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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)...
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... our hypothesis was true, animal personality and behavioral syndromes should not emerge across individuals that were reared in isolation from conspecifics, predators, or para- sites, while receiving food and water ad libitum. As previ- ous studies showed that amphibians provide good models for behavioral consistency research ( Sih et al. 2003;Wilson and Krause 2012;Ursz an et al. 2015), we studied agile frog (Rana dalmatina Fitzinger in Bonaparte, 1839; Fig 1) tadpoles. We tested our hypothesis by assessing activity and risk-taking three times in tadpoles reared under different treatments. ...
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The existence of among-individual variation in behaviour within populations is poorly understood. Recent theory suggests that fine-scale individual differences in investment into current versus future reproduction may lead to a ‘slow-fast’-pace-of-life continuum, also referred to as the ‘pace-of-life-syndrome’ (POLS) hypothesis. According to this i...
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... In selection lines of slow and fast exploring great tits, sibling competition and food shortage had different effects on the development of exploration behaviour depending on the selection line, suggesting the combined importance of genetics, epigenetics and multiple developmental stressors in determining phenotype [68]. Furthermore, in tadpoles (Rana dalmatina), activity risk-taking behavioural syndromes emerged given joint exposure to conspecifics and predator cues, likely due to among-individual differences in developmental behavioural plasticity [69]. However, more multi-stress studies are needed to determine the importance of multi-stress effects to personality development. ...
... Few studies have quantified behavioural reaction norms across multi-stress gradients. Moreover, despite extensive literature regarding how developmental stress can affect behavioural phenotypes [69], how multi-stress effects might differ from single-stressor effects has rarely been explored. ...
Animal personality differences may have evolved as alternative strategies for negotiating multiple stressor landscapes. Indeed, ecologists are increasingly recognizing that interactions among multiple stressors can transform selective landscapes and behavioural and physiological responses to stress regimes. Yet, evaluating this hypothesis poses challenges, as most studies involving relationships between personality variation and the environment consider single stressors. Here, we review the literature to explore the theory and evidence that multiple stressor environments may mediate personality variation. We consider effects on evolution of personality variation, as influenced by life-history, energetic and behavioural trade-offs, and effects on phenotypic expression of personality traits. We then explore how personality variation may modulate behavioural and physiological responses to multiple stressors, and how differential responses may be affected by personality-dependent movement ecology and cognitive strategies. Among-individual differences in responses to multiple stressors are critical to elucidate, as multi-stress interactions may transform animal behavioural and physiological responses relative to those predicted under single stressor scenarios, and because among-individual variation comprises the basis for evolutionary shifts in stress responsiveness and population resiliency to global environmental change.
... Bell and Sih (2007) 10 quantified the relative influence of selection and plasticity, following predator exposure, on induction of a boldness/aggressiveness syndrome in adult sticklebacks; noteworthy, the sticklebacks did not change in boldness, just the syndrome became apparent. Urszan et al. (2015) 11 observed personality formation in tadpoles following experience with predator cues, though no real predation risk, early in life. Without early-life predator cue exposure, the tadpoles' behavioral traits were not repeatable, that is, the tadpoles did not show personalities. ...
... for fish and Urszan et al. (2015)11 for tadpoles, looked at experience-induced (Residence preference of IGP-naive and IGP-experienced females of P persimilis in three successive boldness tests, each representing a different context In each test, each female was given a choice between safe and risky sites in an acrylic T-maze cage. Thick horizontal lines are the medians, pluses show the means, boxes represent the interquartile range, whiskers extend to minimum and maximum values, light gray dots are the individual data points. ...
Animal personalities are defined by within-individual consistency, and consistent among-individual variation, in behavior across time and/or contexts. Here we hypothesized that brief early-life experience of intraguild predation (IGP) risk has enduring phenotypic effects on personality expression in boldness and aggressiveness in later life. We tested our hypothesis in predatory mites Phytoseiulus persimilis, which are IG predators with ontogenetic role reversals, i.e. they are potential IG prey during early life but IG predators as adults. Adult P. persimilis females, which had experienced IGP risk early in life or not, were subjected to three tests each for boldness and aggressiveness. IGP-experienced individuals were on average bolder and more aggressive. Boldness was moderately repeatable, aggressiveness was weakly repeatable. Strikingly, early-life IGP experience shifted the within-group personality composition towards consistently bold and aggressive personalities. Phenotypic adjustment of personality expression was adaptive, as indicated by the positive correlation between personality scores and egg production.
