Intraindividual variability in behavior shapes fitness landscapes

Although intraindividual variability (IIV) in behavior is fundamental to ecological dynamics, the factors that contribute to the expression of IIV are poorly understood. Using an individual‐based model, this study examined the effects of stochasticity on the evolution of IIV represented by the residual variability of behavior. The model describes a population of prey with nonoverlapping generations, in which prey take refuge upon encountering a predator. The strategy of a prey is characterized by the mean and IIV (i.e., standard deviation) of hiding duration. Prey with no IIV will spend the same duration hiding in a refuge at each predator encounter, while prey with IIV will have variable hiding durations among encounters. For the sources of stochasticity, within‐generation stochasticity (represented by random predator encounters) and between‐generation stochasticity (represented by random resource availability) were considered. Analysis of the model indicates that individuals with high levels of IIV are maintained in a population in the presence of between‐generation stochasticity even though the optimal strategy in each generation is a strategy with no IIV, regardless of the presence or absence of within‐generation stochasticity. This contradictory pattern emerges because the mean behavioral trait and IIV do not independently influence fitness (e.g., the sign of the selection gradient with respect to IIV depends on the mean trait). Consequently, even when evolution eventually leads toward a strategy with no IIV (i.e., the optimal strategy), greater IIV may be transiently selected. Between‐generation stochasticity consistently imposes such transient selection and maintain high levels of IIV in a population.     

Intraindividual Variability of Boldness Is Repeatable across Contexts in a Wild Lizard

Animals do not behave in exactly the same way when repeatedly tested in the same context or situation, even once systematic variation, such as habituation, has been controlled for. This unpredictability is called intraindividual variability (IIV) and has been little studied in animals. Here we investigated how IIV in boldness (estimated by flight initiation distances) changed across two seasons—the dry, non-breeding season and the wet, breeding season—in a wild population of the Namibian rock agama, Agama planiceps. We found significant differences in IIV both between individuals and seasons, and IIV was higher in the wet season, suggesting plasticity in IIV. Further, IIV was highly repeatable (r = 0.61) between seasons and we found strong negative correlations between consistent individual differences in flight initiation distances, i.e. their boldness, and individuals'' IIVs. We suggest that to understand personality in animals, researchers should generate a personality ‘profile’ that includes not only the relative level of a trait (i.e. its personality), but also its plasticity and variability under natural conditions.     

How do anthropogenic contaminants (ACs) affect behaviour? Multi-level analysis of the effects of copper on boldness in hermit crabs

Natural animal populations are increasingly exposed to human impacts on the environment, which could have consequences for their behaviour. Among these impacts is exposure to anthropogenic contaminants. Any environmental variable that influences internal state could impact behaviour across a number of levels: at the sample mean, at the level of among-individual differences in behaviour (‘animal personality’) and at the level of within-individual variation in behaviour (intra-individual variation, ‘IIV’). Here we examined the effect of exposure to seawater-borne copper on the startle response behaviour of European hermit crabs, Pagurus bernhardus across these levels. Copper exposure rapidly led to longer startle responses on average, but did not lead to any change in repeatability indicating that individual differences were present and equally consistent in the presence and absence of copper. There was no strong evidence that copper exposure led to changes in IIV. Our data show that exposure to copper for 1 week produces sample mean level changes in the behaviour of hermit crabs. However, there is no evidence that this exposure led to changes in repeatability through feedback loops.     

How do developmental and parental exposures to predation affect personality and immediate behavioural plasticity in the snail Physa acuta?

Individuals differ in personality and immediate behavioural plasticity. While developmental environment may explain this group diversity, the effect of parental environment is still unexplored—a surprising observation since parental environment influences mean behaviour. We tested whether developmental and parental environments impacted personality and immediate plasticity. We raised two generations of Physa acuta snails in the laboratory with or without developmental exposure to predator cues. Escape behaviour was repeatedly assessed on adult snails with or without predator cues in the immediate environment. On average, snails were slower to escape if they or their parents had been exposed to predator cues during development. Snails were also less plastic in response to immediate predation risk on average if they or their parents had been exposed to predator cues. Group diversity in personality was greater in predator-exposed snails than unexposed snails, while parental environment did not influence it. Group diversity in immediate plasticity was not significant. Our results suggest that only developmental environment plays a key role in the emergence of group diversity in personality, but that parental environment influences mean behavioural responses to the environmental change. Consequently, although different, both developmental and parental cues may have evolutionary implications on behavioural responses.     

