Predation environment affects boldness temperament of neotropical livebearers

Behavioral traits of individuals are important phenotypes that potentially interact with many other traits, an understanding of which may illuminate the evolutionary forces affecting populations and species. Among the five axes of temperament is the propensity to behave boldly in the presence of a perceived risk. To determine the effect of different predatorial regimes on boldness and fearfulness, we assessed the behavior of individuals in a novel portable swim chamber (i.e., forced open‐field test) by Brachyrhaphis rhabdophora (n = 633). We used an information theoretic framework to compare generalized (logistic) linear fixed‐effects models of predatorial regime (predator‐free [n = 6] and predator [n = 4] sites), sex, and standard length (SL). Fish from predator sites were much more fearful in the novel arena than fish from nonpredator sites. This varied by length, but not by sex. At 48 mm SL, fish from nonpredator sites were 4.9 times more likely to express bold behavior (ambulation) in the novel swim chamber as fish from predator sites. Probabilities of “ambulating” within the swim chamber increased with size for nonpredator sites and decreased with size for predator sites.     

Evolutionary dynamics of fearfulness and boldness

A negative relationship between reproductive effort and survival is consistent with life-history. Evolutionary dynamics and evolutionarily stable strategy (ESS) for the trade-off between survival and reproduction are investigated using a simple model with two phenotypes, fearfulness and boldness. The dynamical stability of the pure strategy model and analysis of ESS conditions reveal that: (i) the simple coexistence of fearfulness and boldness is impossible; (ii) a small population size is favorable to fearfulness, but a large population size is favorable to boldness, i.e., neither fearfulness, nor boldness is always favored by natural selection; and (iii) the dynamics of population density is crucial for a proper understanding of the strategy dynamics.     

Game theory and the evolution of fearfulness in wild birds

When animals in a group live under predation threat, the fate of each individual depends on the way it reacts to danger, but also on the behaviour of its companions. Game theory should then help to understand the evolution of fearful behaviour in gregarious animals. To illustrate this approach, a model determines evolutionarily stable levels of fearfulness in bird flocks, assuming that flocks are the object of both predatory attacks and nonlethal disturbance. In the model, high levels of flightiness limit the risk of being killed by predators, but increase the amount of energy lost in flights during the season. The predicted levels of fearfulness are extremely variable. They depend on the respective frequencies of predatory attacks and simple disturbing events, and on the capacity of birds to detect and escape predators. These results may help to explain the variability of flightiness reported in birds.     

Picking personalities apart: estimating the influence of predation,sex and body size on boldness in the guppy Poecilia reticulata

Predation is a strong selective force in most natural systems, potentially fueling evolutionary changes in prey morphology, life history and behaviour. Recent work has suggested that contrasting predation pressures may lead to population differentiation in personality traits. However, there are indications that these personality traits also differ between sexes and not necessarily in a consistent way between populations. We used an integrative approach to quantify boldness (latency to emerge from a shelter) in wild‐caught guppies in relation to predation pressure, population origin, sex and size. In addition we quantified the repeatability of these personality traits. We show that predation regime had significant effects on emergence time. In general, fish from high predation localities emerged sooner from the shelter compared to those from low predation localities. We found strong sex differences; males were significantly bolder than females. The relationship between emergence time and body size was non‐significant in all populations. We discuss what responses to expect from predator‐naïve versus predator‐experienced individuals and how this can be linked to the shyness–boldness continuum.     

Plasticity of boldness in rainbow trout,Oncorhynchus mykiss: do hunger and predation influence risk-taking behaviour?

