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

  • Sarah E. WestrickEmail author
  • Freya van Kesteren
  • Rupert Palme
  • Rudy Boonstra
  • Jeffery E. Lane
  • Stan Boutin
  • Andrew G. McAdam
  • Ben Dantzer
Original Article

Abstract

Individuals 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 statement

Individuals 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.

Keywords

Coping styles Glucocorticoids North American red squirrels Behavioral syndromes 

Notes

Acknowledgments

We thank Agnes MacDonald and her family for long-term access to her trapline, and the Champagne and Aishihik First Nations for allowing us to conduct our work within their traditional territory. We thank Adi Boon, Amanda Kelley, and Ryan W. Taylor for collecting much of the behavioral data and all the volunteers, field assistants, and graduate students for their assistance in data collection. We thank the two anonymous reviewers for the helpful feedback which improved the manuscript. This work was supported by the American Society of Mammalogists to SEW; University of Michigan to SEW and BD; National Science Foundation (IOS-1749627) to BD; and Natural Sciences and Engineering Research Council to SB, AGM, JL, and RB. This is publication no. 103 of the Kluane Red Squirrel Project.

Compliance with ethical standards

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted. Animal ethics approvals were received from Michigan State University (AUF#04/08-046-00) and University of Guelph (AUP#09R006).

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

265_2019_2728_MOESM1_ESM.pdf (164 kb)
ESM 1 (PDF 164 kb)

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Copyright information

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Authors and Affiliations

  1. 1.Department of PsychologyUniversity of MichiganAnn ArborUSA
  2. 2.Department of Biomedical SciencesUniversity of Veterinary MedicineViennaAustria
  3. 3.Department of Biological SciencesUniversity of Toronto ScarboroughTorontoCanada
  4. 4.Department of BiologyUniversity of SaskatchewanSaskatoonCanada
  5. 5.Department of Biological SciencesUniversity of AlbertaEdmontonCanada
  6. 6.Department of Integrative BiologyUniversity of GuelphGuelphCanada
  7. 7.Department of Ecology and Evolutionary BiologyUniversity of MichiganAnn ArborUSA

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