Comparing the strength of behavioural plasticity and consistency across situations: animal personalities in the hermit crab Pagurus bernhardus

Many phenotypic traits show plasticity but behaviour is often considered the 'most plastic' aspect of phenotype as it is likely to show the quickest response to temporal changes in conditions or 'situation'. However, it has also been noted that constraints on sensory acuity, cognitive structure and physiological capacities place limits on behavioural plasticity. Such limits to plasticity may generate consistent differences in behaviour between individuals from the same population. It has recently been suggested that these consistent differences in individual behaviour may be adaptive and the term 'animal personalities' has been used to describe them. In many cases, however, a degree of both behavioural plasticity and relative consistency is probable. To understand the possible functions of animal personalities, it is necessary to determine the relative strength of each tendency and this may be achieved by comparison of statistical effect sizes for tests of difference and concordance. Here, we describe a new statistical framework for making such comparisons and investigate cross-situational plasticity and consistency in the duration of startle responses in the European hermit crab Pagurus bernhardus, in the field and the laboratory. The effect sizes of tests for behavioural consistency were greater than for tests of behavioural plasticity, indicating for the first time the presence of animal personalities in a crustacean model.     

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.     

Individual and Sex Differences in Habituation and Neophobia in House Sparrows (Passer domesticus)

Heterogeneity in the environment favours foragers that are flexible (phenotypically plastic). However, consistent individual differences in behaviour (personality), such as in risk‐taking, might affect an individual's ability to find food, avoid predators and adjust to new conditions. It is now well known that personalities exist in many taxa, but much less is known about individual variation in plasticity. We measured the tendency to begin foraging across different levels of risk in house sparrows (Passer domesticus), using a behavioural reaction norm framework to simultaneously assess personality and plasticity. We asked whether individuals were consistently different across risk levels, and whether they differed in habituation and neophobia, both of which were treated as cases of plasticity. We found that males habituated more than females by beginning to feed sooner after repeated instances of a human disturbance in the presence of an initially unfamiliar object. Individuals of both sexes also exhibited consistent differences across trials, but did not differ in the rate of habituation beyond the difference between the sexes. When a novel object was placed in the foraging area, both sexes exhibited similar degrees of neophobia by delaying feeding. The magnitude of this change varied among birds, indicating individual differences in neophobia. Our results indicate that both personality and individual variation in plasticity exist but should be treated as independent phenomena. The presence of variation in plasticity implies that the raw material necessary for selection on neophobia exists, and that if heritable, plasticity in risk‐taking across contexts could evolve.     

Individual variation in behavioural plasticity: direct and indirect effects of boldness,exploration and sociability on habituation to predators in lizards

Little is known about the factors causing variation in behavioural plasticity and the interplay between personality and plasticity. Habituation to predators is a special case of behavioural plasticity. We investigated the direct and indirect effects of boldness, exploration and sociability traits on the habituation ability of Iberian wall lizards, considering exposure and sex effects. Individual boldness was consistent across several non-habituation contexts, but it did not significantly affect habituation. Exploration had a strong direct effect on habituation, with more exploratory individuals being able to habituate faster than less exploratory ones, probably because of their ability to assess risk better. Individual variation in habituation was also affected by sociability, but this was an indirect effect mediated by exposure to the predator. Less social individuals avoided refuges with conspecific cues, increasing exposure to the predator and eventually habituation. Finally, the direct effects of sex (females habituated faster than males) were opposite to its indirect effects through exposure. We conclude that risk assessment, instead of the proactivity–reactivity gradient usually considered in the literature, can affect behavioural plasticity through complex interactions between direct and indirect effects, including exploratory behaviour, degree of exposure to the predator and sex, which represent novel mechanisms generating inter-individual variation in plasticity.     

Individual quality and personality: bolder males are less fecund in the hermit crab Pagurus bernhardus

One explanation for animal personality is that different behavioural types derive from different life-history strategies. Highly productive individuals, with high growth rates and high fecundity, are assumed to live life at a fast pace showing high levels of boldness and risk taking, compared with less productive individuals. Here, we investigate among-individual differences in mean boldness (the inverse of the latency to recover from a startling stimulus) and in the consistency of boldness, in male hermit crabs in relation to two aspects of life-history investment. We assessed aerobic scope by measuring the concentration of the respiratory pigment haemocyanin, and we assessed fecundity by measuring spermatophore size. First, we found that individuals investing in large spermatophores also had high concentrations of haemocyanin. Using doubly hierarchical-generalized linear models to analyse longitudinal data on startle responses, we show that hermit crabs vary both in their mean response durations and in the consistency of their behaviour. Individual consistency was unrelated to haemocyanin concentration or spermatophore size, but mean startle response duration increased with spermatophore size. Thus, counter to expectations, it was the most risk-averse individuals, rather than the boldest and most risk prone, that were the most productive. We suggest that similar patterns should be present in other species, if the most productive individuals avoid risky behaviour.     

