In utero accumulated steroids predict neonate anti‐predator response in a wild mammal

Abstract

Behavioural variation at the individual level has been shown to play an important role in animal ecology and evolution. Whereas most studies have focused on subadult or adult subjects, neonates have been relatively neglected, despite studies showing that neonates can exhibit consistent inter‐individual differences during early developmental stages. Steroid hormones, including glucocorticoids (e.g. cortisol) and androgens (e.g. testosterone), play a crucial role in foetal development and maturation and could therefore drive neonate behaviour, although this relationship is poorly understood in wild animal populations. Our study addresses these knowledge gaps by investigating the association between neonate fallow deer Dama dama fawn inter‐individual variability in behavioural response to human handling and hair cortisol and testosterone levels. We found strong evidence that individual neonates display repeatable differences in the way they cope with a risky situation during their first days of life, and showed how these differences are linked to cortisol and testosterone levels accumulated in utero. We showed that, when both steroids are included in the same model, neonates with high cortisol and low testosterone levels coped in a more proactive way with human handling (higher heart rate during handling and shorter latency to leave when released) compared to those with low cortisol and high testosterone levels (lower heart rate and longer latency to leave). These results provide novel insights into the proximate mechanism leading to neonate inter‐individual variation in a wild population of large mammals. A free Plain Language Summary can be found within the Supporting Information of this article.

Neonate personality affects early-life resource acquisition in a large social mammal

“…Using fishing nets (1-1.5m diameter; various brands), we located and tagged a total of 185 fawns over two consecutive years (n = 102 in 2018, n = 83 in 2019), of which 91 were recaptured once (n = 43 in 2018, n = 48 in 2019), 33 twice (n = 14 in 2018, n = 19 in 2019), and 9 three times or more (n = 4 in 2018, n = 5 in 2019). We recorded the following confounding variables which have been shown to affect neonatal response to handling (Amin et al 2021): weight (in kg) was measured using a digital scale by laying the fawn in a 100-litre bag (resolution: 0.01 kg – Dario Markenartikelvertrieb, Hamburg, Germany); air temperature was measured at the bed-site location using a digital thermometer (Grandbeing, China). We quantified the behaviour of the fawn prior to capture (prior behaviour) by recording whether the fawn was in motion (yes = 1, no = 0), turned its head to look around (yes = 1, no = 0), kept its head up or down (up = 1, down = 0), had its ears up or down (up = 1, down = 0), was down but got up (yes = 1, no = 0), and attempted to run away (yes = 1, no = 0).…”

“…Directly relevant to this study, we selected a physiological trait (heart rates prior to release, i.e. a physiological response of fawns to human handling) and a behavioural trait (latency to leave upon release), both shown to be repeatable at the among-individual level previously (Amin et al, 2021). Heart rates were taken directly before the weighting of the fawns and quantified by counting the number of beats per 20 seconds using a Lightweight Dual Head Stethoscope (MDF®, California, USA).…”

“…Since the logit of 0 and 1 translate to -∞ and ∞, we added the smallest non-zero value to both the numerator and denominator of the logit equation (Warton & Hui, 2011). We used a priori model structures for each response variable, which in the case of the neonate capture traits were based on a previous study (Amin et al, 2021). In the case of scanning time, we included explanatory variables that contained information on the context of each observation, where we included both the linear and quadratic terms for all the numerical explanatory variables to allow non-linear effects.…”

“…Fallow deer are a hider species (Lent, 1974): fawns experience a solitary life during their first 2-4 weeks of life remaining hidden in vegetation while occasionally being visited by their mother for maternal care (Chapman & Chapman 1997). We recently showed that repeatable among-individual differences are present during the first days of life in this population (Amin et al, 2021). Some neonates display repeatable active responses – i.e.…”

“…elevated heart rates and short latency to leave when released - whereas other neonates are bolder and less risk aversive – i.e. they maintain low heart rates during human handling and have longer latencies to leave once released (Amin et al, 2021).…”