Variation In Behavioural Plasticity Research Articles

Scope and adaptive value of modulating aggression over breeding stages in a competitive female bird

Abstract In seasonally breeding animals, the costs and benefits of territorial aggression should vary over time; however, little work thus far has directly examined the scope and adaptive value of individual-level plasticity in aggression across breeding stages. We explore these issues using the tree swallow (Tachycineta bicolor), a single-brooded bird species in which females compete for limited nesting sites. We measured aggressiveness in nearly 100 females within 3 different stages: (1) shortly after territory-establishment, (2) during incubation, and (3) while caring for young chicks. Based on the timing, direction, and magnitude of behavioral changes between stages, we used k-means clustering to categorize each female’s behavior into a “plasticity type.” We then tested whether plasticity type and stage-specific aggression varied with key performance metrics. About 40% of females decreased aggressiveness across consecutive breeding stages to some degree, consistent with population-level patterns. 33% of females exhibited comparatively little plasticity, with moderate to low levels of aggression in all stages. Finally, 27% of females displayed steep decreases and then increases in aggression between stages; females exhibiting this pattern had significantly lower body mass while parenting, they tended to hatch fewer eggs, and they had the lowest observed overwinter survival rates. Other patterns of among-stage changes in aggressiveness were not associated with performance. These results reveal substantial among-individual variation in behavioral plasticity, which may reflect diverse solutions to trade-offs between current reproduction and future survival.

Behavioral Responses to Touch and Leading in Lippizan Mares: Natural vs. Traditional Handling Method

Background: Proper handling and a well-established human-animal relationship influence both the behavior and the welfare of an animal. Methods: In this study, we compared the behavioral responses to touch and leading in mares using two handling methods. A traditional method (T) was based on forced cooperation and a natural (TTEAM) on tactile stimulation and mares’ natural behavior. Twenty-two group housed Lipizzan mares participated. Throughout four consecutive weeks, there were six observational days per method and based on a predefined ethogram, mares were scored daily on a 6-point scale. Higher scores indicated better reception of touch and leading, relaxation and cooperation, whereas lower scores indicated agonistic and/or fear-related behaviors. The time spent to implement touch and leading was also recorded. Result: Despite significant individual differences, touch and leading scores were found to be higher in the TTEAM compared to the T. Our results imply that mares were more relaxed, displayed better cooperation and had reduced agonistic and fear-related behavior during TTEAM. We suggest that implementation of TTEAM positively affected mares’ reception of touch and leading, but due to variation in behavioral plasticity, the importance of mare’s individuality is accentuated.

Boldness predicts plasticity in flight responses to winds.

Behavioural plasticity can allow populations to adjust to environmental change when genetic evolution is too slow to keep pace. However, its constraints are not well understood. Personality is known to shape individual behaviour, but its relationship to behavioural plasticity is unclear. We studied the relationship between boldness and behavioural plasticity in response to wind conditions in wandering albatrosses (Diomedea exulans). We fitted multivariate hidden Markov models to an 11-year GPS dataset collected from 294 birds to examine whether the probability of transitioning between behavioural states (rest, prey search and travel) varied in response to wind, boldness and their interaction. We found that movement decisions varied with boldness, with bolder birds showing preferences for travel, and shyer birds showing preferences for search. For females, these effects depended on wind speed. In strong winds, which are optimal for movement, females increased time spent in travel, while in weaker winds, shyer individuals showed a slight preference for search, while bolder individuals maintained preference for travel. Our findings suggest that individual variation in behavioural plasticity may limit the capacity of bolder females to adjust to variable conditions and highlight the important role of behavioural plasticity in population responses to climate change.

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

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

Context-dependent trait covariances: how plasticity shapes behavioral syndromes.

The study of behavioral syndromes aims to understand among-individual correlations of behavior, yielding insights into the ecological factors and proximate constraints that shape behavior. In parallel, interest has been growing in behavioral plasticity, with results commonly showing that animals vary in their behavioral response to environmental change. These two phenomena are inextricably linked—behavioral syndromes describe cross-trait or cross-context correlations, while variation in behavioral plasticity describes variation in response to changing context. However, they are often discussed separately, with plasticity analyses typically considering a single trait (univariate) across environments, while behavioral trait correlations are studied as multiple traits (multivariate) under one environmental context. Here, we argue that such separation represents a missed opportunity to integrate these concepts. Through observations of multiple traits while manipulating environmental conditions, we can quantify how the environment shapes behavioral correlations, thus quantifying how phenotypes are differentially constrained or integrated under different environmental conditions. Two analytical options exist which enable us to evaluate the context dependence of behavioral syndromes—multivariate reaction norms and character state models. These models are largely two sides of the same coin, but through careful interpretation we can use either to shift our focus to test how the contextual environment shapes trait covariances.

