Heterothermy in large mammals: inevitable or implemented?

Abstract

Advances in biologging techniques over the past 20 years have allowed for the remote and continuous measurement of body temperatures in free-living mammals. While there is an abundance of literature on heterothermy in small mammals, fewer studies have investigated the daily variability of body core temperature in larger mammals. Here we review measures of heterothermy and the factors that influence heterothermy in large mammals in their natural habitats, focussing on large mammalian herbivores. The mean 24 h body core temperatures for 17 species of large mammalian herbivores (>10 kg) decreased by ∼1.3°C for each 10-fold increase in body mass, a relationship that remained significant following phylogenetic correction. The degree of heterothermy, as measured by the 24 h amplitude of body core temperature rhythm, was independent of body mass and appeared to be driven primarily by energy and water limitations. When faced with the competing demands of osmoregulation, energy acquisition and water or energy use for thermoregulation, large mammalian herbivores appear to relax the precision of thermoregulation thereby conserving body water and energy. Such relaxation may entail a cost in that an animal moves closer to its thermal limits for performance. Maintaining homeostasis requires trade-offs between regulated systems, and homeothermy apparently is not accorded the highest priority; large mammals are able to maintain optimal homeothermy only if they are well nourished, hydrated, and not compromised energetically. We propose that the amplitude of the 24 h rhythm of body core temperature provides a useful index of any compromise experienced by a free-living large mammal and may predict the performance and fitness of an animal.

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

“…Similarly, in hot environments, body core temperature in free-living large mammals, across a broad range of species, varied by less than 2.5°C over 24 h [50,51]. Contrary to what might be predicted from the physical principles of body size, the increase in body core temperature across the day, which is reflected in the amplitude of the 24 h rhythm of body core temperature, is not correlated with the body mass of large free-living mammals with access to drinking water [55]. As shown in Fig.…”

“…In an analysis of body core temperatures obtained from free-living large herbivorous mammals, we found that mean body core temperature decreased by 1.3°C for each 10-fold increase in body mass [55]. However, the relationship between mean body core temperature and body mass also is influenced by phylogeny.…”

“…Indeed, where they have access to water, free-living large mammals appear to use evaporative water loss (see below) routinely to regulate body core temperature independently of environmental heat load [55]. They therefore routinely operate outside the boundaries of their laboratory-determined thermoneutral zones.…”

“…Reducing evaporative water loss in hot, dry environments implies that large mammals prioritize osmoregulation over the maintenance of a constant body core temperature [55]. A decrease in metabolic heat production in dehydrated large mammals [109,111] may reduce the extent of hyperthermia when evaporative cooling is reduced.…”

“…3, Arabian oryx reached a higher body core temperature in a hot, dry period compared to when it was warm and wet. A depression of the 24 h minimum body temperature also was evident in the hot, dry period, but that reduction is likely to represent a failure to maintain 24 h minimum body temperature in response to energy deprivation (see below), rather than an adaptive response to increase heat storage capacity [55]. In Arabian oryx in a desert environment, the period of lowest water and lowest energy availability coincided in summer.…”