Marcus Michelangeli

Are behavioural syndromes sex specific? Personality in a widespread lizard species

Understanding how and why consistent behavioural traits (i.e. animal personality) vary between individuals, and identifying the mechanisms that underlie such variation, is a key focus in behavioural and evolutionary ecology. In many animals, male and female behaviour often diverges in response to different selection pressures and life history trajectories post-maturation. Despite this, animal personality studies spanning several personality traits rarely consider both sexes, ignoring the very strong possibility that key components of personality, behavioural consistency and behavioural correlations, may vary between males and females. Furthermore, such variation can play an important role in ecological processes such as mediating the invasion propensity of a species. Here, we took an animal personality approach to studying the behaviour of a repeatedly successful invasive species, the delicate skink (Lampropholis delicata). We investigated whether male and female delicate skinks differed in their personality across five behavioural traits, as sex differences in behaviour could provide a mechanism that explains the delicate skink’s successful invasion history via accidental introductions. We found that females were more social than males and showed a trend towards being faster explorers. Both sexes shared the same behavioural syndrome suggesting that it is evolutionarily stable and not easily decoupled by selection. Specifically, skinks that were consistently more active explored environments faster and were more likely to bask with other skinks. In sum, we found limited evidence of sex-specific personality in the delicate skink suggesting that both sexes might have an equal invasion potential. More broadly, our study highlights the need to consider whether, in fact, differences in personality are important in mediating a species propensity to invade.Significance statementMales and females likely differ in their personality because they often face different selection pressures when they are adults. An individual’s personality may also determine how likely they are to invade novel environments. Thus, we compared personality traits of males and females in an invasive species, the delicate skink, for what it may reveal about the potential mechanisms that drive the species successful invasion history. We found that females were more social and showed a trend towards being faster explorers than males. Both sexes had positive correlations between activity, exploratory and social behaviour suggesting the presence of a non-sex-specific behavioural syndrome. Our results suggest limited behavioural variation between the sexes and that both sexes may have an equal invasion potential.

Thermal physiology: A new dimension of the pace-of-life syndrome

Current syndrome research focuses primarily on behaviour with few incorporating components of physiology. One such syndrome is the pace-of-life syndrome (POLS) which describes covariation between behaviour, metabolism, immunity, hormonal response, and life-history traits. Despite the strong effect temperature has on behaviour, thermal physiology has yet to be considered within this syndrome framework. We proposed the POLS to be extended to include a new dimension, the cold-hot axis. Under this premise, it is predicted that thermal physiology and behaviour would covary, whereby individual positioning along the thermal continuum would coincide with that of the behavioural continuum. This hypothesis was tested by measuring thermal traits of delicate skinks (Lampropholis delicata) and linking it to their behaviour. Principal components analysis and structural equation modelling were used to determine if traits were structured within the POLS and to characterize the direction of their interactions. Model results supported the inclusion of the cold-hot axis into the POLS and indicated that thermal physiology was the driver of this relationship, in that thermal traits either constrained or promoted activity, exploration, boldness and social behaviour. This study highlights the need to integrate thermal physiology within a syndrome framework.

An endocrine-disrupting agricultural contaminant impacts sequential female mate choice in fish

The environmental impact of endocrine-disrupting chemicals (EDCs)-compounds that interfere with endocrine system function at minute concentrations-is now well established. In recent years, concern has been mounting over a group of endocrine disruptors known as hormonal growth promotants (HGPs), which are natural and synthetic chemicals used to promote growth in livestock by targeting the endocrine system. One of the most potent compounds to enter the environment as a result of HGP use is 17β-trenbolone, which has repeatedly been detected in aquatic habitats. Although recent research has revealed that 17β-trenbolone can interfere with mechanisms of sexual selection, its potential to impact sequential female mate choice remains unknown, as is true for all EDCs. To address this, we exposed female guppies (Poecilia reticulata) to 17β-trenbolone at an environmentally relevant level (average measured concentration: 2 ng/L) for 21 days using a flow-through system. We then compared the response of unexposed and exposed females to sequentially presented stimulus (i.e., unexposed) males that varied in their relative body area of orange pigmentation, as female guppies have a known preference for orange colouration in males. We found that, regardless of male orange pigmentation, both unexposed and exposed females associated with males indiscriminately during their first male encounter. However, during the second male presentation, unexposed females significantly reduced the amount of time they spent associating with low-orange males if they had previously encountered a high-orange male. Conversely, 17β-trenbolone-exposed females associated with males indiscriminately (i.e., regardless of orange colouration) during both their first and second male encounter, and, overall, associated with males significantly less than did unexposed females during both presentations. This is the first study to demonstrate altered sequential female mate choice resulting from exposure to an endocrine disruptor, highlighting the need for a greater understanding of how EDCs may impact complex mechanisms of sexual selection.