Yes, correct context is indeed the key: An answer to Haave-Audet et al. 2019.

We published a study recently testing the link between brain size and behavioural plasticity using brain size selected guppy (Poecilia reticulata) lines (2019, Journal of Evolutionary Biology, 32, 218-226). Only large-brained fish showed habituation to a new, but actually harmless environment perceived as risky, by increasing movement activity over the 20-day observation period. We concluded that "Our results suggest that brain size likely explains some of the variation in behavioural plasticity found at the intraspecific level". In a commentary published in the same journal, Haave-Audet et al. challenged the main message of our study, stating that (a) relative brain size is not a suitable proxy for cognitive ability and (b) habituation measured by us is likely not adaptive and costly. In our response, we first show that a decade's work has proven repeatedly that relative brain size is indeed positively linked to cognitive performance in our model system. Second, we discuss how switching from stressed to unstressed behaviour in stressful situations without real risk is likely adaptive. Finally, we point out that the main cost of behavioural plasticity in our case is the development and maintenance of the neural system needed for information processing, and not the expression of plasticity. We hope that our discussion with Haave-Audet et al. helps clarifying some central issues in this emerging research field.

The influence of environmental gradients on individual behaviour: Individual plasticity is consistent across risk and temperature gradients.

The expression of individual behaviour as a function of environmental variation (behavioural plasticity) is recognized as a means for animals to modify their phenotypes in response to changing conditions. Plasticity has been studied extensively in recent years, leading to an accumulation of evidence for behavioural plasticity within natural populations. Despite the recent attention given to studying individual variation in behavioural plasticity, there is still a lack of consensus regarding its causes and constraints. One pressing question related to this is whether individual plasticity carries over across temporal and environmental gradients. That is, are some individuals more plastic (responsive) than others in general? Here, we examined the influence of temporal and environmental gradients on individual behavioural responses in a marine gastropod, Littoraria irrorata. We measured individual boldness repeatedly over time and in response to tidal cycle (high vs. low, an index of risk) and daily temperature fluctuations (known to affect metabolism), in a controlled field experiment. On average, boldness increased from high to low tide and with increasing temperature but decreased marginally over time. Individuals also differed in their responses to variation in tide and temperature, but not over time. Those which were relatively bold at high tide (when predation risk is greater) were similarly bold at low tide, whereas shy individuals became much more "bold" at low tide. Most notably, individuals that were more responsive to tide (and thus risk) were also more responsive to temperature changes, indicating that plasticity was correlated across contexts (r=0.57) and that bolder individuals were least plastic overall. This study provides a rare and possibly first example of consistency of individual behavioural plasticity across contexts, suggesting underlying physiology as a common mechanism, and raises the possibility of correlational selection on plasticity.

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 20days 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.

Behavioural variation and plasticity along an invasive ant introduction pathway.

Once established in new areas, introduced species may exhibit changes in their biology due to phenotypic plasticity, novel selection pressures and genetic drift. Moreover, the introduction process itself has been hypothesised to act as a selective filter for traits that promote invasiveness. We tested the hypothesis that behaviours thought to promote invasiveness-such as increased foraging activity and aggression-are selected for during invasion by comparing traits among native and introduced populations of the widespread Argentine ant (Linepithema humile). We studied Argentine ant populations in the native range in Argentina and in three invaded regions along an introduction pathway: California, Australia and New Zealand. In each region, we set up 32 experimental colonies to measure foraging activity and interspecific aggression in a subset of the study regions. These colonies were subject to experimental manipulation of carbohydrate availability and octopamine, a biogenic amine known to modulate behaviour in insects, to measure variation in behavioural plasticity. We found variation in foraging activity among populations, but this variation was not consistent with selection on behaviour in relation to the invasion process. We found that colonies with limited access to carbohydrates exhibited unchanged exploratory behaviour, but higher exploitation activity and lower aggression. Colonies given octopamine consistently increased foraging behaviour (both exploration and exploitation), as well as aggression when also sugar-deprived. There was no difference in the degree of behavioural response to our experimental treatments along the introduction pathway. We did not find support for selection of behavioural traits associated with invasiveness along the Argentine ant's introduction pathway or clear evidence for an association between the introduction process and variation in behavioural plasticity. These results indicate that mechanisms promote behavioural variation in a similar fashion both in native and introduced ranges. Our results challenge the assumption that introduced populations always perform better in key behavioural traits hypothesised to be associated with invasion success.

