Developmental and geographic variation in stress hormones in wild Belding's ground squirrels (Spermophilus beldingi)

Abstract

Extensive research has been conducted on the role of glucocorticoids in regulating growth, mobilizing energy, responding to stressors and modulating learning and memory. However, little is known about the production of corticoids during early development in free-living animals, particularly during sensitive periods of acquisition of important behaviors. In a four-year study of Belding's ground squirrels, Spermophilus beldingi, a non-invasive assay of glucocorticoids was used to quantify age and population differences among juveniles from three California locations. Fecal-cortisol metabolites are elevated during a short period when juveniles first emerge aboveground from their natal burrows at about 4 weeks of age. This period of cortisol elevation coincides with when young are learning survival behaviors such as anti-predator responses and foraging strategies. Population differences in juvenile cortisol levels, which may reflect local variation in habitat quality and predator environments, were not evident until 2 weeks after emergence. Elevated cortisol at the age of emergence was also observed in juveniles born and reared in captivity without exposure to typical stressors that occur around the age of emergence. These results indicate that corticoids are regulated during early development, and the possible functions of age-related corticoid levels are discussed, including mobilization of glucose for natal emergence and later facilitation of growth and energy storage during the short summer before hibernation. In some species, elevated corticoids can also facilitate learning and memory, and current work is exploring whether the higher cortisol observed in all three S. beldingi populations just after emergence function to promote rapid acquisition of survival behaviors.

Fig. 1

Correlations between days since natal emergence and fecal corticoids (ng/g dried feces) in juvenile S. beldingi at Rock Creek. Unadjusted fecal cortisol levels are shown; analyses were based on log-transformed data. (A) 2002: n=166, r=−0.57, P<0.0001; y=−0.073×+6.756, regression t=−8.89, P<0.0001. (B) 2003: n=69, r=−0.65, P<0.0001; y =−0.16×+7.007, regression t=−6.90, P<0.0001. (C) 2004: n=154, r=−0.41, P<0.0001; y=−0.015×+6.049, regression t=−5.60, P<0.0001. (D) 2005: n=52, r=−0.49, P<0.0001; y=−0.057×+6.047, regression t=−3.95, P<0.0001.

Fig. 2

Patterns of developmental and geographic variation in fecal corticoids (ng/g dried feces+SEM) of free-living juvenile S. beldingi from three populations in 2002–2005 (A–D). Unadjusted fecal cortisol levels are shown; analyses were based on log-transformed data. Round 1 represents fecal sampling during the first 5 days after natal emergence and Round 2 occurred approximately 2 weeks later. After Round 2, juveniles were sampled almost weekly at Rock Creek for several weeks in 2002 and 2004. Lines over columns indicate significant population differences within an age group based on Bonferroni pairwise comparisons for significant ANOVAs (*P<0.05; **P<0.01). See Tables 2 and 3 for ANOVA results.

Fig. 3

Unadjusted mean fecal corticoids (ng/g dried feces+SEM) of 12 captive-born juvenile S. beldingi. Different letters inside columns indicate significant age differences based on a repeated-measures ANOVA of log-transformed data.