Aggression mediates dispersal tendency in an invasive lizard

Personality-dependent dispersal is a key ecological and evolutionary process that is likely to facilitate the successful movement and colonization/invasion success of species. This dispersal syndrome suggests that dispersers should possess a suite of behavioural tendencies that differ from those of nondispersers, thus influencing the composition of populations in the new range and, ultimately, colonization success. However, dispersal is also often condition dependent, and is probably mediated by the interaction between an individuals personality and environmental and social factors such as competition. Accordingly, we investigated whether dispersal tendency was linked to an activity, exploration and social syndrome and/or aggression in a reptile, the delicate skink, Lampropholis delicata, which has had a successful invasion history via accidental introductions. Contrary to our prediction, we found that dispersal was not related to activity, exploration or social personality traits. Instead, dispersal tendency was associated with aggression: the most aggressive individuals dispersed further and faster than less aggressive individuals. The presence of aggression-dependent dispersal could be due to either (1) dispersers generally being more aggressive than nondispersers or (2) aggressive individuals forcing nonaggressive individuals into hiding, thus impinging on the ability of subordinates to disperse regardless of their personality. Our study highlights the need to consider the ecological context when examining personality-dependent dispersal and suggests that aggression and the social environment can play an important role in dispersal decisions.

Does personality influence learning? A case study in an invasive lizard

Learning is a change in state resulting from new experiences enabling behavioural responses to be adjusted in alignment with external cues. Individuals differ in the speed and accuracy at which they learn. Personality has been postulated as being a major influence on learning ability in terms of attention and encounter rates of environmental cues. This link forms the basis of the cognitive style hypothesis (CSH), predicting that an individual’s cognitive style will occur along a fast–slow behavioural gradient. Fast types are characterised as being active, neophilic, and bold individuals who sample their environment rapidly, yet superficially, enabling learning to occur at a higher speed, but at the cost of accuracy. Slow types have the opposite suite of personality traits resulting in them being more accurate flexible learners. Greater level of learning flexibility is thought to help promote invasions success. Here, we test the predictions of the CSH in an invasive lizard (Lampropholis delicata) to determine if personality dictates learning performance in a two-phase associative task. Results indicated that the delicate skink was capable of learning an associative task but only provided partial support for the CSH. Personality was found to influence learning accuracy, however, the direction of that relationship was opposite to that predicted. Instead, fast lizards made fewer mistakes when learning to associate a colour to a goal. These findings highlight the need to further investigate the CSH across taxa and consider its potential as an underlying mechanism of the invasion process.

Impact of the widespread pharmaceutical pollutant fluoxetine on behaviour and sperm traits in a freshwater fish

Pharmaceutical pollutants are detected in aquatic habitats and wildlife tissues globally. One widespread contaminant of major concern is the antidepressant fluoxetine, which can affect behavioural and physiological processes in non-target species. Despite this, effects of fluoxetine on wildlife behaviour have seldom been investigated across multiple fitness-related contexts, especially at environmentally realistic concentrations. Accordingly, we examined impacts of 35-day fluoxetine exposure at two environmentally relevant concentrations (31 and 374 ng/L) across a suite of fitness-related contexts in wild-caught male mosquitofish (Gambusia holbrooki). First, we investigated anxiety-related behaviours (boldness, exploration and activity) in a novel environment (maze arena) and found no significant impacts of exposure. Second, we tested effects of fluoxetine in a reproductive context, including mating behaviour and sperm quality. We found that, relative to controls, fluoxetine exposure resulted in males spending a greater amount of time pursuing females. Further, low-exposed males were more likely to attempt copulation than unexposed males. Lastly, we investigated across-context behavioural correlations, and how fluoxetine exposure might affect such relationships. A significant positive correlation was detected in control fish between activity levels in the maze and time spent pursuing females in the reproductive assay. This relationship was disrupted by fluoxetine at both exposure levels. This is the first evidence that field-detected concentrations of a pharmaceutical pollutant can disturb across-context behavioural correlations in wildlife. Our findings provide clear evidence that fluoxetine can produce context-specific behavioural effects in fish and underscore how pharmaceutical exposure at field-detected concentrations can induce important shifts in wildlife behaviour.

