scholarly journals Stress activity is not predictive of coping style in North American red squirrels

2018 ◽  
Author(s):  
Sarah E. Westrick ◽  
Freya van Kesteren ◽  
Rupert Palme ◽  
Rudy Boonstra ◽  
Jeffery E. Lane ◽  
...  

AbstractIndividuals vary in their behavioral and physiological responses to environmental changes. These behavioral responses are often described as ‘coping styles’ along a proactive-reactive continuum. Studies in laboratory populations often, but not always, find that behavioral responses and physiological responses to stressors covary, where more proactive (more aggressive and active) individuals have a lower physiological stress response, specifically as measured by hypothalamic-pituitary-adrenal (HPA) axis activity. These studies support the possibility of hormonal pleiotropy underlying the presentation of behaviors that make up the proactive-reactive phenotype. However, recent research in wild populations is equivocal, with some studies reporting the same pattern as found in many controlled laboratory studies, whereas others do not. We tested the hypothesis that physiological and behavioral stress responses are correlated in wild adult North American red squirrels (Tamiasciurus hudsonicus). We used fecal cortisol metabolites (FCMs) as a non-invasive, integrated estimate of circulating glucocorticoids for our measurement of HPA axis activity. We found that FCM concentrations were not correlated with three measures of behavioral coping styles (activity, aggression, and docility) among individuals. This does not support the hypothesis that hormonal pleiotropy underlies a proactive-reactive continuum of coping styles. Instead, our results support the “two-tier” hypothesis that behavioral and physiological stress responses are independent and uncorrelated traits among individuals in wild populations that experience naturally varying environments rather than controlled environments. If also found in other studies, this may alter our predictions about the evolutionary consequences of behavioral and endocrine coping styles in free-living animals.Significance StatementIndividuals vary in how they respond to stressors through behavior and physiology, but we find the two responses are independent in wild animals. Many laboratory studies find links between the behavioral and physiological stress responses, however studies conducted with wild populations are less conclusive. In wild North American red squirrels, independence between the physiological response and behavioral response may allow adaptive responses to a changing environment without pleiotropic constraint.

2019 ◽  
Vol 30 (4) ◽  
pp. 1030-1040 ◽  
Author(s):  
Matt Sehrsweeney ◽  
David R Wilson ◽  
Maggie Bain ◽  
Stan Boutin ◽  
Jeffrey E Lane ◽  
...  

AbstractAcoustic signaling is an important means by which animals communicate both stable and labile characteristics. Although it is widely appreciated that vocalizations can convey information on labile state, such as fear and aggression, fewer studies have experimentally examined the acoustic expression of stress state. The transmission of such public information about physiological state could have broad implications, potentially influencing the behavior and life-history traits of neighbors. North American red squirrels (Tamiasciurus hudsonicus) produce vocalizations known as rattles that advertise territorial ownership. We examined the influence of changes in physiological stress state on rattle acoustic structure through the application of a stressor (trapping and handling the squirrels) and by provisioning squirrels with exogenous glucocorticoids (GCs). We characterized the acoustic structure of rattles emitted by these squirrels by measuring rattle duration, mean frequency, and entropy. We found evidence that rattles do indeed exhibit a “stress signature.” When squirrels were trapped and handled, they produced rattles that were longer in duration with a higher frequency and increased entropy. However, squirrels that were administered exogenous GCs had similar rattle duration, frequency, and entropy as squirrels that were fed control treatments and unfed squirrels. Our results indicate that short-term stress does affect the acoustic structure of vocalizations, but elevated circulating GC levels do not mediate such changes.


2018 ◽  
Author(s):  
Matt Sehrsweeney ◽  
David R. Wilson ◽  
Maggie Bain ◽  
Stan Boutin ◽  
Jeffrey E. Lane ◽  
...  

AbstractAcoustic signaling is an important means by which animals communicate both stable and labile characteristics. Although it is widely appreciated that vocalizations can convey information on labile state, such as fear and aggression, very few studies have experimentally examined the acoustic expression of short-term stress state. The transmission of such information about physiological state could have broad implications, potentially allowing other individuals to modify their behavior or life history traits in response to this public information. North American red squirrels (Tamiasciurus hudsonicus) produce vocalizations known as rattles that advertise territorial ownership. We examined the influence of changes in physiological stress state on rattle acoustic structure through the application of a stressor (trapping and handling the squirrels) and by provisioning squirrels with exogenous glucocorticoids (GCs). We characterized the acoustic structure of rattles emitted by these squirrels by measuring rattle duration, mean frequency, and entropy. Our results provide mixed evidence that rattles show a “stress signature”. When squirrels were trapped and handled, they produced rattles that were longer in duration with a higher frequency and increased entropy. However, squirrels that were administered exogenous GCs had similar rattle duration, frequency, and entropy as squirrels that received control treatments and unmanipulated (unfed) squirrels. Our results indicate that short-term stress does affect the acoustic structure of vocalizations, but elevated circulating GC levels are not solely responsible for such changes.


2020 ◽  
Author(s):  
Sarah E Westrick ◽  
Freya van Kesteren ◽  
Stan Boutin ◽  
Jeffrey E Lane ◽  
Andrew G McAdam ◽  
...  

