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

Abstract

Mechanistic approaches for predicting the ranges of endotherms are needed to forecast their responses to environmental change. We test whether physiological constraints on maximum metabolic rate and the factor by which endotherms can elevate their metabolism (metabolic expansibility) influence cold range limits for mammal and bird species. We examine metabolic expansibility at the cold range boundary (ME_CRB) and whether species' traits can predict variability in ME_CRB and then use ME_CRB as an initial approach to project range shifts for 210 mammal and 61 bird species. We find evidence for metabolic constraints: the distributions of metabolic expansibility at the cold range boundary peak at similar values for birds (2.7) and mammals (3.2). The right skewed distributions suggest some species have adapted to elevate or evade metabolic constraints. Mammals exhibit greater skew than birds, consistent with their diverse thermoregulatory adaptations and behaviors. Mammal and bird species that are small and occupy low trophic levels exhibit high levels of ME_CRB. Mammals with high ME_CRB tend to hibernate or use torpor. Predicted metabolic rates at the cold range boundaries represent large energetic expenditures (>50% of maximum metabolic rates). We project species to shift their cold range boundaries poleward by an average of 3.9° latitude by 2070 if metabolic constraints remain constant. Our analysis suggests that metabolic constraints provide a viable mechanism for initial projections of the cold range boundaries for endotherms. However, errors and approximations in estimating metabolic constraints (e.g., acclimation responses) and evasion of these constraints (e.g., torpor/hibernation, microclimate selection) highlight the need for more detailed, taxa-specific mechanistic models. Even coarse considerations of metabolism will likely lead to improved predictions over exclusively considering thermal tolerance for endotherms.

Keywords: distribution; endotherm; metabolic expansibility; metabolic scope; range limit; thermal neutral zone.

Figure 1

How ambient temperature governs metabolic rate. The thermal neutral zone [bounded by lower (T _lc) and upper (T _uc) critical temperatures] is the range of temperatures over which endotherms are able to maintain their basal metabolic rate (BMR). We use the minimum (T _min) and maximum (T _max) ambient temperatures across a species’ range to estimate sustained metabolic rate at the range boundary (MR_CRB). We calculate metabolic expansibility (ME_CRB) as MR_CRB/BMR and depict maximum (summit) metabolic capacity (M_sum). Thermal conductance (C) is calculated as the slope of the line terminating at body temperature (T _b)

Figure 2

The density distribution of metabolic expansibility, ME_CRB (the factor by which metabolic rate at the cold range edge is elevated over basal metabolic rate) peaks at similar values for birds and mammals (a). We examine interspecific variation in ME_CRB by (b) plotting the physiological temperature limit predicted by assuming the mode of ME_CRB (x‐axes) and the observed temperatures at the cold range boundaries (y‐axes). Mammals and birds that are small (symbol size) and use torpor or hibernation (color, 1 = use, gray = no data) tend to be found in environments colder than predicted assuming the mode ME_CRB (i.e., they have higher ME_CRB). The lines indicate 1:1 relationships.

Figure 3

A histogram (a) of the ratio of summit metabolic capacity (M_sum) to estimated metabolic rate at the cold range boundary (MR_CRB) suggests the high energetic demands of thermoregulation. We examine interspecific variation in the ratio (MR_CRB/M_sum) by plotting the observed temperatures at the cold range boundaries against the physiological temperature limit corresponding to MR_CRB = 0.7 M_sum (b). We depict mammals (filled circles) and birds (hollow circles), mass (symbol size), and use of torpor or hibernation (color, 1 indicates use).

Figure 4

We depict observed cold range boundaries (CRB, black polygons: IUCN range maps) and those projected based on metabolic constraints for exemplar North American rodents in current (blue: 1950–2000) and predicted future (pink: 2061–2080 from HadGEM2‐AO model) climates (a–c). Purple shading indicates portions of the projected range occupancy that persists through climate warming. We note few areas of range contraction (blue) since we are only predicting CRBs (the depicted equatorward extent is not meaningful). We restrict our CRB projections to the observed longitudinal extent. The species differ in the extent of their current distribution and the projected CRB shift resulting from climate change (a, Marmota monax, groundhog; b, Microtus montanus, montane vole; and c, Peromyscus eremicus, cactus mouse). Projections based on metabolic constraints indicate that the majority of mammals (purple) and birds (green) will shift their CRB modestly poleward through climate changes (d). However, numerous species are projected to shift their CRB poleward by 10° latitude and some species are projected to shift by as much as 22°