... This is because novel and risky contexts may result in potentially bolder or more cautious behaviors compared to familiar, low risk contexts (Carter et al. 2013;Perals et al. 2017;Kelleher et al. 2018). An individual's perception of risk may further be dependent on the extent and type of competition they are exposed to during development (Urszán et al. 2015;Han and Dingemanse 2017;He et al. 2017;Castellano et al. 2022). Increased competition for resources may mean that individuals which are in greater need of resources may be prepared to take more risks and travel further distances in unfamiliar contexts Houston 1987, 1994;Werner 1995, 1998). ...
... The superior competitive ability of L. fuscus is thought to be attributed to its larger starting size and higher activity rates (Downie and Nokhbatolfoghahai 2006;Downie et al. 2008). Amphibian larvae represent an ideal life stage and group of organisms in which to investigate the effects of competition on animal personality and behavioral syndromes (Urszán et al. 2015(Urszán et al. , 2018Castellano et al. 2022). Across a variety of species, tadpoles compete with both conspecifics and heterospecifics for access to resources to fuel fast growth and development prior to metamorphosis and many of these interactions involve asymmetrical competition between species (Werner 1992;Bardsley and Beebee 2001;Richter-Boix et al. 2004, 2007Smith et al. 2004;Ramamonjisoa and Natuhara 2017;Castellano et al. 2022). ...
Repeated social interactions with conspecifics and/or heterospecifics during early development may drive the differentiation of behavior among individuals. Competition is a major form of social interaction and its impacts can depend on whether interactions occur between conspecifics or heterospecifics and the directionality of a response could be specific to the ecological context that they are measured in. To test this, we reared tungara frog tadpoles (Engystomops pustulosus) either in isolation, with a conspecific tadpole or with an aggressive heterospecific tadpole, the whistling frog tadpole (Leptodactylus fuscus). In each treatment, we measured the body size and distance focal E. pustulosus tadpoles swam in familiar, novel and predator risk contexts six times during development. We used univariate and multivariate hierarchical mixed effect models to investigate the effect of treatment on mean behavior, variance among and within individuals, behavioral repeatability and covariance among individuals in their behavior between contexts. There was a strong effect of competition on behavior, with different population and individual level responses across social treatments. Within a familiar context, the variance in the distance swam within individuals decreased under conspecific competition but heterospecific competition caused more variance in the average distance swam among individuals. Behavioral responses were also context specific as conspecific competition caused an increase in the distance swam within individuals in novel and predator risk contexts. The results highlight that the impact of competition on among and within individual variance in behavior is dependent on both competitor species identity and context.
... Physiological changes that occur as an organism develops and grows (e.g., changes in hormonal levels and/or metamorphosis) may drive shifts in behavioral patterns, especially during the transition between stages of the life cycle, such as reaching sexual maturity (Bell and Stamps 2004;Stamps and Groothuis 2010;Wilson and Krause 2012). Furthermore, the environmental cues to which an individual is exposed to throughout development, such as climate, predation risk, or food availability, can influence behavioral type Bell and Sih 2007;Pinter-Wollman et al. 2012a, b;Stahlschmidt et al. 2014;Urszán et al. 2015). ...
Behavioral shifts in animals are often driven by ontogenetic processes such as aging or life experiences, through changes in their physiology and/or gene expression. Colonies of eusocial animals such as social hymenopterans may experience behavioral shifts at the colony-level due to maturation and/or experience throughout the colony cycle. In this study, we investigated the nest defense behavior of social wasp Vespula vulgaris colonies and whether behavioral changes over time or differences in experience with simulated threats can affect aggressive response. Colonies were divided into two treatment groups and experimentally disturbed over a seven-week period by simulating a mammal attack. This procedure was carried out for “hi-freq” colonies on a weekly basis (weeks 1–6), whereas “lo-freq” groups were disturbed once every three weeks (weeks 1, 3, and 7). We show that nest defense behavior in V. vulgaris decreases over time, towards the end of the colony cycle, regardless of how frequently they faced a simulated predator attack. We found no evidence that undisturbed foraging activity or nest size could be used to predict defensive behavior. Our results show anti-predator colony behaviors in Vespula are influenced by the colony cycle, possibly through demographic shifts over time: colonies near their decline are less likely to respond to a simulated threat when compared to earlier in the season. We propose colony behavior is strongly engrained in seasonality and internal development, to a degree that it might overrule the effect of interactions with potential predators.
