Interpreting indices of physiological stress in free-living vertebrates
When vertebrate physiological ecologists use the terms ‘stress’ or ‘physiological stress’, they typically mean the level of hypothalamus–pituitary–adrenal (HPA-) axis activation. Measurements of stress hormone concentrations (e.g. glucocorticoids in blood, urine or faeces), leukocytes (e.g. the neutrophil–lymphocyte ratio or heterophil equivalent), immunofunction (e.g. innate, cell-mediated or humoral immunity measures) and regenerative anaemia (e.g. mean erythrocyte volume and red blood cell distribution width) have all been used to estimate HPA-axis activity in free-living vertebrates. Stress metrics have provided insights into aspects of autecology or population regulation that could not have been easily obtained using other indices of population wellbeing, such as body condition or relative abundance. However, short- and long-term stress (often problematically termed acute and chronic stress, respectively) can interact in unpredictable ways. When animals experience trapping and handling stress before blood, faeces and/or urine is sampled, the interaction of short- and long-term stress can confound interpretation of the data, a fact not always acknowledged in studies of stress in free-living vertebrates. This review examines how stress metrics can be confounded when estimates of HPA-axis activation are collected for free-living vertebrates and outlines some approaches that can be used to help circumvent the influence of potentially confounding factors.
KeywordsHPA axis Corticosteroids Corticosterone Cortisol Glucocorticoids H:L ratio N:L ratio Physiological stress Stress/heat shock proteins Vertebrate
We would like to thank all those who provided feedback on the ideas presented here at the ANZSCPB conference in Tasmania, 2011. We would also like to thank the four anonymous reviewers, whose comments have helped improve the manuscript.
- Atchley WR, Gaskins CT, Anderson D (1976) Statistical properties of ratios. I. Empirical results. Syst Biol 25:137–148Google Scholar
- Balcombe JP, Barnard ND, Sandusky C (2004) Laboratory routines cause animal stress. Contemp Topics 43:42–51Google Scholar
- Cockrem JF, Barrett DP, Candy EJ, Potter MA (2009) Corticosterone responses in birds: individual variation and repeatability in Adelie penguins (Pygoscelis adeliae) and other species, and the use of power analysis to determine sample sizes. Gen Comp Endocrinol 163:158–168PubMedCrossRefGoogle Scholar
- Hamilton J (2008) Evaluation of indicators of stress in populations of polar bears (Ursus maritimus) and grizzly bears (Ursus arctos). Department of Biology, University of Waterloo, OntarioGoogle Scholar
- Hothorn T, Hornik K, Zeileis A (2006) Party: a laboratory for recursive partytioning. R package version 09-0. http://CRANR-projectorg
- Jain NC (1993) Essentials of veterinary hematology. Wiley-Blackwell, Media, PAGoogle Scholar
- Johnstone CP, Lill A, Reina RD (2011) Does habitat fragmentation cause stress in the agile antechinus? A haematological approach. J Comp Physiol B Biochem Syst Environ Physiol 182(1):139–155Google Scholar
- Jones ME, Barmuta LA (1998) Diet overlap and relative abundance of sympatric dasyurid carnivores: a hypothesis of competition. J Anim Ecol, 410–421Google Scholar
- Le Maho Y, Karmann H, Briot D, Handrich Y, Robin JP, Mioskowski E, Cherel Y, Farni J (1992) Stress in birds due to routine handling and a technique to avoid it. Am J Physiol Regul Intergr Comp Physiol 263:775–781Google Scholar
- Lewis SM, Bain BJ, Bates I, Dacie JV (2006) Dacie and Lewis practical haematology. Churchill Livingstone, LondonGoogle Scholar
- Popper KR (2003) The open society and its enemies: Hegel and Marx. Routledge Classics, New YorkGoogle Scholar
- Suorsa P, Helle H, Koivunen V, Huhta E, Nikula A, Hakkarainen H (2004) Effects of forest patch size on physiological stress and immunocompetence in an area-sensitive passerine, the Eurasian treecreeper (Certhia familiaris): an experiment. Proc R Soc Lond Ser B Biol Sci (London) 271:435–440CrossRefGoogle Scholar