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.     

Inspection behaviour and inter-individual cooperation in juvenile qingbo: the effects of prior predator exposure and food deprivation

The predation pressure and food availability to which individuals are exposed during their life histories shape inspection behaviour in animals. In this study, we aimed to test whether such behaviours varied with prior experience (predation, starvation or both treatments) or measurement condition (with or without the presence of a predator; here, the snakehead fish, Channa argus) in the fish species Spinibarbus sinensis, known as qingbo. Unexpectedly, prior predator experience showed no significant effect on inspection behaviour as demonstrated by either the frequency or the duration of each activity outside shelter or on cooperation as demonstrated by the inter-individual distance or synchronization of speed. This may have been due to the different adjustments in behaviour among individuals (more shelter use vs. more inspection), the predator treatment used in the present study (exposure to caged predator rather than direct predation) and/or a species-specific strategy in the qingbo. The starved fish displayed shorter inspection latency, increased inspection behaviour and greater cooperation when measured without the predator; however, when measured in the presence of the predator, the starved fish showed increased inspection frequency but shorter inspection duration, possibly due to the compromise between energy needs and predation risk. Similar to those of the predation group, the fish from the double-treated group showed no difference in inspection behaviour compared to the control group under the predator-absent condition, while the high-frequency, short-duration inspection behaviours remained the same as in the starved group. These findings suggested that the adjustment of inspection behaviour and related cooperation are rather complicated according to either predator experience or food deprivation, partially due to the inter-individual differences in behavioural adjustment and/or different environmental conditions.     

Environmental and genetic effects shape the development of personality traits in the mangrove killifish Kryptolebias marmoratus

Consistent individual differences in behaviour are well documented, for example, individuals can be defined as consistently bold or consistently shy. To date our understanding of the mechanisms underpinning consistent individual differences in behaviour (also termed behavioural types (BTs)) remains limited. Theoretical work suggests life‐history tradeoffs drive BT variation, however, empirical support is scarce. Moreover, whilst life‐history is known to be phenotypically plastic in response to environmental conditions during ontogeny, the extent to which such plasticity drives plasticity in behavioural traits and personality remains poorly understood. Using a natural clonal vertebrate, Kryptolebias marmoratus, we control for genetic variation and investigate developmental plasticity in life‐history and three commonly studied behavioural traits (exploration, boldness, aggression) in response to three ecologically relevant environments; conspecific presence, low food and perceived risk. Simulated predation risk was the only treatment that generated repeatable behaviour i.e. personality during ontogeny. Treatments differed in their effects on mean life‐history and behavioural scores. Specifically, low food fish exhibited reduced growth rate and exploration but did not differ from control fish in their boldness or aggression scores. Conspecific presence resulted in a strong negative effect on mean aggression, boldness and exploration during ontogeny but had minimal effect on life‐history traits. Simulated predation risk resulted in increased reproductive output but had minimal effect upon average behavioural scores. Together these results suggest that life‐history plasticity/variation may be insufficient in driving variation in personality during development. Finally, using offspring derived from each rearing environment we investigate maternal effects and find strong maternal influence upon offspring size, but not behaviour. These results highlight and support the current understanding that risk perception is important in shaping personality, and that social experience during ontogeny is a major influence upon behavioural expression.     

Consistency in boldness expression varies with ecological context in a jumping spider

Animals can adjust their behaviours depending on ecological context (i.e., behavioural plasticity), and an individual's response to a given context may also vary from occasion to occasion (intra‐individual variability). Recognizing the roles of both behavioural plasticity and intra‐individual variability is important in understanding how behavioural diversity is maintained within populations. However, how the ecological context itself influences the individual behavioural response and intra‐individual variability (e.g., how variable an individual is in their behavioural expression) remains largely unexplored. Here, we examine boldness expression (the duration of startle response) in a specialised spider‐eating jumping spider, Portia labiata, across three contexts following a mild disturbance: presence of a conspecific intruder (most dangerous), environmental change but no conspecific intruder, and no conspecific intruder or environmental change (safest). We found that context does not significantly influence the average boldness expression at the population level. However, each individual responded to each context differently, and the repeatability of boldness expression—the proportion of behavioural variation attributable to the between ‐individual level—is context‐dependent. We also found that in the presence of a conspecific intruder, spiders behave less predictably than in the environmental change context, but not differently from the safest context. These findings may suggest that the presence of conspecifics influences behavioural consistency in individuals, but that this may occur without influencing the population average behaviour.     