Are some individuals generally more behaviorally plastic than others? An experiment with sailfin mollies.

Individuals within the same population generally differ among each other not only in their behavioral traits but also in their level of behavioral plasticity (i.e., in their propensity to modify their behavior in response to changing conditions). If the proximate factors underlying individual differences in behavioral plasticity were the same for any measure of plasticity, as commonly assumed, one would expect plasticity to be repeatable across behaviors and contexts. However, this assumption remains largely untested. Here, we conducted an experiment with sailfin mollies (Poecilia latipinna) whose behavioral plasticity was estimated both as the change in their personality traits or mating behavior across a social gradient and using their performance on a reversal-learning task. We found that the correlations between pairwise measures of plasticity were weak and non-significant, thus indicating that the most plastic individuals were not the same in all the tests. This finding might arise because either individuals adjust the magnitude of their behavioral responses depending on the benefits of plasticity, and/or individuals expressing high behavioral plasticity in one context are limited by neural and/or physiological constraints in the amount of plasticity they can express in other contexts. Because the repeatability of behavioral plasticity may have important evolutionary consequences, additional studies are needed to assess the importance of trade-offs between conflicting selection pressures on the maintenance of intra-individual variation in behavioral plasticity.

Experience during development triggers between-individual variation in behavioural plasticity.

Behavioural consistency within and across behaviours (animal personality and behavioural syndrome, respectively) has been vigorously studied in the last decade, leading to the emergence of "animal personality" research. It has been proposed recently that not only mean behaviour (behavioural type), but the environmentally induced behavioural change (behavioural plasticity) might also differ between individuals within populations. While case studies presenting between-individual variation in behavioural plasticity have started to accumulate, the mechanisms behind its emergence are virtually unknown. We have recently demonstrated that ecologically relevant environmental stimuli during ontogeny are necessary for the development of animal personality and behavioural syndromes. However, it is unknown whether between-individual variation in behavioural plasticity is hard-wired or induced. Here, we tested whether experience with predation during development affected predator-induced behavioural plasticity in Rana dalmatina tadpoles. We ran a common garden experiment with two ontogenetic predation treatments: tadpoles developed from hatching in either the presence or absence of olfactory predator stimuli. Then, we assayed all tadpoles repeatedly for activity and risk-taking both in the absence and presence of olfactory predator stimuli. We found that (a) between-individual variation in predator-induced behavioural plasticity was present only in the group that developed in the presence of olfactory stimuli from predators and (b) previous experience with predatory stimuli resulted in lower plastic response at the group level. The latter pattern resulted from increased between-individual variation and not from universally lower individual responses. We also found that experience with predation during development increased the predictability (i.e. decreased the within-individual variation unrelated to environmental change) of activity, but not risk-taking. In line with this, tadpoles developing under perceived predatory risk expressed their activity with higher repeatability. We suggest that ecologically relevant environmental stimuli are not only fundamental for the development of animal personality and behavioural syndromes, but also for individual variation in behavioural plasticity. Thus, experience is of central importance for the emergence of individual behavioural variation at many levels.

Is behavioural plasticity consistent across different environmental gradients and through time?

Despite accumulating evidence for individual variation in behavioural plasticity, there is currently little understanding of the causes and consequences of this variation. An outstanding question is whether individual reaction norm (RN) slopes are consistent across different environmental variables-that is, whether an individual that is highly responsive to one environmental variable will be equally responsive to a second variable. Another important and related question is whether RNs are themselves consistently expressed through time or whether they are simply state dependent. Here, we quantified individual activity rates of zebrafish in response to independent manipulations of temperature and food availability that were repeated in discrete 'bursts' of sampling through time. Individuals that were thermally responsive were not more responsive to food deprivation, but they did exhibit greater unexplained variation. Individual RN slopes were consistent (repeatable) over time for both temperature (Rslope = 0.92) and food deprivation responses (Rslope = 0.4), as were mean activity rates in the standard environment (Rintercept = 0.83). Despite the high potential lability of behaviour, we have demonstrated consistency of behavioural RN components and identified potential energetic constraints leading to high consistency of thermal RNs and low consistency of food deprivation RNs.

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 (>10m-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.

