Social Dominance Is Associated with Individual Differences in Heart Rate and Energetic Response to Food Restriction in Female Red Deer

Abstract

Energy expenditure is a key mechanism underlying animal ecology, yet why individuals often differ in metabolic rate even under identical conditions remains largely unexplained. Individual variation in metabolism might be explained by correlations with other behavioral and physiological traits, with individual syndromes having environment- or state-dependent costs and benefits to fitness. We tested whether social rank within herds of female red deer is associated with individual differences in resting heart rate, an index of metabolic rate, and energetic response to monthly periods of food restriction during winter in a large outdoor enclosure near Vienna, Austria. Social rank had a strong positive effect on average daily heart rate, independent of the effects of food intake, air temperature, body temperature, and body mass. Subordinate individuals had lower heart rates than dominants, and consequently they suffered lower rates of body mass loss during periods of restricted pellet food supply. A greater capacity to minimize energy requirements might benefit the survival of subdominant female red deer during periods of negative energy balance in winter. Our study provides empirical support in a large mammal for linkages in behavior and metabolism within individuals that have environment-dependent consequences to the energy budget.

Meta-analysis reveals that resting metabolic rate is not consistently related to fitness and performance in animals

“…In contrast, dominance was clearly positively correlated with RMR for both ectotherms and endotherms. Dominant individuals are often those that can acquire more resources (territory, food, or mates), and in accordance with the increased intake hypothesis, these individuals should be able to maintain high RMR in non-limiting conditions (Careau et al 2008;Careau and Garland 2012;Turbill et al 2013). However, the relatively large effect size may be inflated by early studies that found large effects from small samples (e.g., Røskaft et al 1986), as more recent studies with much larger samples sizes typically identify far smaller effects (e.g., Radwan et al 2004).…”

Heart rate as a measure of emotional arousal in evolutionary biology

“…Already the approach by a dominant group member and the associated risk of aggression were found to significantly increase heart rate in rhesus macaques [26], and even indirect social interactions can affect heart rate, for example observing aggressive interactions as a bystander [20,21], or visual and olfactory presentation of dominant or aggressive individuals [36,46]. The relationship between social status and heart rate can manifest itself in rank-dependent differences in resting heart rates, as described in red deer, Cervus elaphus , where subordinate individuals have lower resting heart rates compared to dominant individuals, which might result in a better capacity to minimize energy requirements [25].

Figure 1Examples of heart rate modulation in greylag geese.

…”

“…[24]red deer, Cervus elaphus rumen-located transmittersTurbill et al . [25]rhesus macaques, Macaca mulatta implanted radio-transmitterAureli et al . [26]anthropogenic disturbanceAdélie penguins, Pygoscelis adeliae artificial eggsNimon et al .…”

Towards a mechanistic understanding of the responses of large terrestrial mammals to heat and aridity associated with climate change

“…However, acclimatization to changing stressors and intraspecific differences in a population, in terms of social positioning, reproductive status, and age, may influence an individual's sensitivity and vulnerability to climate change. For example, when food was restricted, subordinate female red deer, surprisingly, achieved a much lower metabolic rate than did dominant females, resulting in less body mass loss [160]. On the other hand, vervet monkeys (Chlorocebus pygerythrus) with a greater number of social partners achieved better regulation of body temperature during winter than did those with fewer relationships [149].…”