No 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.

Sloths are considered to have one of the lowest mass-specific metabolic rates of any mammal and, in tandem with a slow digestive rate, have been theorized to have correspondingly low rates of ingestion. Here, we show in a study conducted over five months, that three captive Bradypus variegatus (Brown-throated sloths) had a remarkably low mean food intake of 17 g kg−1day−1 (SD 4.2). Food consumption was significantly affected by ambient temperature, with increased intake at higher temperatures. We suggest that the known fluctuation of sloth core body temperature with ambient temperature affects the rate at which gut fauna process digesta, allowing for increased rates of fermentation at higher temperatures. Since Bradypus sloths maintain a constantly full stomach, faster rates of fermentation should enhance digestive throughput, increasing the capacity for higher levels of food intake, thereby allowing increased energy acquisition at higher ambient temperatures. This contrasts with other mammals, which tend to show increased levels of food intake in colder conditions, and points to the importance of temperature in regulating all aspects of energy use in sloths.

Sloths are canopy-dwelling inhabitants of American neotropical rainforests that exhibit suspensory behaviors. These abilities require both strength and muscular endurance to hang for extended periods of time; however, the skeletal muscle mass of sloths is reduced, thus requiring modifications to muscle architecture and leverage for large joint torque. We hypothesize that intrinsic muscle properties are also modified for fatigue resistance and predict a heterogeneous expression of slow/fast myosin heavy chain (MHC) fibers that utilize oxidative metabolic pathways for economic force production. MHC fiber type distribution and energy metabolism in the forelimb muscles of three-toed ( Bradypus variegatus, n = 5) and two-toed ( Choloepus hoffmanni, n = 4) sloths were evaluated using SDS-PAGE, immunohistochemistry, and enzyme activity assays. The results partially support our hypothesis by a primary expression of the slow MHC-1 isoform as well as moderate expression of fast MHC-2A fibers, whereas few hybrid MHC-1/2A fibers were found in both species. MHC-1 fibers were larger in cross-sectional area (CSA) than MHC-2A fibers and comprised the greatest percentage of CSA in each muscle sampled. Enzyme assays showed elevated activity for the anaerobic enzymes creatine kinase and lactate dehydrogenase compared with low activity for aerobic markers citrate synthase and 3-hydroxyacetyl CoA dehydrogenase. These findings suggest that sloth forelimb muscles may rely heavily on rapid ATP resynthesis pathways, and lactate accumulation may be beneficial. The intrinsic properties observed match well with suspensory requirements, and these modifications may have further evolved in unison with low metabolism and slow movement patterns as means to systemically conserve energy. NEW & NOTEWORTHY Myosin heavy chain (MHC) fiber type and fiber metabolic properties were evaluated to understand the ability of sloths to remain suspended for extended periods without muscle fatigue. Broad distributions of large, slow MHC-1 fibers as well as small, fast MHC-2A fibers are expressed in sloth forelimbs, but muscle metabolism is generally not correlated with myosin fiber type or body size. Sloth muscles rely on rapid, anaerobic pathways to resist fatigue and sustain force production.