Brain size predicts behavioural plasticity in guppies (Poecilia reticulata): An experiment

Understanding how animal personality (consistent between‐individual behavioural differences) arises has become a central topic in behavioural sciences. This endeavour is complicated by the fact that not only the mean behaviour of individuals (behavioural type) but also the strength of their reaction to environmental change (behavioural plasticity) varies consistently. Personality and cognitive abilities are linked, and we suggest that behavioural plasticity could also be explained by differences in brain size (a proxy for cognitive abilities), since accurate decisions are likely essential to make behavioural plasticity beneficial. We test this idea in guppies (Poecilia reticulata), artificially selected for large and small brain size, which show clear cognitive differences between selection lines. To test whether those lines differed in behavioural plasticity, we reared them in groups in structurally enriched environments and then placed adults individually into empty tanks, where we presented them daily with visual predator cues and monitored their behaviour for 20 days with video‐aided motion tracking. We found that individuals differed consistently in activity and risk‐taking, as well as in behavioural plasticity. In activity, only the large‐brained lines demonstrated habituation (increased activity) to the new environment, whereas in risk‐taking, we found sensitization (decreased risk‐taking) in both brain size lines. We conclude that brain size, potentially via increasing cognitive abilities, may increase behavioural plasticity, which in turn can improve habituation to novel environments. However, the effects seem to be behaviour‐specific. Our results suggest that brain size likely explains some of the variation in behavioural plasticity found at the intraspecific level.     

Context-Dependent Plastic Response during Egg-Laying in a Widespread Newt Species

Previous research on predator-induced phenotypic plasticity mostly focused on responses in morphology, developmental time and/or behaviour during early life stages, but the potential significance of anticipatory parental responses has been investigated less often. In this study I examined behavioural and maternal responses of gravid female smooth newts, Lissotriton vulgaris, in the presence of chemical cues originating from invertebrate predators, Acilius sulcatus water beetles and Aeshna cyanea dragonfly larvae. More specifically, I tested the extent of oviposition preference, plasticity in egg-wrapping behaviour and plasticity in egg size when females had the possibility to lay eggs at oviposition sites with and without predator cues during overnight trials. I found that individuals did not avoid laying eggs in the environment with predator cues; however, individuals that deposited eggs into both environments adjusted the size of the laid eggs to the perceived environment. Females deposited larger eggs earlier in the season but egg size decreased with time in the absence of predator cues, whereas individuals laid eggs of average size throughout the investigated reproductive period when such cues were present. Also, egg size was found to be positively related to hatching success. Individuals did not adjust their wrapping behaviour to the presence of predator cues, but females differed in the extent of egg-wrapping between ponds. Females’ body mass and tail depth were also different between ponds, whereas their body size was positively associated with egg size. According to these results, female smooth newts have the potential to exhibit activational plasticity and invest differently into eggs depending on temporal and environmental factors. Such an anticipatory response may contribute to the success of this caudate species under a wide range of predator regimes at its natural breeding habitats.     

Behavioural syndrome in a solitary predator is independent of body size and growth rate

Models explaining behavioural syndromes often focus on state-dependency, linking behavioural variation to individual differences in other phenotypic features. Empirical studies are, however, rare. Here, we tested for a size and growth-dependent stable behavioural syndrome in the juvenile-stages of a solitary apex predator (pike, Esox lucius), shown as repeatable foraging behaviour across risk. Pike swimming activity, latency to prey attack, number of successful and unsuccessful prey attacks was measured during the presence/absence of visual contact with a competitor or predator. Foraging behaviour across risks was considered an appropriate indicator of boldness in this solitary predator where a trade-off between foraging behaviour and threat avoidance has been reported. Support was found for a behavioural syndrome, where the rank order differences in the foraging behaviour between individuals were maintained across time and risk situation. However, individual behaviour was independent of body size and growth in conditions of high food availability, showing no evidence to support the state-dependent personality hypothesis. The importance of a combination of spatial and temporal environmental variation for generating growth differences is highlighted.     

