Quantifying long-term stress in brown bears with the hair cortisol concentration: a biomarker that may be confounded by rapid changes in response to capture and handling

Abstract

The measurement of cortisol in hair is becoming important in studying the role of stress in the life history, health and ecology of wild mammals. The hair cortisol concentration (HCC) is generally believed to be a reliable indicator of long-term stress that can reflect frequent or prolonged activation of the hypothalamic-pituitary-adrenal axis over weeks to months through passive diffusion from the blood supply to the follicular cells that produce the hair. Diffusion of cortisol from tissues surrounding the follicle and glandular secretions (sebum and sweat) that coat the growing hair may also affect the HCC, but the extent of these effects is thought to be minimal. In this study, we report on a range of factors that are associated with, and possibly influence, cortisol concentrations in the hair of free-ranging brown bears (Ursus arctos). Through two levels of analyses that differed in sample sizes and availability of predictor variables, we identified the presence or absence of capture, restraint and handling, as well as different methods of capture, as significant factors that appeared to influence HCC in a time frame that was too short (minutes to hours) to be explained by passive diffusion from the blood supply alone. Furthermore, our results suggest that HCC was altered after hair growth had ceased and blood supply to the hair follicle was terminated. However, we also confirmed that HCC was inversely associated with brown bear body condition and was, therefore, responsive to diminished food availability/quality and possibly other long-term stressors that affect body condition. Collectively, our findings emphasize the importance of further elucidating the mechanisms of cortisol accumulation in hair and the influence of long- and short-term stressors on these mechanisms.

Keywords: Barbed-wire snag; Ursus arctos; body condition; capture; hair cortisol concentration; stress.

Figure 1:

Brown bear study areas in Alberta, Canada from 1994 to 2012. Hair samples were collected following the capture of 53 unique animals in the Eastern Slopes Grizzly Bear Project (ESGBP) study area (from 1994 to 2002) and from 125 unique animals in the Foothills Research Institute Grizzly Bear Project (FRIGBP) study area (from 2001 to 2012). Hair samples also were collected by barbed-wire snagging from 323 unique animals in the Alberta Grizzly Bear DNA Inventory study area from 2004 to 2008. Abbreviation: BMA, bear management area. Map projection, Mercator.

Figure 2:

Box plot comparison of hair cortisol concentration (HCC) among female and male brown bears (n = 486) sampled by barbed-wire hair snagging (barbed wire) or by clipping hair following capture by remote drug delivery from helicopter (helicopter), leg-hold snare (snare) or culvert trap (culvert). The top and bottom of each box represents the first and third quartiles (Q1 and Q3), while the inside line represents the median. The vertical line goes to the first data points before the ‘1.5’ cut-off above and below the box. The ‘1.5’ cut-off above is calculated as Q3 + 1.5 × (Q3 − Q1) and the ‘1.5’ cut-off below is calculated as Q1 − 1.5 × (Q3 − Q1). The points represent values (outliers) lying outside of the range defined by the vertical lines. Sample sizes for sex × hair collection method categories are presented in parentheses below each box plot.

Figure 3:

The association between hair cortisol concentration and body condition index (BCI) values for 116 brown bears captured in Alberta, Canada. The continuous curved line is the estimated smoother for the BCI taken from the additive mixed model in Table 5, the dashed curved lines are point-wise 95% confidence bands, and the points are the observed values for bears captured by remote drug delivery from helicopter (open circles), leg-hold snare (filled circles) or culvert trap (filled triangles).