A hot lunch for herbivores: physiological effects of elevated temperatures on mammalian feeding ecology

Abstract

Mammals maintain specific body temperatures (T b ) across a broad range of ambient temperatures. The energy required for thermoregulation ultimately comes from the diet, and so what animals eat is inextricably linked to thermoregulation. Endothermic herbivores must balance energy requirements and expenditure with complicated thermoregulatory challenges from changing thermal, nutritional and toxicological environments. In this review we provide evidence that plant-based diets can influence thermoregulation beyond the control of herbivores, and that this can render them susceptible to heat stress. Notably, herbivorous diets often require specialised digestive systems, are imbalanced, and contain plant secondary metabolites (PSMs). PSMs in particular are able to interfere with the physiological processes responsible for thermoregulation, for example by uncoupling mitochondrial oxidative phosphorylation, binding to thermoreceptors, or because the pathways required to detoxify PSMs are thermogenic. It is likely, therefore, that increased ambient temperatures due to climate change may have greater and more-specific impacts on herbivores than on other mammals, and that managing internal and external heat loads under these conditions could drive changes in feeding ecology.

Cold temperature improves tannin tolerance in a granivorous rodent

“…Additionally, several studies have found that the enzyme activities of key biotransformation enzymes are reduced in the livers of rodents acclimated to warm temperatures compared to cooler ones, even when animals are not exposed to toxins (Connors et al, ; Kaplanski & Ben‐Zvi, ; Settivari et al, ). The prevailing theory for down‐regulation of detoxification systems by endotherms at high ambient temperatures is an increased need to dissipate body heat (Beale et al, ). As both temperatures tested in our study are expected to be below the lower limit of the thermoneutral zone for A. speciosus (21.6°C; Sekijima, ), heat dissipation limitation is unlikely to be affecting the mice, despite a 10°C difference in the ambient temperature.…”

“…Cold-induced tannin tolerance may help to further explain the relationships between acorn production and the population dynamics of granivores. Furthermore, a better understanding of these temperature-plant-herbivore relationships is of major importance in predicting the impact of global climate change on mammals (Beale et al, 2018;Moore, Wiggins, Marsh, Dearing, & Foley, 2015).…”

“…Rate of detoxification is influenced by PSM dose, enzyme activity, as well as genetic factors, disease and age (McLean & Duncan, ). In addition to these intrinsic factors, ambient temperature may have a significant role to play in PSM detoxification and, therefore, the tolerance of mammals to PSMs (Beale, Marsh, Foley, & Moore, ; Dearing, ).…”

Review: Using physiologically based models to predict population responses to phytochemicals by wild vertebrate herbivores

“…Ambient temperature can change nutritional demands of herbivores (e.g. metabolic costs, Hillebrand et al, 2009;Smith-Ramesh et al, 2017;Hristov et al, 2018) and the toxicity of ingested phytochemicals (Dearing, 2013;Connors et al, 2017;Beale et al, 2018). As such, estimating biologically relevant physiological parameters requires knowledge of phytochemical intake within an environmental context, which is always challenging in wild herbivores.…”

Influence of leaf chemistry on dietary choice and habitat quality of koala (Phascolarctos cinereus) populations in southwest Queensland

“…The importance of water has been emphasised for marsupial folivores in semi-arid areas, especially in harsh dry conditions (Gordon et al 1988, Munks et al 1996. Consuming PSMs increases the water requirements of animals to excrete urinary metabolites of PSMs (Beale et al 2017). In hot weather, koalas have higher rates of water influx for cooling via evapotranspiration (Ellis et al 1995).…”