Abstract

Poikilotherms and homeotherms have different, well-defined metabolic responses to ambient temperature (Ta), but both groups have high power costs at high temperatures. Sloths (Bradypus) are critically limited by rates of energy acquisition and it has previously been suggested that their unusual departure from homeothermy mitigates the associated costs. No studies, however, have examined how sloth body temperature and metabolic rate vary with Ta. Here we measured the oxygen consumption (VO2) of eight brown-throated sloths (B. variegatus) at variable Ta’s and found that VO2 indeed varied in an unusual manner with what appeared to be a reversal of the standard homeotherm pattern. Sloth VO2 increased with Ta, peaking in a metabolic plateau (nominal ‘thermally-active zone’ (TAZ)) before decreasing again at higher Ta values. We suggest that this pattern enables sloths to minimise energy expenditure over a wide range of conditions, which is likely to be crucial for survival in an animal that operates under severe energetic constraints. To our knowledge, this is the first evidence of a mammal provisionally invoking metabolic depression in response to increasing Ta’s, without entering into a state of torpor, aestivation or hibernation.

Highlights

  • Animals must remain in positive energy balance over their lifetime, with energy acquisition occurring via food, and energy expenditure occurring via movement (Nathan et al, 2008; Shepard et al, 2013), growth (Careau et al, 2013; Pontzer et al, 2014), reproduction (Gittleman & Thompson, 1988; Thometz et al, 2016), and physiological homeostasis (Haim & Borut, 1981; Silva, 2005)

  • This comes at an energetic cost though (Nagy, 2005), because at low Ta’s, where the heat produced by metabolic processes during normal activity does not equal the heat lost (below the thermoneutral zone (TNZ)), animals have to increase their metabolic rate to keep warm (Haim & Borut, 1981)

  • Our results are broadly comparable to both the resting metabolic rate (RMR) and field metabolic rate (FMR) values previously recorded for three-fingered sloths (Irving, Scholander & Grinnell, 1942; McNab, 1978; Nagy & Montgomery, 1980; Pauli et al, 2016) and confirm the notion that sloths have one of the lowest metabolic rates of any non-hibernating mammal

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Summary

Introduction

Animals must remain in positive energy balance over their lifetime, with energy acquisition occurring via food, and energy expenditure occurring via movement (Nathan et al, 2008; Shepard et al, 2013), growth (including tissue regeneration) (Careau et al, 2013; Pontzer et al, 2014), reproduction (Gittleman & Thompson, 1988; Thometz et al, 2016), and physiological homeostasis (Haim & Borut, 1981; Silva, 2005). Homeotherms usually use adaptive thermogenesis to maintain high, stenothermal, Tb’s that are largely independent of their surroundings (Lowell & Spiegelman, 2000), maintaining physical performance at a range of Ta’s (Pat, Stone & Johnston, 2005) This comes at an energetic cost though (Nagy, 2005), because at low Ta’s, where the heat produced by metabolic processes during normal activity does not equal the heat lost (below the thermoneutral zone (TNZ)), animals have to increase their metabolic rate to keep warm (Haim & Borut, 1981). Metabolic rate and body temperature can be depressed for prolonged periods (Wilz & Heldmaier, 2000)

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