... Additional studies on anuran activity have been largely restricted to the larval stage (e.g., Urszán et al., 2015) and, in one case, extended to metamorphosis (Wilson & Krause, 2012). As dispersal typically takes place post-metamorphosis and movement patterns differ in aquatic versus terrestrial habitats, it remains unclear the extent to which personalities can drive movement patterns of adult terrestrial amphibians within and between habitats (Kelleher et al., 2018). ...
Dispersive movements are often thought to be multicausal and driven by individual body size, sex, conspecific density, environmental variation, personality, and/or other variables. Yet such variables often do not account for most of the variation among dispersive movements in nature, leaving open the possibility that dispersion may be indeterministic. We assessed the amount of variation in 24 h movement distances that could be accounted for by potential drivers of displacement with a large empirical dataset of movement distances performed by Fowler's Toads (Anaxyrus fowleri) on the northern shore of Lake Erie at Long Point, Ontario (2002-2021, incl.). These toads are easy to sample repeatedly, can be identified individually and move parallel to the shoreline as they forage at night, potentially dispersing to new refuge sites. Using a linear mixed-effect model that incorporated random effect terms to account for sampling variance and inter-annual variation, we found that all potential intrinsic and extrinsic drivers of movement accounted for virtually none of the variation observed among 24 h distances moved by these animals, whether over short or large spatial scales. We examined the idea of movement personality by testing variance per individual toad and found no evidence of individuality in movement distances. We conclude that deterministic variables, whether intrinsic or extrinsic, neither can be shown to nor are necessary to drive movements in this population over all spatial scales. Stochastic, short time-scale movements, such as daily foraging movements, can instead accumulate over time to produce large spatial-scale movements that are dispersive in nature.
... Previous studies have found impacts of developmental environments on repeatability in behavior. For example, agile frog tadpoles, Rana dalmatina, only had significant repeatability in risk-taking behavior when reared in an environment containing predator scent (Urszan et al. 2015). Similarly, DiRienzo et al. (2015) found that early exposure to pathogens resulted in lower repeatability in some boldness measures in field crickets, Gryllus integer. ...
... For example, work on Drosophila (Sokolowski 2001), zebrafish, Danio rerio (Norton et al. 2011), and bighorn ewes, Ovis canadensis (Dingemanse and Réale 2005), support a strong genetic basis for behavioral syndromes. In contrast, support for environmental effects and instability within short time periods has been seen in agile frog tadpoles, R. dalmatina (Urszan et al. 2015) and three-spined sticklebacks, Gasterosteus aculeatus (Bell and Sih 2007;Dingemanse et al. 2007). If the latter is the case, it would suggest that developmental environments could shape these between-individual correlations, although our understanding of how these early environments affect behavioral syndromes is still limited (Han and Dingemanse 2015;Royauté and Dochtermann 2017). ...
... In this species, incubation temperature was found to affect dessication rate and short-term critical thermal minima (Llewelyn et al. 2018), but effects of incubation temperature on behavior have not yet been investigated. Furthermore, while no behavioral syndrome has yet been found in captive-reared southern rainforest sunskinks (Goulet et al. 2021), previous studies have suggested that natural environments may be necessary to generate and maintain repeatability in, and correlations between, behavioral traits (Wilson et al. 1994;Urszan et al. 2015). As such, a secondary aim of our study was to investigate if skinks that had developed in captivity differed in animal personality from those that had developed in the wild. ...
