Abstract
The hypothalamus–pituitary–adrenal/interrenal (HPA) axis of vertebrates integrates external information and orchestrates responses to cope with energy-demanding and stressful events through changes in circulating glucocorticoid levels. Urbanization exposes animals to a wide variety of ever-changing stimuli caused by human activities that may affect local wildlife populations. Here, we empirically tested the hypothesis that urban and rural owls (Athene cunicularia) show different adrenocortical responses to stress, with urban individuals showing a reduced HPA-axis response compared to rural counterparts to cope with the high levels of human disturbance typical of urban areas. We applied a standard capture-restraint protocol to measure baseline levels and stress-induced corticosterone (CORT) responses. Urban and rural owls showed similar circulating baseline CORT levels. However, maximum CORT levels were attained earlier and were of lower magnitude in urban compared to rural owls, which showed a more pronounced and long-lasting response. Variability in CORT responses was also greater in rural owls and contained the narrower variability displayed by urban ones. These results suggest that only individuals expressing low-HPA-axis responses can thrive in cities, a pattern potentially mediated by three alternative and non-exclusive hypotheses: phenotypic plasticity, natural selection and matching habitat choice. Due to their different conservation implications, we recommend further research to properly understand wildlife responses to humans in an increasingly urbanized world.
Highlights
Urbanization induces a wide range of ecological changes (Vitousek et al, 1997), often acting as a selective in natural populations (Alberti, 2015), changing biotic and abiotic environmental factors, and having important consequences for biodiversity conservation worldwide
These results suggest that only individuals expressing low-HPA-axis responses can thrive in cities, a pattern potentially mediated by three alternative and non-exclusive hypotheses: phenotypic plasticity, natural selection and matching habitat choice
Based on our previous knowledge of our study model, we predicted that (i) urban and rural birds will show similar baseline CORT levels, as birds occupy sites according to their tolerance to human disturbance (Carrete and Tella, 2010, 2011; Rebolo-Ifrán et al, 2015); (ii) rural birds will show higher variability in the CORT levels in the bloodstream, encompassing the variability shown by urban ones, as expected from previous behavioural studies assessing variability in fear of humans (Carrete and Tella, 2010, 2011); and (iii) urban birds will show lower stress-induced CORT levels, as only individuals with particular physiological responses are able to live close to humans without experiencing chronic stress (Lowry et al, 2013; Rebolo-Ifrán et al, 2015)
Summary
Urbanization induces a wide range of ecological changes (Vitousek et al, 1997), often acting as a selective in natural populations (Alberti, 2015), changing biotic and abiotic environmental factors, and having important consequences for biodiversity conservation worldwide. Carrete and Tella (2010, 2011) have proposed that bird species able to colonize urban habitats are those with higher inter-individual variability in their fear of humans (estimated as the distance at which a given individual flees when approached by a human, hereafter flight initiation distance FID). This suggests that from a pool of behaviourally variable rural individuals, only the less fearful ones can colonize cities (Carrete and Tella, 2011). As FID is a repeatable and heritable trait, this non-random distribution of individuals would likely arise through natural selection or matching habitat choice, some degree of plasticity cannot be completely ruled out (Carrete and Tella, 2010, 2013; Carrete et al, 2016)
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