Boldness, a measure of an individual's propensity for taking risks, is an important determinant of fitness but is not necessarily a fixed trait. Dependent upon an individual's state, and given certain contexts or challenges, individuals may be able to alter their inclination to be bold or shy in response. Furthermore, the degree to which individuals can modulate their behaviour has been linked with physiological responses to stress. Here we attempted to determine whether bold and shy rainbow trout, Oncorhynchus mykiss, can exhibit behavioural plasticity in response to changes in state (nutritional availability) and context (predation threat). Individual trout were initially assessed for boldness using a standard novel object paradigm; subsequently, each day for one week fish experienced either predictable, unpredictable, or no simulated predator threat in combination with a high (2% body weight) or low (0.15%) food ration, before being reassessed for boldness. Bold trout were generally more plastic, altering levels of neophobia and activity relevant to the challenge, whereas shy trout were more fixed and remained shy. Increased predation risk generally resulted in an increase in the expression of three candidate genes linked to boldness, appetite regulation and physiological stress responses - ependymin, corticotrophin releasing factor and GABA(A) - but did not produce a significant increase in plasma cortisol. The results suggest a divergence in the ability of bold and shy trout to alter their behavioural profiles in response to internal and exogenous factors, and have important implications for our understanding of the maintenance of different behavioural phenotypes in natural populations.     

Predator-induced natural selection on temperament in bighorn ewes

Temperament traits in animals may have important fitness consequences, but have received little attention from ecologists or evolutionary biologists. A few studies have linked variation in temperament with fitness, but none has measured selection on temperament traits. We estimated the strength of selection on female boldness and docility on bighorn sheep ewes, Ovis canadensis. The Ram Mountain population experienced little predation pressure during the first 25 years of study, then 2 years (1997 and 1998) of frequent predation by cougars, Puma concolor, during which adult ewe mortality almost tripled over the long-term average, to 27% a year. During years of high predation, we found moderate selection favouring bold ewes, and age-specific selection on docility. Old ewes appeared more vulnerable to predation than young ewes. In contrast, no evidence of selection on temperament traits was observed during 2 years of low predation (1996 and 1999). These results suggest predator-induced selection favouring bold and nondocile ewes. Leadership was highly correlated with age and may increase the risk of predator encounter. Leadership alone, however, could not explain the higher vulnerability of old ewes to predation. Cougar predation on bighorn sheep occurs sporadically and unpredictably, probably because individual cougars often are prey specialists. Cougar predation may have limited microevolutionary effects on temperament in bighorn sheep, because it mostly affects ewes near the end of their reproductive life span and because of potential countervailing selection on boldness and docility. Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Conditions for the spread of conspicuous warning signals: a numerical model with novel insights

The initial evolution of conspicuous warning signals presents an evolutionary problem because selection against rare conspicuous signals is presumed to be strong, and new signals are rare when they first arise. Several possible solutions have been offered to solve this apparent evolutionary paradox, but disagreement persists over the plausibility of some of the proposed mechanisms. In this paper, we construct a deterministic numerical simulation model that allows us to derive the strength of selection on novel warning signals in a wide range of biologically relevant situations. We study the effects of predator psychology (learning, rate of mistaken attacks, and neophobia) on selection. We also study the how prey escape, predation intensity, number of predators, and abundance of different prey types affects selection. The model provides several important results. Selection on novel warning signals is number rather than frequency dependent. In most cases, there exists a threshold number of aposematic individuals below which aposematism is selected against and above which aposematism is selected for. Signal conspicuousness (which increases detection rate) and distinctiveness (which allows predator to distinguish defended from nondefended prey) have opposing effects on evolution of warning signals. A more conspicuous warning signal cannot evolve unless it makes the prey more distinctive from palatable prey, reducing mistaken attacks by predators. A novel warning signal that is learned quickly can spread from lower abundance more easily than a signal that is learned more slowly. However, the relative rate at which the resident signal and the novel signal are learned is irrelevant for the spread of the novel signal. Long-lasting neophobia can facilitate the spread of novel warning signals. Individual selection via the ability of defended prey to escape from predator is not likely to facilitate evolution of conspicuous warning signals if both the resident (cryptic) morph and the novel morph have the same escape probability. Predation intensity (defined as the proportion of palatable prey eaten by the predator) has a strong effect on selection. More intense predation results in strong selection against rare signals, but also strong selective advantage to common signals. The threshold number of aposematic individuals is lower when predation is intense. Thus, the evolution of warning signals may be more likely in environments where predation is intense. The effect of numbers of predators depends on whether predation intensity also changes. When predation intensity is constant, increasing numbers of predators raises the threshold number of aposematic individuals, and thus makes evolution of aposematism more difficult. If predation intensity increases in parallel with number of predators, the threshold number of aposematic individuals does not change much, but selection becomes more intense on both sides of the threshold.     