Developmental environments play a significant role in shaping animal phenotype, including behavior. Within a species, individuals often differ in behavior in a consistent and repeatable way (i.e., demonstrate animal personality). This consistency in behavior can be affected by differences in conditions experienced early in life. It is, however, unclear whether effects of developmental environments on animal personality are driven by changes in within- or between-individual variation. To investigate this, we measured activity, exploration, sociability, and boldness in adult male southern rainforest sunskinks, Lampropholis similis, incubated at either 23 °C or 26 °C, and compared behavioral phenotypes between these incubation treatments. We also compared the behavior of these incubation groups to a cohort of wild-caught skinks to determine whether rearing in captivity also affected the personality of the lizards. Skinks that had been incubated at a higher temperature were more explorative and demonstrated personality in a larger suite of traits compared to lizards incubated at a lower temperature or caught in the wild. These differences among developmental environment were primarily driven by within-individual variation, which tended to be higher among the high incubation treatment. We also found no evidence for a behavioral syndrome in either captive- or wild-reared skinks. Our results suggest the potential for greater behavioral plasticity in skinks incubated at a higher temperature, which may enable them to cope with environmental change, such as climate warming, in the short term. Overall, we show that effects of developmental environment are complex and play a pivotal role in shaping animal personality.
Significance statement
Experiences during development are expected to influence how animals develop, including their behavior. We tested early environment effects on behavior in adult southern rainforest sunskinks by comparing lizards incubated at different temperatures as well as comparing those reared in the wild with those reared in captive environments. We found that lizards incubated at the higher temperature were more exploratory. Furthermore, both incubation temperature and captivity/wild-rearing had pronounced effects on the consistency of behavior—in different directions for different traits—demonstrating developmental environments have strong effects on animal personality. Such changes in behavioral traits likely have flow-on effects for the animal’s fitness and biotic interactions.
... Additional studies on anuran activity have been largely restricted to the larval stage (e.g., Urszán et al., 2015) and, in one case, extended to metamorphosis (Wilson & Krause, 2012). As dispersal typically takes place post-metamorphosis and movement patterns differ in aquatic versus terrestrial habitats, it remains unclear the extent to which personalities can drive movement patterns of adult terrestrial amphibians within and between habitats (Kelleher et al., 2018). ...
Dispersive movements are often thought to be multiclausal and driven by individual body size, sex, conspecific density, environmental variation and/or other factors. Yet such factors rarely account for most of the variation present among dispersive movements in nature, leaving open the possibility that dispersion might be indeterministic and vary in response to environmental stochasticity. We assessed the amount of variation in movement distances that could be accounted for by potential predictors of dispersal with a large empirical dataset of movement distances performed by Fowler’s Toads (Anaxyrus fowleri) on the northern shore of Lake Erie at Long Point, Ontario (2002 – 2021, incl.). These toads are easy to sample repeatedly, can be identified individually and undertake dispersive movements parallel to the shoreline on a daily basis as they forage at night. Using a linear mixed-effect model that incorporated random effect terms to account for sampling variance and inter-year environmental variation, we found that all potential predictors of dispersive movements of these animals were, at best, weak predictors that accounted for virtually none of the variation observed among movement distances. We also used linear regression models to test for the impact of environmental stochasticity on dispersive movements and identified a strong positive correlation between the distribution of toad movement distances and variability in lake water level. We conclude that deterministic proximal factors, whether intrinsic or extrinsic, neither can be shown nor are necessary to drive dispersive movements in this population. Variation in dispersive movements can be ascribed, instead, to environmental unpredictability, consistent with nomadism.
... Only one of three measured behaviors of wood frogs in our study changed in response to exposure to oil-contaminated water. Sociality and space use have been found to be repeatable in amphibian larvae, suggesting that these risk-taking personality traits should be related to activity (Carlson and Langkilde, 2013;Urszan et al., 2015). Perhaps the sample size did not provide sufficient statistical power to detect the effect of oil exposure on sociality and space use. ...
... Perhaps the sample size did not provide sufficient statistical power to detect the effect of oil exposure on sociality and space use. Further, the absence of predators in our study may have contributed, as repeatable behaviors are more likely to exhibit high interindividual variation in the presence of predator cues (Urszan et al., 2015). ...
