Metabolic heat production and thermal conductance are mass-independent adaptations to thermal environment in birds and mammals

Abstract

The extent to which different kinds of organisms have adapted to environmental temperature regimes is central to understanding how they respond to climate change. The Scholander-Irving (S-I) model of heat transfer lays the foundation for explaining how endothermic birds and mammals maintain their high, relatively constant body temperatures in the face of wide variation in environmental temperature. The S-I model shows how body temperature is regulated by balancing the rates of heat production and heat loss. Both rates scale with body size, suggesting that larger animals should be better adapted to cold environments than smaller animals, and vice versa. However, the global distributions of ∼9,000 species of terrestrial birds and mammals show that the entire range of body sizes occurs in nearly all climatic regimes. Using physiological and environmental temperature data for 211 bird and 178 mammal species, we test for mass-independent adaptive changes in two key parameters of the S-I model: basal metabolic rate (BMR) and thermal conductance. We derive an axis of thermal adaptation that is independent of body size, extends the S-I model, and highlights interactions among physiological and morphological traits that allow endotherms to persist in a wide range of temperatures. Our macrophysiological and macroecological analyses support our predictions that shifts in BMR and thermal conductance confer important adaptations to environmental temperature in both birds and mammals.macrophysiology | Bergmann's rule | body size | metabolic rate | thermal conductance A fundamental problem in ecology and biogeography is to elucidate the physiological processes that determine the environmental tolerances and influence the distributions of species. Across their nearly worldwide distributions, endothermic birds and mammals maintain near-constant body temperatures in the face of extreme and fluctuating environmental temperatures. Elucidating the morphological and physiological adaptations that allow species to inhabit such a wide spectrum of thermal environments is important for understanding the distribution of biodiversity and for predicting responses of species to climate change (1, 2).In a seminal paper, Scholander et al. (3) showed how endotherms balance rates of heat production and heat loss so as to maintain a constant body temperature in the face of varying environmental temperatures. The essence of the Scholander-Irving (S-I) model is the equation:where T b is body temperature, T a is ambient temperature, B is the rate of metabolic heat production, and C is the rate of heat loss or thermal conductance (4). For a resting animal, which has minimized heat loss by maximizing insulation and optimizing body posture, C = minimum thermal conductance (C MIN ); B = basal metabolic rate (BMR); and T a = T lc , where T lc is the lower critical temperature or the lower limit of the thermal neutral zone (TNZ).The TNZ is ecologically important because it is the range of environmental temperatures where energy expenditure is minimal; out...

Effects of Contingency versus Constraints on the Body-Mass Scaling of Metabolic Rate

“…Within the thermoneutral zone, metabolic heat production exactly balances the heat dissipated, which is chiefly a function of surface area. However, as the cross-surface temperature differential increases, the metabolic scaling slope should approach~0.45-0.55, as typically observed for the scaling of thermal conductance in birds and mammals [6,[79][80][81][82][83][84][85][86]. As predicted, when T a equals 0 • C (which is greater than 30 • C below T b ), the metabolic scaling exponents for mammals (0.40), passerine birds (0.52) and nonpasserine birds (0.53) ( [56,58]; Figures 3 and 4) all approach that observed for the scaling exponent of thermal conductance.…”

Environment predicts repeated body size shifts in a recent radiation of Australian mammals*

“…) and basal metabolic rate (Fristoe et al. ). Specifically among rodents, kidney function (MacMillen and Lee ; Giorello et al.…”

Does metabolism constrain bird and mammal ranges and predict shifts in response to climate change?

“…Those MR values reported in watts were converted to oxygen consumption assuming a factor of 179 ml O 2 h −1 W −1 , which corresponds to lipid metabolism (Schmidt‐Nielsen, ). Minimum conductance was estimated as the absolute value of the slope of the line connecting T lc at BMR to T b when metabolic rate is 0: C min = |(0‐BMR)/( T b − T lc )|(Fristoe et al, ; Scholander et al, ). This assumption is often violated by conductance continuing to decline below the T lc , but we feel that the estimate approach best balances accuracy and viability.…”

“…Here we leverage extensive metabolic, distribution, and phylogenetic datasets (Fristoe et al, ; Khaliq, Hof, Prinzinger, Böhning‐Gaese, & Pfenninger, ) to test the viability of using metabolic constraints to project bird and mammal distributions. Specifically, we estimate the factor by which metabolism is elevated at the cold range boundaries (metabolic expansibility, ME CRB ).…”