Predation threat modifies relationships between metabolism and behavioural traits but not their ecological relevance in Chinese bream

The aims of this study were to test whether the metabolism, behavioural traits, growth and survival under predation of a fish species phenotypically changed under predation threat with the particular emphasis on whether short-time predator exposure would amplify the relationships between metabolic rate and behavioural traits and their fitness consequences (growth and survival). We found that Chinese bream under predation threat for 20 days exhibited a lower specific growth rate (SGR), feeding rate (FR) and feeding efficiency (FE) but a higher standard metabolic rate (SMR) and survival when encountering predators compared to the bream in the no-predator group. Both activity and boldness showed no correlation to SMR in the no-predator group, while it was vice versa in the predator group according to Pearson correlation. It thus demonstrated that short-time predator exposure can mediate the relationships between metabolism and behavioural traits, suggesting that predation may play an important evolutionary role in modifying intraspecific behavioural differences via metabolism. However, no significant effect of predator treatment acted on relationships between behaviour traits and SMR according to ANCOVA, which possibly due to the small sample size of this study. Additionally, the SMR of both groups was positively correlated with survival under predation, whereas the relationships between SMR and fitness cost such as growth and survival are rather complicated and need further investigation.     

The role of size-specific predation in the evolution and diversification of prey life histories

Some of the best empirical examples of life-history evolution involve responses to predation. Nevertheless, most life-history theory dealing with responses to predation has not been formulated within an explicit dynamic food-web context. In particular, most previous theory does not explicitly consider the coupled population dynamics of the focal species and its predators and resources. Here we present a model of life-history evolution that explores the evolutionary consequences of size-specific predation on small individuals when there is a trade-off between growth and reproduction. The model explicitly describes the population dynamics of a predator, the prey of interest, and its resource. The selective forces that cause life-history evolution in the prey species emerge from the ecological interactions embodied by this model and can involve important elements of frequency dependence. Our results demonstrate that the strength of the coupling between predator and prey in the community determines many aspects of life-history evolution. If the coupling is weak (as is implicitly assumed in many previous models), differences in resource productivity have no effect on the nature of life-history evolution. A single life-history strategy is favored that minimizes the equilibrium resource density (if possible). If the coupling is strong, then higher resource productivities select for faster growth into the predation size refuge. Moreover, under strong coupling it is also possible for natural selection to favor an evolutionary diversification of life histories, possibly resulting in two coexisting species with divergent life-history strategies.     

Mothers' Egg-pooling and Aposematic Offspring's Gregariousness: Cui bono?

Recently Sillén-Tullberg & Leimar (1988) modelled a general explanation for the evolution of gregariousness in prey organisms that live exposed, have no means of escape when discovered by a predator, and are small in relation to a potential predator (who thus can sample many prey individuals in one encounter). The model predicts that gregarious prey organisms of that type ought to be distasteful, and that the evolution of gregariousness will be favoured by aposematic coloration facilitating avoidance learning in a predator. Obviously, any protective power of grouping depends on group size. According to the Sillén-Tullberg & Leimar model, (1) “members of small groups may have a higher rate of death from predation than solitary individuals, but above a certain minimum group size, group members do better than solitary individuals; … as group size increases above the minimum value, group members suffer fewer and fewer deaths from predation”. They benefit from the “decreased risk of predator attack on any particular individual”, called dilution effect. (2) “The more prey specimens that the predator needs to sample during avoidance learning, the larger an aggregation needs to be in order for gregariousness to be advantageous”. It is further explained that (3) selection resulting from predation favours increase in group size until it “acts like a predator-satiation mechanism”.     

Loss of body mass under predation risk: cost of antipredatory behaviour or adaptive fit-for-escape?