Personality and Nest Defence in the Great Tit (Parus major)

A growing number of studies have shown that individuals differ consistently in a suite of correlated behavioural traits across various contexts and situations. Yet, most work on animal personalities has been performed under laboratory conditions and still little is known about the ecological significance of differences in personality in the wild, and the behavioural mechanisms underlying possible fitness consequences. In this study, we investigated individual differences in personality in relation to nest defence behaviour in wild great tits. Nest defence is an important aspect of parental care and involves a trade‐off between two fitness components (i.e. survival and reproduction). As a measure of personality we used exploratory behaviour in a novel environment as this has been shown to be correlated with several other behavioural traits including risk‐taking and aggression, two important behavioural components of nest defence. We found that the intensity of alarm calling towards a human intruder was positively associated with exploratory behaviour, while there was a negative association between exploration score and number of movements during nest defence. Thus, fast explorers are shown to respond more boldly towards predators in the field. More generally we show that individuals with different personalities vary in their anti‐predator and reproductive investment strategies.     

Sex‐Specific Associations Between Nest Defence,Exploration and Breathing Rate in Breeding Pied Flycatchers

Correlations between behavioural traits constrain animals to a limited range of behavioural choices and set a limit to the available variation in behavioural phenotype of a population. These constraints are especially important during stressful situations, potentially limiting the ability to cope with stress appropriately. As yet, very little consideration has been given to a possible role for sexual selection in maintaining differences in behavioural stability within individuals: sex‐specific differences in behavioural correlations have been seldom studied, especially in the wild. In this field study, we investigated associations between neophobia (latency to enter nest in the presence of a novel object), nest defence (response to a model predator) and breathing rate in response to handling in breeding pied flycatchers (Ficedula hypoleuca). We did not find any significant difference in antipredator responses between males and females, which indicates low sexual conflict over parental care in the pied flycatcher. However, females were more neophobic than males, while males and females did not differ in their breathing rates. Further, our study demonstrated a strong positive correlation between nest defence behaviour and neophobia in male, but not in female pied flycatchers. Males that defended their nest more had lower breathing rate and higher latency to resume nestling feeding after encountering a predator decoy than males that mobbed less intensely. We found only weak evidence that nest partners might affect each other's behaviour in these contexts.     

Tracking the startle response of guppies Poecilia reticulata in three dimensions

A three‐dimensional analysis of startle behaviours of guppies Poecilia reticulata, in dyads or alone, from two populations that show distinct differences in shoaling behaviour was performed. During the first few seconds after a startling stimulus, changes in behaviour, which could be critical if an individual is to survive a predatory attack, and the interactions between pairs of P. reticulata were examined. The enhanced social interactions immediately after the stimulus, as a proxy for shoaling behaviour, and their dissipation were quantified. Social (individuals tested in dyads) v. asocial (tested alone) responses to the startling stimulus were also compared. The three‐dimensional reconstruction, from a two‐camera, high‐frame‐rate tracking system allowed for the tracking of the individuals' speed and speed recovery and, for P. reticulata in dyads, interindividual distance and orientation. For the dyads from the high‐predation population, the closer the individuals were to each other, the more likely they were to be parallel, but no correlation was found for the low‐predation P. reticulata. The startle response of P. reticulata comprised the following sequence: freezing, darting and skittering and recovery to pre‐stimulus swimming behaviour. Upon repeated encounters with the stimulus, a reduced shoaling and startle response was observed, although the rate of reduction was faster in P. reticulata from the high‐predation population than those from the low‐predation population. The results are discussed in light of what is known about the anti‐predator behaviour of this species.     

High in situ repeatability of behaviour indicates animal personality in the beadlet anemone Actinia equina (Cnidaria)

'Animal personality' means that individuals differ from one another in either single behaviours or suites of related behaviours in a way that is consistent over time. It is usually assumed that such consistent individual differences in behaviour are driven by variation in how individuals respond to information about their environment, rather than by differences in external factors such as variation in microhabitat. Since behavioural variation is ubiquitous in nature we might expect 'animal personality' to be present in diverse taxa, including animals with relatively simple nervous systems. We investigated in situ startle responses in a sea anemone, Actinia equina, to determine whether personalities might be present in this example of an animal with a simple nervous system. We found very high levels of repeatability among individuals that were re-identified in the same locations over a three week sampling period. In a subset of the data, where we used tide-pool temperature measurements to control for a key element of variation in microhabitat, these high levels of repeatability remained. Although a range of other consistent differences in micro-habitat features could have contributed to consistent differences between the behaviour of individuals, these data suggest the presence of animal personality in A. equina. Rather than being restricted to certain groups, personality may be a general feature of animals and may be particularly pronounced in species with simple nervous systems.