AbstractEnvironmental factors experienced during development can affect the physiology and behavior of offspring. Maternal glucocorticoids (GCs) may convert environmental cues experienced by the mother into a cue triggering adaptive developmental plasticity in offspring. In North American red squirrels (Tamiasciurus hudsonicus), females exhibit increases in GCs when conspecific density is elevated, and selection favors more aggressive and perhaps more active mothers under high density conditions. We experimentally elevated maternal GCs during gestation or early lactation to test the hypothesis that elevated maternal GCs cause shifts in offspring aggression and activity that may prepare them for high density conditions. When offspring were weaned, we measured two behavioral traits (activity and aggression) using a standardized behavioral assay. Because maternal GCs may influence offspring hypothalamic-pituitary-adrenal (HPA) axis activity and HPA axis activity may in turn affect offspring behavior, we also measured the impact of our treatments on offspring HPA axis activity (adrenal reactivity and negative feedback) and the association between offspring HPA axis activity and behavior. Increased maternal GCs during lactation, but not gestation, only slightly elevated activity levels in offspring. Offspring aggression, adrenal reactivity, and negative feedback did not differ between GC-treated and control groups. Offspring with higher adrenal reactivity did exhibit lower aggression, but the relationship between adrenal reactivity and aggression was not affected by treatment with maternal GCs. These results suggest maternal GCs during gestation or early lactation alone may not be a sufficient cue to produce changes in behavioral and physiological stress responses in offspring in natural populations.Summary StatementWe found maternal glucocorticoid levels do not influence offspring personality or HPA axis dynamics in North American red squirrels. Regardless of maternal glucocorticoid treatment, more aggressive squirrels exhibited lower adrenal reactivity.


2019 ◽  
Vol 66 (2) ◽  
pp. 197-204 ◽  
Author(s):  
Francesca Santicchia ◽  
Lucas A Wauters ◽  
Ben Dantzer ◽  
Sarah E Westrick ◽  
Nicola Ferrari ◽  
...  

Abstract Glucocorticoids (GCs) are involved in the regulation of an animal’s energetic state. Under stressful situations, they are part of the neuroendocrine response to cope with environmental challenges. Animals react to aversive stimuli also through behavioral responses, defined as coping styles. Both in captive and wild populations, individuals differ in their behavior along a proactive–reactive continuum. Proactive animals exhibit a bold, active-explorative and social personality, whereas reactive ones are shy, less active-explorative and less social. Here, we test the hypothesis that personality traits and physiological responses to stressors covary, with more proactive individuals having a less pronounced GC stress response. In wild populations of invasive gray squirrels Sciurus carolinensis, we measured fecal glucocorticoid metabolites (FGMs), an integrated measure of circulating GCs, and 3 personality traits (activity, sociability, and exploration) derived from open field test (OFT) and mirror image stimulation (MIS) test. Gray squirrels had higher FGMs in Autumn than in Winter and males with scrotal testes had higher FGMs than nonbreeding males. Personality varied with body mass and population density. Squirrels expressed more activity-exploration at higher than at lower density and heavier squirrels had higher scores for activity-exploration than animals that weighed less. Variation in FGM concentrations was not correlated with the expression of the 3 personality traits. Hence, our results do not support a strong association between the behavioral and physiological stress responses but show that in wild populations, where animals experience varying environmental conditions, the GC endocrine response and the expression of personality are uncorrelated traits among individuals.


Oikos ◽  
1998 ◽  
Vol 81 (1) ◽  
pp. 81 ◽  
Author(s):  
C. Dustin Becker ◽  
Stan Boutin ◽  
Karl W. Larsen

2019 ◽  
Vol 151 ◽  
pp. 29-42 ◽  
Author(s):  
Erin R. Siracusa ◽  
David R. Wilson ◽  
Emily K. Studd ◽  
Stan Boutin ◽  
Murray M. Humphries ◽  
...  

2018 ◽  
Author(s):  
David N. Fisher ◽  
Jessica A. Haines ◽  
Stan Boutin ◽  
Ben Dantzer ◽  
Jeffrey E. Lane ◽  
...  

AbstractInteractions between organisms are ubiquitous and have important consequences for phenotypes and fitness. Individuals can even influence those they never meet, if they have extended phenotypes which mean the environments others experience are altered. North American red squirrels (Tamiasciurus hudsonicus) guard food hoards, an extended phenotype that typically outlives the individual and is almost always inherited by non relatives. Hoarding by previous owners can therefore influence subsequent owners. We found that red squirrels bred earlier and had higher lifetime fitness if the previous owner was a male. This was driven by hoarding behaviour, as males and mid-aged squirrels had the largest hoards, and these effects persisted across owners, such that if the previous owner was male or died in mid-age subsequent occupants had larger hoards. Individuals can, therefore, influence each other’s resource dependent traits and fitness without meeting via extended phenotypes, and so the past can influence contemporary population dynamics.


2021 ◽  
Author(s):  
Lauren Petrullo ◽  
Tiantian Ren ◽  
Martin Wu ◽  
Rudy Boonstra ◽  
Rupert Palme ◽  
...  

Gut microbiome diversity plays an important role in host health and fitness, in part through the diversification of gut metabolic function and pathogen protection. Elevations in glucocorticoids (GCs) appear to reduce gut microbiome diversity in experimental studies, suggesting that a loss of microbial diversity may be a negative consequence of increased GCs. However, given that ecological factors like food availability and population density may independently influence both GCs and microbial diversity, understanding how these factors structure the GC-microbiome relationship is crucial to interpreting its significance in wild populations. Here, we used an ecological framework to investigate the relationship between GCs and gut microbiome diversity in wild North American red squirrels (Tamiasciurus hudsonicus). We found that higher GCs predicted lower gut microbiome diversity and an increase in metabolic taxa. In addition, we identified a loss of potentially pathogenic bacteria with increasing GCs. Both dietary heterogeneity and an upcoming masting event exhibited direct effects on gut microbiome diversity, whereas conspecific density and host reproductive activity impacted diversity indirectly via changes in GCs. Together, our results suggest that GCs coordinate the effects of ecological change and host biology on gut microbiome diversity, and highlight the importance of situating the GC-microbiome relationship within an ecological framework.


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