Size-selective mortality fosters ontogenetic changes in collective risk-taking behaviour in zebrafish, Danio rerio

Size-selective mortality is common in fish populations and can operate either in a positive size-selective fashion or be negatively size-selective. Through various mechanisms (like genetic correlations among behaviour and life-history traits or direct selection on behaviour co-varying with growth rate or size-at-maturation), both positive- and negative size-selection can result in evolutionary changes in behavioural traits. Theory suggests that size-selection alone favours boldness, but little experimental evidence exists about whether and to what extent size-selection can trigger its evolution. Here we investigated the impact of size-selective mortality on boldness across ontogeny using three experimental lines of zebrafish (Danio rerio) generated through positive (large-harvested), negative (small-harvested) and random (control line) size-selective mortality for five generations. We measured risk-taking during feeding (boldness) under simulated aerial predation threat and in presence of a live cichlid. We found that boldness decreased with ontogenetic age under aerial predation threat, and the small-harvested line was consistently bolder than controls. Collective personality emerged post larval stages among the selection lines. In presence of a cichlid, the large-harvested line was bolder at the highest risk of predation. The large-harvested line showed higher variability and plasticity in boldness across life stages and predation risks. Collectively, our results demonstrate that size-selective harvesting may evolutionarily alter risk-taking tendency. Size-selection alone favours boldness when selection acts on small fish. Selection typical of fisheries operating on large fish favours boldness at the highest risk of predation and increases behavioural variability and plasticity. There was no evidence for positive size-selection favouring evolution of shyness.

Reactive anti-predator behavioral strategy shaped by predator characteristics

Large mammalian herbivores use a diverse array of strategies to survive predator encounters including flight, grouping, vigilance, warning signals, and fitness indicators. While anti-predator strategies appear to be driven by specific predator traits, no prior studies have rigorously evaluated whether predator hunting characteristics predict reactive anti-predator responses. We experimentally investigated behavioral decisions made by free-ranging impala, wildebeest, and zebra during encounters with model predators with different functional traits. We hypothesized that the choice of response would be driven by a predator’s hunting style (i.e., ambush vs. coursing) while the intensity at which the behavior was performed would correlate with predator traits that contribute to the prey’s relative risk (i.e., each predator’s prey preference, prey-specific capture success, and local predator density). We found that the choice and intensity of anti-predator behaviors were both shaped by hunting style and relative risk factors. All prey species directed longer periods of vigilance towards predators with higher capture success. The decision to flee was the only behavior choice driven by predator characteristics (capture success and hunting style) while intensity of vigilance, frequency of alarm-calling, and flight latency were modulated based on predator hunting strategy and relative risk level. Impala regulated only the intensity of their behaviors, while zebra and wildebeest changed both type and intensity of response based on predator traits. Zebra and impala reacted to multiple components of predation threat, while wildebeest responded solely to capture success. Overall, our findings suggest that certain behaviors potentially facilitate survival under specific contexts and that prey responses may reflect the perceived level of predation risk, suggesting that adaptive functions to reactive anti-predator behaviors may reflect potential trade-offs to their use. The strong influence of prey species identity and social and environmental context suggest that these factors may interact with predator traits to determine the optimal response to immediate predation threat.

Acoustic and visual adaptations to predation risk: A predator affects communication in vocal female fish

Predation is an important ecological constraint that influences communication in animals. Fish respond to predators by adjusting their visual signalling behaviour, but the responses in calling behaviour in the presence of a visually detected predator are largely unknown. We hypothesize that fish will reduce visual and acoustic signalling including sound levels and avoid escalating fights in the presence of a predator. To test this we investigated dyadic contests in female croaking gouramis (Trichopsis vittata, Osphronemidae) in the presence and absence of a predator (Astronotus ocellatus, Cichlidae) in an adjoining tank. Agonistic behaviour in T. vittata consists of lateral (visual) displays, antiparallel circling and production of croaking sounds and may escalate to frontal displays. We analysed the number and duration of lateral display bouts, the number, duration, sound pressure level and dominant frequency of croaking sounds as well as contest outcomes. The number and duration of lateral displays decreased significantly in predator as compared to no-predator trials. Total number of sounds per contest dropped in parallel but no significant changes were observed in sound characteristics. In the presence of a predator dyadic contests were decided or terminated during lateral displays and never escalated to frontal displays. The gouramis showed approaching behaviour towards the predator between lateral displays. This is the first study supporting the hypothesis that predators reduce visual and acoustic signalling in a vocal fish. Sound properties, in contrast, did not change. Decreased signalling and the lack of escalating contests reduce the fish’s conspicuousness and thus predation threat.