Integrating thermal physiology within a syndrome: Locomotion, personality and habitat selection in an ectotherm

1. Physiology and temperature can both have a profound influence on behaviour and metabolism. Despite this, thermal physiology has rarely been considered within the animal personality framework, but could be an inherent mechanism maintaining consistent individual differences in behaviour, particularly in species that need to thermoregulate (i.e. ectotherms). 2. Here, we present evidence for a thermal-behavioural syndrome and detail how it is linked to variation in habitat selection in an Australian lizard, the delicate skink, Lampropholis delicata. 3. We predicted that individuals would occur along a cold-hot continuum – analogues to the slow-fast continuum proposed by the pace-of-life hypothesis - whereby an individual’s placement along a thermal physiological axis will correspond with their placement along a personality axis. We first tested the thermal-behavioural syndrome by measuring the thermal preferences and optimal performance temperature of individual skinks and linking it to their activity, exploratory, social and boldness behaviours. 4. In line with our predictions, we found that individuals with a ‘hot’ thermal type performed optimally at higher temperatures, had faster sprint speeds and were more active, explorative and bold relative to ‘cold’ thermal types. 5. We then monitored each individual’s habitat selection within an artificial environment containing three microhabitats differing in their thermal characteristics. 6. We found that an individual’s thermal type mediated their use of habitat, in which ‘hot’ individuals utilised a hotter microhabitat more regularly than both ‘cold’ and ‘intermediate’ thermal types, suggesting that the thermal-behavioural syndrome could drive ecological niche partitioning in this species. 7. We envisage that the thermal-behavioural syndrome concept is likely to extend to other study systems, particularly to ectothermic organisms that rely heavily on behavioural thermoregulation to maintain optimal body temperature.

Evaluating cognition and thermal physiology as components of the pace-of-life syndrome

The pace-of-life syndrome (POLS) suggests that behavioral traits are correlated and integrate within a fast–slow physiological continuum. At the fast extreme, individuals having higher metabolic rates are more active, exploratory, and bold with the opposite suite of traits characterizing those at the slow physiological extreme. A recent framework suggests that behavioral types may also differ consistently in their cognitive style. Accordingly, we propose that cognition could be further incorporated into the POLS framework comprised of behavioral and thermal physiological traits. Under this premise, fast behavioral types having high thermal traits are predicted to acquire a novel task faster but at the cost of accuracy while slow behavioral types with low thermal traits would be more attentive, responding to cues at a slower rate leading to higher accuracy and flexibility. This was tested by measuring physiological and behavioral traits in delicate skinks (Lampropholis delicata) and testing their learning ability. Correlations were detected between cognition and behavior but not thermal physiology. Contrary to our predictions, individual positioning along these axes opposed our predicted directions along the fast–slow continuum. Fast lizards preferring lower body temperatures expressed higher activity, exploration, sociality, and boldness levels, and learned the discrimination learning task at a slower rate but made the most errors. Additionally, modelling results indicated that neither thermal physiology, behavior, or their interaction influenced cognitive performance. Although the small number of animals completing the final stages of the learning assays limits the strength of these findings. Thus, we propose that future research involving a greater sample size and number of trials be conducted so as to enhance our understanding into how the integration of cognitive style, behavior, and physiology may influence individual fitness within natural populations.

Field-realistic exposure to the androgenic endocrine disruptor 17β-trenbolone alters ecologically important behaviours in female fish across multiple contexts

The capacity of pharmaceutical pollution to alter behaviour in wildlife is of increasing environmental concern. A major pathway of these pollutants into the environment is the treatment of livestock with hormonal growth promotants (HGPs), which are highly potent veterinary pharmaceuticals that enter aquatic ecosystems via effluent runoff. Hormonal growth promotants are designed to exert biological effects at low doses, can act on physiological pathways that are evolutionarily conserved across taxa, and have been detected in ecosystems worldwide. However, despite being shown to alter key fitness-related processes (e.g., development, reproduction) in various non-target species, relatively little is known about the potential for HGPs to alter ecologically important behaviours, especially across multiple contexts. Here, we investigated the effects of exposure to a field-realistic level of the androgenic HGP metabolite 17β-trenbolone-an endocrine-disrupting chemical that has repeatedly been detected in freshwater systems-on a suite of ecologically important behaviours in wild-caught female eastern mosquitofish (Gambusia holbrooki). First, we found that 17β-trenbolone-exposed fish were more active and exploratory in a novel environment (i.e., maze arena), while boldness (i.e., refuge use) was not significantly affected. Second, when tested for sociability, exposed fish spent less time in close proximity to a shoal of stimulus (i.e., unexposed) conspecific females and were, again, found to be more active. Third, when assayed for foraging behaviour, exposed fish were faster to reach a foraging zone containing prey items (chironomid larvae), quicker to commence feeding, spent more time foraging, and consumed a greater number of prey items, although the effect of exposure on certain foraging behaviours was dependent on fish size. Taken together, these findings highlight the potential for exposure to sub-lethal levels of veterinary pharmaceuticals to alter sensitive behavioural processes in wildlife across multiple contexts, with potential ecological and evolutionary implications for exposed populations.