An experimental approach to the formation of diet preferences and individual specialisation in European mink

Individual dietary specialisation can occur within populations even when average diets suggest that the population has a generalist feeding strategy. Individual specialisation may impact fitness and has been related to demographic traits, ecological opportunity, competition, learning and animal personality. However, the causation and formation of individual specialisation are not fully understood. Experiments on animals raised in controlled environments provide an opportunity to examine dietary preferences and learning largely independent from variation in lifetime experiences and ecological opportunity. Here, we use a feeding experiment to examine individual specialisation and learning in captive bred European mink (Mustela lutreola) in an Estonian conservation programme. In a series of cafeteria experiments, animals could choose between one familiar food item (Baltic herring Clupea harengus membras) and two initially novel ones (noble crayfish Astacus astacus and house mouse Mus musculus). In general, mice were rarely eaten whilst crayfish consumption increased over time and fish decreased. At the individual level, there was a mix of generalists and crayfish or fish specialists, and the individuals differed in learning time in relation to novel prey. Our results indicate that individual variation in innate preferences and learning both contributes to individual diet specialisation. The differences in learning indicate individual variation in behavioural plasticity, which in turn can be related to personality. This could be of concern in conservation, as personality has been shown to affect survival in translocations.

Ambidextrous ungulates have more flexible behaviour, bolder personalities and migrate less.

Studies of wildlife have shown consistent individual variation in behavioural plasticity, which affects the rate of adaptation to changing environments. More flexible individuals may thus be more prone to habituation and conflict behaviour, but these applications of personality to wildlife management are little explored. Behavioural lateralization reflects cerebral specialization that may predict diverse expressions of behavioural plasticity. We recorded front-limb biases (i.e. handedness) in wild elk (Cervus canadensis), a species with facultative migration and high rates of habituation inside protected areas. Less lateralized elk responded more strongly to the application of aversive conditioning (predator-resembling chases by humans) by increasing their average flight response distances, but these same animals were also quicker to reduce their flight responses (i.e. habituate) when human approaches were benign. Greater laterality was correlated with, but not completely predicted by, bolder personalities, which we quantified via five correlated behavioural metrics. Lastly, lateralized elk were three times more likely to migrate, whereas less lateralized animals were similarly likely to remain near humans year-round. Lateralized behaviours can provide insight into behavioural flexibility enabling certain individuals to more quickly adapt to human-disturbed landscapes, and offer an especially productive arena for collaborative work by behaviourists, conservation biologists and wildlife managers.

Predation Risk Reduces a Female Preference for Heterospecific Males in the Green Swordtail

AbstractThe presence of a predator can result in the alteration, loss or reversal of a mating preference. Under predation risk, females often change their initial preference for conspicuous males, favouring less flashy males to reduce the risk of being detected by predators. Previous studies on predator‐induced plasticity in mate preferences have given females a choice between more and less conspicuous conspecific males. However, in species that naturally hybridize, it is also possible that females might choose an inconspicuous heterospecific male over a conspicuous conspecific male under predation risk. Our study addresses this question using the green swordtail (Xiphophorus helleri) and the southern platyfish (Xiphophorus maculatus), which are sympatric in the wild. We hypothesized that X. helleri females would prefer the sworded conspecific males in the absence of a predator but favour the less conspicuous, swordless, heterospecific males in the presence of a predator. Contrary to our expectation, females associated more with the heterospecific male than the conspecific male in the control (no predator) treatment, and they were non‐choosy in the predator treatment. This might reflect that females were attracted to the novel male phenotype when there was no risk of predation but became more neophobic after predator exposure. Regardless of the underlying mechanism, our results suggest that predation pressure may affect female preferences for conspecific versus heterospecific males. We also found striking within‐population, between‐individual variation in behavioural plasticity: females differed in the strength and direction of their preferences, as well as in the extent to which they altered their preferences in response to changes in perceived predation risk. Such variation in female preferences for heterospecific males could potentially lead to temporal and spatial variation in hybridization rates in the wild.

Behavioral plasticity is not significantly associated with head volume in a wild Chestnut Thrush (Turdus rubrocanus) population

The drivers of intraspecific variation in behavioral plasticity are poorly known. A widely held hypothesis is that brain size is positively correlated with behavioral plasticity. A total of 71 Chestnut Thrushes (Turdus rubrocanus) were caught in the wild population. We quantified behavior plasticity of activity of individuals measured in the same cage across two contexts (common and with a novel object stimulation), using a random regression analysis. We then investigated whether head volume (a proxy for brain size) was associated with behavioral plasticity in activity level using Spearman rank-order correlation. We found no significant evidence that activity plasticity was associated with relative head volume. There was no sex difference in head volume or in variance in head volume. We speculate that the absence of an association between brain volume and activity behavior plasticity may result from the inaccuracy of using external skull measurements to estimate brain size, or from a particular part of the brain being responsible for plasticity in activity level.