Long-term Exposure to Predation Threat Can Modulate the Expression of Sexually Selected Traits in Male Guppy (Poecilia reticulata)

The expression of sexual traits can be affected by different environmental factors among which predation may be particularly important life-history traits. This study investigated the effects of predation risk on courtship behavior, growth and sexual color patterns in male guppy (Poecilia reticulata). In the study, juvenile male guppies were randomly assigned to two treatments, namely T1 (predation threat) and T2 (no predation threat). The courtship performances were visually observed and recorded, while color patterns and morphological traits were measured by using the ImageJ software from the captured photos. The courtship behavioral trials revealed that predation threatened males performed significantly lower number of sigmoid displays than those of no-predation group. Further, the predation scared group had significantly shorter standard length, body area and a reduced number and area of orange spots than their counter group. However, the predation threat did not affect significantly the gonopodial thrusts, and black and iridescent color components (spot number and area). The reduction of costly traits (e.g. behavior, color patterns and body size) is common anti-predator response which presumably reduces predation risks. Male guppies are probably using this form of defence in response to the increased predation risk. The overall result suggests that growth and sexually selected trait expression are sensitive to predation risk and thereby aid in our understanding to predict the evolution of phenotypic variation in natural systems.

Social partner cooperativeness influences brain oxytocin transcription in Trinidadian guppies (Poecilia reticulata)

For non-kin cooperation to be maintained, individuals need to respond adaptively to the cooperative behaviour of their social partners. Currently, however, little is known about the biological responses of individuals to experiencing cooperation. Here, we quantify the neuroregulatory response of Trinidadian guppies (Poecilia reticulata) experiencing cooperation or defection by examining the transcriptional response of the oxytocin gene (oxt; also known as isotocin), which has been implicated in cooperative decision-making. We exposed wild-caught females to social environments where partners either cooperated or defected during predator inspection, or to a control (non-predator inspection) context, and quantified the relative transcription of the oxt gene. We tested an experimental group, originating from a site where individuals are under high predation threat and have previous experience of large aquatic predators (HP), and a control group, where individuals are under low predation threat and naïve to large aquatic predators (LP). In HP, but not LP, fish brain mid-section oxt relative transcription varied depending on social partner behaviour. HP fish experiencing cooperation during predator inspection had lower oxt transcription than those experiencing defection. This effect was not present in the control population or in the control context, where the behaviour of social partners did not affect oxt transcription. Our findings provide insight into the neuromodulation underpinning behavioural responses to social experiences, and ultimately to the proximate mechanisms underlying social decision-making.

Antipredatory Responses of Mosquito Pupae to Non-Lethal Predation Threat—Behavioral Plasticity Across Life-History Stages

Antipredatory behavioral responses tend to be energetically expensive, and prey species thus need to resolve trade-offs between these behaviors and other activities such as foraging and mating. While these trade-offs have been well-studied across taxa, less is known about how costs and benefits vary in different life-history contexts, and associated consequences. To address this question, we compared responses of the yellow fever mosquito (Aedes aegypti [Diptera: Culicidae]) to predation threat from guppy (Poecilia reticulata [Cyprinodontiformes: Poeciliidae]) across two life-history stages—larvae (data from previous study) and pupae (from this study). Pupae are motile but do not feed and are comparable to larvae in terms of behavior. To understand how physiological costs affect the threat sensitivity of pupae, we used sex (with size as a covariate) as a proxy for stored energy reserves, and quantified movement and space use patterns of male (small-sized) and female (large-sized) pupae when exposed to predation threat. We found that pupae did not alter movement when exposed to predator cues but instead altered spatial use by spending more time at the bottom of the water column. We found no effect of pupa sex (or size) on the behavioral responses we measured. We conclude that pupa behavior, both antipredatory and otherwise, is primarily targeted at minimizing energy expenditure, as compared with larval behavior, which appears to balance energy expenditure between the opposing pressures of foraging and of avoiding predation. We suggest that antipredatory defenses in metamorphosing prey are modulated by varying energetic trade-offs associated with different life-history stages.