Predation risk may compromise the ability of animals to acquire and maintain body reserves by hindering foraging efficiency and increasing physiological stress. Locomotor performance may depend on body mass, so losing mass under predation risk could be an adaptive response of prey to improve escape ability. We studied individual variation in antipredatory behaviour, feeding rate, body mass and escape performance in the lacertid lizard Psammodromus algirus. Individuals were experimentally exposed to different levels of food availability (limited or abundant) and predation risk, represented by reduced refuge availability and simulated predator attacks. Predation risk induced lizards to reduce conspicuousness behaviourally and to avoid feeding in the presence of predators. If food was abundant, alarmed lizards reduced feeding rate, losing mass. Lizards supplied with limited food fed at near-maximum rates independently of predation risk but lost more mass when alarmed; thus, mass losses experienced under predation risk were higher than those expected from feeding interruption alone. Although body mass of lizards varied between treatments, no component of escape performance measured during predator attacks (endurance, speed, escape strategy) was affected by treatments or by variations in body mass. Thus, the body mass changes were consistent with a trade-off between gaining resources and avoiding predators, mediated by hampered foraging efficiency and physiological stress. However, improved escape efficiency is not required to explain mass reduction upon predator encounters beyond that expected from feeding interruption or predation-related stress. Therefore, the idea that animals may regulate body reserves in relation to performance demands should be reconsidered.     

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.     

Consequences of information use in breeding habitat selection on the evolution of settlement time

The role of temporal changes and spatial variability in predation risk and prey's means of mitigating such risks is poorly understood in the context of potential threats of global climate change for migratory birds. Yet nest predation, for example, represents a primary source of reproductive mortality in birds. To assess risk birds must spend time prospecting potential breeding sites for cues or signals of predator presence. However, competition for breeding sites with advantage to prior residency poses an evolutionary dilemma as individuals also benefit from early settling. We develop a model to examine adaptive prospecting time for predator cues on breeding grounds characterized by spatial heterogeneity in nest predation risk. We study how populations respond to environmental change represented by variation in habitat specific levels of nest predation, habitat composition, population vital rates, and availability of information (via prospecting) in the form of acoustic predator cues. We identify two mechanisms that regulate and buffer impacts of environmental change on populations. First, the adaptive response to lower population abundance under deteriorating environmental conditions is to increase prospecting time, which in turn increases individuals nest success to counteract population declines. This occurs because reduced competition for sites decreases the benefit of early settlement. Second, per capita success in site choice increases during population declines owing to reduced competition that increases the availability of good sites. We also show that the increased benefit to settling early when competition increases can lead to the paradoxical result that with greater spatial heterogeneity, less effort is placed on discerning good and bad sites. Our analysis thus contributes several novel results by which nest predation, settlement phenology, prospecting time and information gathering can influence species capacity to adapt to changing environments.     

Predation risk and resource abundance mediate foraging behaviour and intraspecific resource partitioning among consumers in dominance hierarchies

Dominance hierarchies and the resulting unequal resource partitioning among individuals are key mechanisms of population regulation. The strength of dominance hierarchies can be influenced by size‐dependent tradeoffs between foraging and predator avoidance whereby competitively inferior subdominants can access a larger proportion of limiting resources by accepting higher predation risk. Foraging‐predation risk tradeoffs also depend on resource abundance. Yet, few studies have manipulated predation risk and resource abundance simultaneously; consequently, their joint effect on resource partitioning within dominance hierarchies are not well understood. We addressed this gap by measuring behavioural responses of masu salmon Oncorhynchus masou ishikawae to experimental manipulations of predation risk and resource abundance in a natural temperate forest stream. Responses to predation risk depended on body size and social status such that larger fish (often social dominants) exhibited more risk‐averse behaviour (e.g. lower foraging and appearance rates) than smaller subdominants after exposure to a simulated predator. The magnitude of this effect was lower when resources were elevated, indicating that dominant fish accepted a higher predation risk to forage on abundant resources. However, the influence of resource abundance did not extend to the population level, where predation risk altered the distribution of foraging attempts (a proxy for energy intake) from being skewed towards large individuals to being skewed towards small individuals after predator exposure. Our results imply that size‐dependent foraging–predation risk tradeoffs can weaken the strength of dominance hierarchies by allowing competitively inferior subdominants to access resources that would otherwise be monopolized.     

