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.

Maladaptive migration behaviour in hybrids links to predator-mediated ecological selection.

Different migratory species have evolved distinct migratory characteristics that improve fitness in their particular ecological niches. However, when such species hybridize, migratory traits from parental species can combine maladaptively and cause hybrids to fall between parental fitness peaks, with potential consequences for hybrid viability and species integrity. Here, we take advantage of a natural cross-breeding incident to study migratory behaviour in naturally occurring hybrids as well as in their parental species and explore links between migratory traits and predation risk. To achieve this, we used electronic tags and passive telemetry to record detailed individual migration patterns (timing and number of migratory trips) in two common freshwater fish species, roach Rutilus rutilus, common bream Abramis brama as well as their hybrids. Next, we scanned for tags regurgitated by a key avian predator (great cormorant Phalacrocorax carbo) at nearby roosting sites, allowing us to directly link migratory behaviour to predation risk in the wild. We found that hybrid individuals showed a higher number of short, multi-trip movements between lake and stream habitats as compared to both parental species. The mean date of first lake departure differed between bream and roach by more than 10 days, while hybrids departed in two distinct peaks that overlapped with the parental species' averages. Moreover, the probability of cormorant predation increased with multi-trip movement frequency across species and was higher for hybrids. Our data provide novel insights into hybrid viability, with links to predator-mediated ecological selection. Increased exposure to predators via maladaptive migratory behaviour reduces hybrid survival and can thereby reinforce species integrity.

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.

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.

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.

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.

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.

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.

Migration confers survival benefits against avian predators for partially migratory freshwater fish.

The importance of predation risk in shaping patterns of animal migration is not well studied, mostly owing to difficulties in accurately quantifying predation risk for migratory versus resident individuals. Here, we present data from an extensive field study, which shows that migration in a freshwater fish (roach, Rutilus rutilus) that commonly migrates from lakes to streams during winter confers a significant survival benefit with respect to bird (cormorant, Phalacrocorax carbo spp.) predation. We tagged over 2000 individual fish in two Scandinavian lakes over 4 years and monitored migratory behaviour using passive telemetry. Next, we calculated the predation vulnerability of fish with differing migration strategies, by recovering data from passive integrated transponder tags of fish eaten by cormorants at communal roosts close to the lakes. We show that fish can reduce their predation risk from cormorants by migrating into streams, and that probability of being preyed upon by cormorants is positively related to the time individuals spend in the lake during winter. Our data add to the growing body of evidence that highlights the importance of predation for migratory dynamics, and, to our knowledge, is one of the first studies to directly quantify a predator avoidance benefit to migrants in the field.

Variable individual consistency in timing and destination of winter migrating fish.

Migration is an important event in the life history of many animals, but there is considerable variation within populations in the timing and final destination. Such differential migration at the population level can be strongly determined by individuals showing different consistencies in migratory traits. By tagging individual cyprinid fish with uniquely coded electronic tags, and recording their winter migrations from lakes to streams for 6 consecutive years, we obtained highly detailed long-term information on the differential migration patterns of individuals. We found that individual migrants showed consistent site fidelities for over-wintering streams over multiple migratory seasons and that they were also consistent in their seasonal timing of migration. Our data also suggest that consistency itself can be considered as an individual trait, with migrants that exhibit consistent site fidelity also showing consistency in migratory timing. The finding of a mixture of both consistent and inconsistent individuals within a population furthers our understanding of intrapopulation variability in migration strategies, and we hypothesize that environmental variation can maintain such different strategies.

To boldly go: individual differences in boldness influence migratory tendency.

Partial migration, whereby only a fraction of the population migrates, is thought to be the most common type of migration in the animal kingdom, and can have important ecological and evolutionary consequences. Despite this, the factors that influence which individuals migrate and which remain resident are poorly understood. Recent work has shown that consistent individual differences in personality traits in animals can be ecologically important, but field studies integrating personality traits with migratory behaviour are extremely rare. In this study, we investigate the influence of individual boldness, an important personality trait, upon the migratory propensity of roach, a freshwater fish, over two consecutive migration seasons. We assay and individually tag 460 roach and show that boldness influences migratory propensity, with bold individuals being more likely to migrate than shy fish. Our data suggest that an extremely widespread personality trait in animals can have significant ecological consequences via influencing individual-level migratory behaviour.

Sizing up your enemy: individual predation vulnerability predicts migratory probability.

Partial migration, in which a fraction of a population migrate and the rest remain resident, occurs in an extensive range of species and can have powerful ecological consequences. The question of what drives differences in individual migratory tendency is a contentious one. It has been shown that the timing of partial migration is based upon a trade-off between seasonal fluctuations in predation risk and growth potential. Phenotypic variation in either individual predation risk or growth potential should thus mediate the strength of the trade-off and ultimately predict patterns of partial migration at the individual level (i.e. which individuals migrate and which remain resident). We provide cross-population empirical support for the importance of one component of this model--individual predation risk--in predicting partial migration in wild populations of bream Abramis brama, a freshwater fish. Smaller, high-risk individuals migrate with a higher probability than larger, low-risk individuals, and we suggest that predation risk maintains size-dependent partial migration in this system.

Behavioural consequences of sensory plasticity in guppies.

