that migrants should have a more shallow body depth, to reduce the costs associated with migrating into streams with higher flow conditions than the lakes the residents occupy all year round. 3. We find evidence both across and within populations to support our prediction, with individuals from open lakes and migrants from the partially migratory population having a more slender, shallow-bodied morphology than fish from closed lakes and all-year residents. 4. Our data suggest that a shallow body morphology is beneficial to migratory individuals and our study is one of the first to link migratory strategy and intraspecific variation in body shape.

Piscivore-prey fish interactions: mechanisms behind diurnal patterns in prey selectivity in brown and clear water.

Environmental change may affect predator-prey interactions in lakes through deterioration of visual conditions affecting foraging success of visually oriented predators. Environmental change in lakes includes an increase in humic matter causing browner water and reduced visibility, affecting the behavioural performance of both piscivores and prey. We studied diurnal patterns of prey selection in piscivorous pikeperch (Sander lucioperca) in both field and laboratory investigations. In the field we estimated prey selectivity and prey availability during day and night in a clear and a brown water lake. Further, prey selectivity during day and night conditions was studied in the laboratory where we manipulated optical conditions (humic matter content) of the water. Here, we also studied the behaviours of piscivores and prey, focusing on foraging-cycle stages such as number of interests and attacks by the pikeperch as well as the escape distance of the prey fish species. Analyses of gut contents from the field study showed that pikeperch selected perch (Perca fluviatilis) over roach (Rutilus rutilus) prey in both lakes during the day, but changed selectivity towards roach in both lakes at night. These results were corroborated in the selectivity experiments along a brown-water gradient in day and night light conditions. However, a change in selectivity from perch to roach was observed when the optical condition was heavily degraded, from either brown-stained water or light intensity. At longer visual ranges, roach initiated escape at distances greater than pikeperch attack distances, whereas perch stayed inactive making pikeperch approach and attack at the closest range possible. Roach anti-predatory behaviour decreased in deteriorated visual conditions, altering selectivity patterns. Our results highlight the importance of investigating both predator and prey responses to visibility conditions in order to understand the effects of degrading optical conditions on piscivore-prey interaction strength and thereby ecosystem responses to brownification of waters.

Fixed and flexible: coexistence of obligate and facultative migratory strategies in a freshwater fish.

Migration is an important event in many animal life histories, but the degree to which individual animals participate in seasonal migrations often varies within populations. The powerful ecological and evolutionary consequences of such partial migration are now well documented, but the underlying mechanisms are still heavily debated. One potential mechanism of partial migration is between-individual variation in body condition, where animals in poor condition cannot pay the costs of migration and hence adopt a resident strategy. However, underlying intrinsic traits may overrule such environmental influence, dictating individual consistency in migratory patterns. Unfortunately, field tests of individual consistency compared to the importance of individual condition on migratory propensity are rare. Here we analyse 6 years of field data on roach migration, gathered by tagging almost 3000 individual fish and monitoring their seasonal migrations over extended periods of time. Our aims were to provide a field test of the role of condition in wild fish for migratory decisions, and also to assess individual consistency in migratory tendency. Our analyses reveal that (1) migratory strategy, in terms of migration/residency, is highly consistent within individuals over time and (2) there is a positive relationship between condition and the probability of migration, but only in individuals that adopt a migratory strategy at some point during their lives. However, life-long residents do not differ in condition to migrants, hence body condition is only a good predictor of migratory tendency in fish with migratory phenotypes and not a more general determinant of migratory tendency for the population. As resident individuals can achieve very high body condition and still remain resident, we suggest that our data provides some of the first field evidence to show that both facultative and obligate strategies can co-exist within populations of migratory animals.