Local prey vulnerability increases with multiple attacks by a predator

Theory and empirical evidence suggest that predator activity makes prey more wary and less vulnerable to predation. However if at least some prey in the population are energetically or spatially constrained, then predators may eventually increase local prey vulnerability because of the cumulative costs of anti‐predation behaviour. We tested whether repeated attacks by a predator might increase prey vulnerability in a system where redshanks on a saltmarsh are attacked regularly by sparrowhawks from adjacent woodland. Cumulative attack number led to a reduction in redshank numbers and flock size (but had no effect on how close redshanks fed to predator‐concealing cover) because some redshanks moved to safer but less profitable habitats, leaving smaller flocks on the saltmarsh. This effect held even though numbers of redshank on the saltmarsh increased with time of day. As a result of the change in flock size, predicted attack‐success increased up to 1.6‐fold for the sparrowhawk, while individual risk of capture for the redshank increased up to 4.5‐fold among those individuals remaining on the saltmarsh. The effect did not arise simply because hawks were more likely to attack smaller flocks because attack rate was not dependent on flock size or abundance. Our data demonstrate that when some individual prey are constrained in their ability to feed on alternative, safer foraging sites, their vulnerability to predation increases as predator attacks accumulate, although those, presumably better quality individuals that leave the immediate risky area will have lower vulnerability, so that the mean vulnerability across the entire population may not have changed substantially. This suggests that the selective benefits of multiple low‐cost attacks by predators on prey could potentially lead to 1) locally heightened trait‐mediated interactions, 2) locally reduced interference among competing predators, and 3) the evolution of active prey manipulation by predators.     

Habitat quality mediates personality through differences in social context

Assessing the stability of animal personalities has become a major goal of behavioral ecologists. Most personality studies have utilized solitary individuals, but little is known on the extent that individuals retain their personality across ecologically relevant group settings. We conducted a field survey which determined that mud crabs, Panopeus herbstii, remain scattered as isolated individuals on degraded oyster reefs while high quality reefs can sustain high crab densities (>10 m^?2). We examined the impact of these differences in social context on personality by quantifying the boldness of the same individual crabs when in isolation and in natural cohorts. Crabs were also exposed to either a treatment of predator cues or a control of no cue throughout the experiment to assess the strength of this behavioral reaction norm. Crabs were significantly bolder when in groups than as solitary individuals with predator cue treatments exhibiting severally reduced crab activity levels in comparison to corresponding treatments with no predator cues. Behavioral plasticity depended on the individual and was strongest in the presence of predator cues. While bold crabs largely maintained their personality in isolation and group settings, shy crabs would become substantially bolder when among conspecifics. These results imply that the shifts in crab boldness were a response to changes in perceived predation risk, and provide a mechanism for explaining variation in behavioral plasticity. Such findings suggest that habitat degradation may produce subpopulations with different behavioral patterns because of differing social interactions between individual animals.     

Oscillations in a size-structured prey-predator model

This article introduces a predator–prey model with the prey structured by body size, based on reports in the literature that predation rates are prey-size specific. The model is built on the foundation of the one-species physiologically structured models studied earlier. Three types of equilibria are found: extinction, multiple prey-only equilibria and possibly multiple predator–prey coexistence equilibria. The stabilities of the equilibria are investigated. Comparison is made with the underlying ODE Lotka–Volterra model. It turns out that the ODE model can exhibit sustain oscillations if there is an Allee effect in the net reproduction rate, that is the net reproduction rate grows for some range of the prey’s population size. In contrast, it is shown that the structured PDE model can exhibit sustain oscillations even if the net reproductive rate is strictly declining with prey population size. We find that predation, even size-non-specific linear predation can destabilize a stable prey-only equilibrium, if reproduction is size specific and limited to individuals of large enough size. Furthermore, we show that size-specific predation can also destabilize the predator–prey equilibrium in the PDE model. We surmise that size-specific predation allows for temporary prey escape which is responsible for destabilization in the predator–prey dynamics.     