Sensory plasticity, whereby individuals compensate for sensory deprivation in one sense by an improvement in the performance of an alternative sense, is a well-documented phenomenon in nature. Despite this, the behavioural and ecological consequences of sensory plasticity have not been addressed. Here we show experimentally that some components (vision and chemoreception) of the sensory system of guppies are developmentally plastic, and that this plasticity has important consequences for foraging behaviour. Guppies reared under low light conditions had a significantly stronger response to chemical food cues encountered in isolation than fish reared at higher light levels. Conversely, they exhibited a weaker response to visual-only cues. When visual and olfactory/gustatory cues were presented together, no difference between the strength of response for fish reared at different light intensities was evident. Our data suggest that guppies can compensate for experience of a visually poor, low light environment via a sensory switch from vision to olfaction/gustation. This switch from sight to chemoreception may allow individuals to carry out the foraging behaviour that is essential to their survival in a visually poor environment. These considerations are especially important given the increasing frequency of anthropogenic changes to ecosystems. Compensatory phenotypic plasticity as demonstrated by our study may provide a hitherto unconsidered buffer that could allow animals to perform fundamental behaviours in the face of considerable change to the sensory environment.

A novel terrestrial fish habitat inside emergent logs.

Reports of new habitats for a major group of organisms are rare. Fishes display diverse adaptations for temporary (amphibious) existence on land, but to our knowledge, none have ever been reported regularly living inside emergent logs. Here, we show that the mangrove killifish, Kryptolebias marmoratus, a species previously known to emerse (leave the water) regularly, is now known to emerse and aggregate in large numbers inside decaying mangrove logs that have been "galleried" by terrestrial insects. This behavior has now been documented in both Belize, Central America, and Florida, U.S.A., populations and represents the first known case of fishes entering terrestrial woody material. The dense packing of fish in the narrow log galleries may imply a novel social context in which intraspecific aggressive behaviors are reduced, possibly mediated by the physiological limitations imposed within this restrictive habitat.

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.

Predation risk as a driving force for sexual segregation: a cross-population comparison.

Sexual segregation is widespread throughout the animal kingdom. Although a number of hypotheses have been proposed to account for observed patterns, the generality of the mechanisms remains debated. One possible reason for this is the focus on segregation patterns in large mammals such as ungulates, where the majority of studies are descriptions of a single population. Here, we present the results of a cross­population comparison of patterns of sexual segregation in the Trinidadian guppy, Poecilia reticulata. We relate observed patterns to experimental quantification of predation risk and sexual harassment of females by males in eight populations. We find that the degree of segregation increases with predation risk, with deeper waters becoming increasingly female biased. Furthermore, we observed that levels of male harassment are lower in deeper water but only in those rivers that contain major guppy predators. We conclude that sexual segregation in guppies is consistent with the predation risk hypothesis: sexual segregation results from a combination of predation risk driving males (the more vulnerable sex) into less risky habitats and females gaining benefits of reduced sexual harassment by remaining in high­predation environments.

Different behaviour-body length correlations in two populations of juvenile three-spined stickleback (Gasterosteus aculeatus).

Behavioural variation among individuals has received a lot of attention by behavioural ecologists in the past few years. Its causes and consequences are becoming vast areas of research. The origin and maintenance of individual variation in behaviour within and among populations is affected by many facets of the biotic and abiotic environment. Here, two populations of lab-reared juvenile three-spined sticklebacks (Gasterosteus aculeatus) are tested for three behaviours (boldness, exploration, and sociability). Given the identical rearing conditions, the only difference between these populations is the parental habitat. In both populations, correlations between behaviour and body length are found. Interestingly, these differ between the populations. In one population body length was negatively correlated with exploratory behaviour, while in the other one body length correlated negatively with sociability. Considering the identical environment these juvenile fish were exposed to, these findings suggest a potential (epi)genetic foundation for these correlations and shows that, in three-spined sticklebacks, the proximate basis for correlations between body length and behaviour appears quite malleable.

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.

Sex and the syndrome: individual and population consistency in behaviour in rock pool prawn Palaemon elegans.

Animal personality has been widely documented across a range of species. The concept of personality is composed of individual behavioural consistency across time and between situations, and also behavioural trait correlations known as behavioural syndromes. Whilst many studies have now investigated the stability of individual personality traits, few have analysed the stability over time of entire behavioural syndromes. Here we present data from a behavioural study of rock pool prawns. We show that prawns are temporally consistent in a range of behaviours, including activity, exploration and boldness, and also that a behavioural syndrome is evident in this population. We find correlations between many behavioural traits (activity, boldness, shoaling and exploration). In addition, behavioural syndrome structure was consistent over time. Finally, few studies have explicitly studied the role of sex differences in personality traits, behavioural consistency and syndrome structure. We report behavioural differences between male and female prawns but no differences in patterns of consistency. Our study adds to the growing literature on animal personality, and provides evidence showing that syndromes themselves can exhibit temporal consistency.

A foraging cost of migration for a partially migratory cyprinid fish.

Migration has evolved as a strategy to maximise individual fitness in response to seasonally changing ecological and environmental conditions. However, migration can also incur costs, and quantifying these costs can provide important clues to the ultimate ecological forces that underpin migratory behaviour. A key emerging model to explain migration in many systems posits that migration is driven by seasonal changes to a predation/growth potential (p/g) trade-off that a wide range of animals face. In this study we assess a key assumption of this model for a common cyprinid partial migrant, the roach Rutilus rutilus, which migrates from shallow lakes to streams during winter. By sampling fish from stream and lake habitats in the autumn and spring and measuring their stomach fullness and diet composition, we tested if migrating roach pay a cost of reduced foraging when migrating. Resident fish had fuller stomachs containing more high quality prey items than migrant fish. Hence, we document a feeding cost to migration in roach, which adds additional support for the validity of the p/g model of migration in freshwater systems.