Development of thermoregulation and torpor in a marsupial: energetic and evolutionary implications

Abstract

Altricial mammals and birds become endothermic at about half the size of adults and presumably would benefit energetically from entering torpor at that time. Because little is known about torpor during development in endotherms, we investigated whether after the establishment of endothermic thermoregulation (i.e. the ability to maintain a high body temperature during cold exposure), Sminthopsis macroura, a small (approximately 25 g) insectivorous marsupial, is capable of entering torpor and whether torpor patterns change with growth. Endothermic thermoregulation was established when the nest young reached a body mass of approximately 10 g, and they were capable of entering torpor early during development at approximately 10-12 g, lending some support to the view that torpor is a phylogenetically old mammalian trait. Torpor bout length shortened significantly and the minimum metabolic rate during torpor increased as juveniles approached adult size, and consequently total daily energy expenditure increased steeply with age. Relationships between total daily energy expenditure and body mass during development of S. macroura (slope approximately 1.3) differed substantially from the relationship between basal metabolism and body mass in adult endotherms (slope approximately 0.75) suggesting that the energy expenditure-size relationship during the development differs substantially from that in adults under thermo-neutral conditions. Our study shows that while torpor can substantially reduce energy expenditure during development of endotherms and hence is likely important for survival during energy bottlenecks, it also may enhance somatic growth when food is limited. We therefore hypothesize that torpor during the development in endotherms is far more widespread than is currently appreciated.

Torpor expression in juvenile and adult Djungarian hamsters (Phodopus sungorus) differs in frequency, duration and onset in response to a daily cycle in ambient temperature

“…This is supported by earlier observations of T a changes being a potential to trigger for arousal from torpor in Djungarian hamsters (personal communication by Heldmaier as well as Blank and Ruf, cited in Ruf, 1991). This thermoregulatory behaviour of passive rewarming can be observed in many other small mammals like stripe-faced dunnarts, pouched mice, bats, shrews, deer mice and mouse lemurs that synchronize torpor expression with the daily changes in T a and thus can save a considerable amount of energy, otherwise needed for shivering thermogenesis (Dausmann et al, 2004;Geiser and Baudinette, 1985;Geiser et al, 2006Geiser et al, , 2004Lovegrove et al, 1999;Lovegrove and Raman, 1998;Mzilikasi et al, 2002;Park et al, 2000;Ruf, 1991;Turbill et al, 2008). To fully exploit the energetic benefits of passive rewarming, these mammals advance their torpor bout entrance into the dark phase and thus extend it long enough to sufficiently save energy without losing the arousal-supporting rise in T a towards noon maximum (Lovegrove et al, 1999;Ruf, 1991).…”

Heterothermy in pouched mammals – a review

“…The T b and BMR values were taken either from the original publications or from Clarke, Rothery & Isaac () and White, Blackburn & Seymour (), respectively. Torpor was defined as a reduction in metabolic rate below 75% of resting metabolic rate (RMR) and TBD as the time metabolic rate remained below 75% of RMR (Geiser et al ., ). Or, if only T b measurements were available, as the time T b remained below 30°C (Körtner & Geiser, ).…”

“…Data from published studies on 41 marsupial species (Australidelphia and Ameridelphia) were available for the present analysis ( (2009), respectively. Torpor was defined as a reduction in metabolic rate below 75% of resting metabolic rate (RMR) and TBD as the time metabolic rate remained below 75% of RMR (Geiser et al, 2006). Or, if only Tb measurements were available, as the time Tb remained below 30°C (Körtner & Geiser, 2000).…”

Developmental phenotypic plasticity in a marsupial

“…We quantified the occurrence, duration and depth of torpor bouts (TMR) as well as average daily MR (ADMR) at 16.0±0.1 and 24.0±0.1°C T a . Torpor was defined as a reduction in MR below 75% of RMR and torpor bout duration was calculated as the time MR remained below 75% RMR (Geiser et al, 2006). TMR was defined as the lowest of at least three continuous readings (i.e.…”