Variation in behavioural plasticity regulates consistent individual differences in Enallagma damselfly larvae

Plastic behavioural responses by individuals to different conditions and consistent individual differences in mean behaviour across situations both contribute to variation in a population. The relationship between behavioural plasticity and consistent individual differences is not clearly understood but may help predict personality variation in animals. High variation in mean behaviour and low variation in individual plastic responses will tend to maintain the rank order of individuals across situations and so permit consistent individual differences. Conversely, low variation in mean behaviour and high variation in plastic responses, by changing the rank orders of individuals, will erode consistent individual differences. Thus, selection that reduces variation in individual plastic responses should increase the opportunity for consistent individual differences in a population. We tested for relationships between heterogeneous predation regimes, the mean and variance of behavioural plasticity and consistent individual differences among three species groups of larval damselflies. Larvae of Enallagma signatum probably face consistent predation from fish over successive generations, whereas Enallagma ebrium/hageni and Enallagma annexum/boreale face a changing predation regime over generations either from fish or larval dragonflies. The behavioural reaction norms of larvae in repeated exposure trials to cues from a predatory fish, dragonfly larvae or no predator differed between species groups. Enallagma ebrium/hageni expressed the most consistent plastic response to predator cues, less variability in plasticity and greater consistent individual differences across cues compared to more variable plastic responses and low consistent individual differences in E. signatum. Selection on behavioural plasticity may enhance consistent individual differences in E. ebrium/hageni whereas relaxing selection on plasticity may reduce consistent individual differences in E. signatum. More generally, selection on plastic behaviour may enhance behavioural types while selection on mean behaviour may reduce behavioural types in animal populations.

No personality without experience? A test on Rana dalmatina tadpoles.

While the number of studies reporting the presence of individual behavioral consistency (animal personality, behavioral syndrome) has boomed in the recent years, there is still much controversy about the proximate and ultimate mechanisms resulting in the phenomenon. For instance, direct environmental effects during ontogeny (phenotypic plasticity) as the proximate mechanism behind the emergence of consistent individual differences in behavior are usually overlooked compared to environmental effects operating across generations (genetic adaptation). Here, we tested the effects of sociality and perceived predation risk during ontogeny on the strength of behavioral consistency in agile frog (Rana dalmatina) tadpoles in a factorial common garden experiment. Tadpoles reared alone and without predatory cues showed zero repeatability within (i.e., lack of personality) and zero correlation between (i.e., lack of syndrome) activity and risk-taking. On the other hand, cues from predators alone induced both activity and risk-taking personalities, while cues from predators and conspecifics together resulted in an activity - risk-taking behavioral syndrome. Our results show that individual experience has an unequivocal role in the emergence of behavioral consistency. In this particular case, the development of behavioral consistency was most likely the result of genotype×environment interactions, or with other words, individual variation in behavioral plasticity.

The interaction between genotype and juvenile and adult density environment in shaping multidimensional reaction norms of behaviour

Summary Both juvenile (Ej) and adult (Ea) environment can alter developmental trajectories, independently or interactively (as environment by environment interaction; Ej × Ea), to shape behaviour in later life. Within a population, however, the developmental response of behaviours to environments can vary among genotypes (G × E × E, multidimensional behavioural reaction norm). Here, we use a full‐sibling, split‐brood experimental design and random regression model to study genetic variation in behavioural plasticity across juvenile/adult density conditions in four behavioural traits of male water striders Tenagogerris euphrosyne: exploration, dispersal, same‐sex sexual behaviour and remounting attempts. Our results showed that both juvenile and adult density affected the expression of behaviours and that there was modest level of genetic variation in all behaviour traits. In contrast, there was little genetic variation in behavioural plasticity across density conditions at different life stages (G × Ej, G × Ea or G × Ej × Ea) observed in all traits other than same‐sex sexual behaviour. We suggest that experiences at different life stages can interact to affect behavioural expression, but the magnitude of G × Ej, G × Ea or G × Ej × Ea interactions depends on the specific traits. Lack of genetic variation in multidimensional behavioural reaction norm may be due to strong selection across environments, high environmental heterogeneity and/or modest genetic variance. Our results highlight the complex ways in which plasticity shapes the behaviours and life histories of organisms.