The risks to aquatic wildlife from spills of diluted bitumen (dilbit) into inland waters are poorly understood. In this paper, we describe the response of larval wood frogs (Rana sylvatica) to hydrocarbons and other compounds released from experimental spills of dilbit in a temperate boreal lake. To simulate a wide range of environmentally relevant oil spill scenarios, different volumes of Cold Lake Winter Blend dilbit (0, 1.5, 2.9, 5.5, 18, 42, 82, and 180 L) were added to 10-m diameter in-lake limnocorrals. Larvae (n = 360) were reared (from Gosner Stage (GS) 25 to ∼42) in land-based aquatic microcosms, where they were first exposed to clean water during a 2-week baseline phase, and then (at GS ∼30), to contaminated water withdrawn from the limnocorrals for 3 weeks. We observed no statistically significant trends in survival, growth, or development of larvae as a consequence of exposure to the chemical compounds released from naturally weathered dilbit. Likewise, cytochrome P450 1A biomarkers or levels of thyroid hormones in wood frogs near metamorphic climax were not related to volume of the oil spills. However, there was a modest statistically significant decrease in larval activity (up to 8.7% relative to the control), but no change in other behavioural metrics (sociality or space use). Our work adds to the limited body of literature on the effects of unconventional oils on aquatic wildlife and helps to inform risk assessments regarding pipeline projects.
... After the boldness assay, we returned the tadpoles to their respective mesocosms. Thus, we cannot rule out the possibility that any individual tadpole was also sampled for a boldness assay at a different age, and we acknowledge that recurrent behavioral testing can influence tadpole behavior in later trials (Urszán et al. 2015a). However, given the high initial number of tadpoles per mesocosm (n = 1000), there is Table 1 The number of tadpoles whose boldness was assayed in our study, separated by age and origin population. ...
Animals are increasingly challenged to respond to novel or rapidly changing habitats due to urbanization and/or displacement
outside their native range by humans. Behavioral differences, such as increased boldness (i.e., propensity for risk-taking),
are often observed in animals persisting in novel environments; however, in many cases, it is unclear how these differences
arise (e.g., through developmental plasticity or evolution) or when they arise (i.e., at what age or developmental stage). In
the Guttural Toad (Sclerophrys gutturalis), adult urban toads from both native and invasive ranges are bolder than conspe-
cifics in natural habitats. Here, we reared Guttural Toad tadpoles in a common garden experiment, and tested for innate
differences in boldness across their development and between individuals whose parents and lineage came from rural-native,
urban-native, and urban-invasive localities (i.e., origin populations). Tadpoles did not differ in their boldness or in how their
boldness changed over ontogeny based on their origin populations. In general, tadpoles typically became less bold as they
aged, irrespective of origin population. Our findings indicate that differences in boldness in free-living adult Guttural Toads
are not innate in the tadpole stage and we discuss three possible mechanisms driving phenotypic divergence in adult boldness
for the focus of future research: habitat-dependent developmental effects on tadpole behavior, decoupled evolution between
the tadpole and adult stage, and/or behavioral flexibility, learning, or acclimatization during the adult stage.
... These findings indicate that the fearful/anxiety trait was plastically altered by daily threatening experiences. Such behavioral plasticity has been observed in fish (Smith and Blumstein 2012;Takahashi et al. 2013;Moscicki and Hurd 2015), amphibians (Urszán et al. 2015;Chivers et al. 2016), reptiles (López et al. 2005), and mammals (Hurst & West 2010). Empirical studies suggest that behavioral plasticity is formed through daily fearful experiences among individuals in diverse taxa. ...
Behavioral variation in animals is often influenced by experience. Previous studies have found that daily threatening experiences can enhance fear- and anxiety-like behaviors in some vertebrates. However, it is unclear whether the change in fear/anxiety behavior occurs in invertebrates. The present study investigated whether fear/anxiety behavior could be affected by a net-chasing treatment in two shrimp species (Neocaridina denticulata ssp. and Palaemon pacificus). The net-chasing treatment was repeated for 8 days to simulate daily predator experiences, and behavioral tests (open-field, shelter-seeking, and escape-response tests) were conducted on the day following the last day of treatment. Net-chased N. denticulata ssp. displayed a tendency to remain near a wall compared with the control in the open-field test, whereas net-chased P. pacificus shrimps demonstrated greater escape behavior compared with the control in the escape-response test. These results suggest that fear/anxiety behavior for both shrimp species can be affected by the net-chasing treatment, although the pattern of behavioral change differed between the two species. The findings suggest that daily threatening experiences change the behavior of shrimp and cause them to select a regular avoidance strategy when they encounter risks and unknown situations.