Influence of predation risk on individual competitive ability and growth in Eurasian perch, Perca fluviatilis

We studied the potential influence of predation risk on the competitive ability and habitat use of foraging perch and the effect of these interactions on growth. Groups of four similar-sized young-of-the-year perch were in visual contact with a piscivorous perch during feeding. The fry had the choice of vegetation and open habitat, with food presented in the open habitat. Competitive ability, defined as proportion of prey attacks, varied between perch individuals and was unaffected by predation risk. The variation in proportion of prey attacks was affected by relative size within each replicate group, despite small size differences (±1 mm), with the largest individual being a better competitor than the smallest ones. The degree of boldness, measured as the proportion of time spent in the open habitat, was significantly related to both competitive ability and prey attack order. Observations of aggressive behaviour indicated a possible occurrence of interference competition, which may contribute to the appearance of different competitive abilities between individuals within a group of perch. A significant correlation was found between competitive ability and growth. Growth variation within groups was not affected by predation risk.     

The non-consumptive effects of predators and personality on prey growth and mortality

Individual organisms vary in personality, and the ecological consequences of that variation can affect the strength of predator–prey interactions. Prey with bolder tendencies can mitigate the strength of species interactions by altering growth and initiating ontogenetic niche shifts (ONS). While the link between personality and growth has been established, recent research has highlighted the important interplay between ONS and predator cues in community ecology. The objective of this study was to evaluate the effects of prey personality and predator cues on prey growth and ONS. We predicted growth–mortality trade-offs among personalities with higher survival, larger size, and accelerated ONS for bold individuals in comparison with shy individuals. To evaluate this objective, we conducted behavioral assays and a mesocosm experiment to test how southern leopard frog (Rana sphenocephala) tadpole personality and predatory fish (bluegill, Lepomis macrochirus) cues affects tadpole growth and metamorphosis. On average, bold tadpoles had higher mortality across all treatments in comparison with shy tadpoles. The effects of fish cues were dependent on tadpole personality with shy tadpoles metamorphosing significantly later than bold tadpoles. Bold tadpoles were larger than shy tadpoles at metamorphosis; however, that pattern reversed with fish cues as shy individuals metamorphosed larger than bold individuals. Our results suggest personality may be useful for predicting growth and life history for some prey species with predators. Specifically, the threat of predation can interact with personality to incur a benefit (earlier ONS) while also incurring a cost (size at metamorphosis). Hence by incorporating predator cues with personality, ecologists will be able to elucidate growth–mortality trade-offs mediated by personality.     

Optimal escape theory predicts escape behaviors beyond flight initiation distance： risk assessment and escape by striped plateau lizards Sceloporus virgatus

Escape theory predicts that flight initiation distance (FID=distance between predator and prey when escape begins) is longer when risk is greater and shorter when escape is more costly. A few tests suggest that escape theory applies to distance fled. Escape models have not addressed stochastic variables, such as probability of fleeing and of entering refuge, but their economic logic might be applicable. Experiments on several risk factors in the lizard Sceloporus virgatus confirmed all predictions for the above escape variables. FID was greater when approach was faster and more direct, for lizards on ground than on trees, for lizards rarely exposed to humans, for the second of two approaches, and when the predator turned toward lizards rather than away. Lizards fled further during rapid and second consecutive approaches. They were more likely to flee when approached directly, when a predator turned toward them, and during second approaches. They were more likely to enter refuge when approached rapidly. A novel finding is that perch height in trees was unrelated to FID because lizards escaped by moving out of sight, then moving up or down unpredictably. These findings add to a growing body of evidence supporting predictions of escape theory for FID and distance fled. They show that two probabilistic aspects of escape are predictable based on relative predation risk levels. Because individuals differ in boldness, the assessed optimal FID and threshold risks for fleeing and entering refuge are exceeded for an increasing proportion of individuals as risk increases[Current Zoology 55(2):123-131,2009].