Thermoregulation in free-ranging African-endemic small mammals : the rock elephant shrew, Elephantulus myurus and the lesser bushbaby, Galago moholi.

Abstract

Endothermy in birds and mammals is invariably associated with homeothermy. However, homeothermy can only be maintained if sufficient energy is obtained to meet the animals' maintenance budget. In mammals, daily torpor and hibernation have evolved to conserve energy when energy inputs from the environment are insufficient to meet maintenance requirements. Several studies have suggested that daily torpor and hibernation do not represent distinct physiological responses but are components of a continuum of heterothermy. Under laboratory conditions, even within phylogenetically ancient eutherian mammals, such as elephant shrews, it is unclear whether daily torpor or hibernation is used. Furthermore, an interpretation of the torpor patterns observed under laboratory conditions is complicated by the fact that torpor patterns often differ between laboratory and free-ranging conditions. Within the more recent mammal lineages, torpor has been observed in strepsirrhine primates. The occurrence of torpor in strepsirrhines is interesting as it pertains to arguments relating to the colonization of Madagascar by strepsirrhine primates as well as implications for human physiology. The first aim of this study was to investigate and quantify parameters that characterize torpor in a phylogenetically ancient eutherian mammal (Macroscelidae: Elephantulus myurus) under free-ranging conditions. This was done mainly to resolve whether daily torpor and hibernation were physiologically discrete responses. The second aim was to investigate torpor occurrence in a more recently evolved eutherian mammal (Primates: Galago moholi). The objective was to gain insights into the phylogenetic distribution of torpor and to provide a physiological verification of torpor occurrence in a mainland strepsirrhine relative to arguments about the colonization of Madagascar. I measured body temperatures in three monthly cycles between May 2001 - May 2002 in 22 free-ranging E. myurus. I recorded a total of 467 torpor bouts throughout the study period. The elephant shrews were capable of daily torpor throughout the year, with torpor most prevalent during winter and correlated with ambient temperature, photoperiod and invertebrate abundance. Only two torpor bouts were observed during summer. I suggest that although torpor use was most prevalent during winter, summer torpor might also be important for energy conservation in this species during drought years. This highlights the need for long-term physiological data in free-ranging animals. The mean torpor Tbmin and the mean bout length for the whole year were in the range expected for daily heterotherms. However, there was some marginal overlap with hibernation characteristics; a few torpor bouts were longer than 24 hrs in duration indicating that the animals were capable of opportunistically extending torpor bouts longer than 24 hours in response to unpredictable energetic shortfalls. Tbmin also decreased below 10°C. However, a consideration of behavioural and ecological factors argues against hibernation in E. myurus. Instead, these results support the idea of a physiological continuum for heterothermy. A return to normothermic body temperatures requires considerable energy expenditure, and this is perceived to be one of the major disadvantages of torpor. E. myurus offset the high cost of arousal from low body temperatures by using exogenous passive heating. This is achieved by coupling of the timing of arousal with ambient temperature cycles. Laboratory studies that quantify torpor energetics are usually conducted under constant temperature conditions and are likely to underestimate the energetic benefits accrued through the use of ambient temperature cycles during arousal. Torpor is often displayed during the animal's rest phase. However, nocturnal small mammals that utilize passive heating to assist arousal from torpor may enter torpor during the nighttime, thus effectively advancing the onset of the rest phase. I investigated the functional significance of daily and seasonal rhythms of body temperature in normothermic and torpid free-ranging E. myurus. Daily patterns of Tb, in normothermic E. myurus suggested polyphasic Tb patterns that nevertheless indicated a rest phase coincident with the daytime. I suggested that the principal benefit of a flexible daily rhythm of Tb, is that it facilitated torpor use during the nighttime and arousal by passive exogenous heating using ambient temperature cycles. It has been suggested that the evolution of endothermy precluded the need for homeothermic mammals to be sensitive to Ta cycles because they could maintain physiological function despite fluctuations in the ambient temperature. Elephant shrews utilize passive heating and provide excellent models with which to investigate whether mammals can entrain their body temperature rhythms to ambient temperature cycles. I experimentally tested whether food restricted E. myurus can entrain torpor cycles to shifts in the Ta cycle while holding the light-dark cycle constant. Food restriction and short photoperiod were only sufficient to induce torpor in E. myurus if photoperiod and Ta, cycles are in phase with each other. Shifting the cold T, into the photophase prevented the expression of torpor. I concluded that the body temperature rhythm is most probably tightly coupled with the photoperiod cycle and that although Ta and photoperiod usually act synergistically in nature, photoperiod is probably the stronger zeitgeber. The evolution of endothermy is thought to have been facilitated by the advent of endothermic energy sources such as brown adipose tissue (BAT), the principal site of nonshivering thermogenesis (NST). Rock elephant shrews are amongst the smallest members of the Afrotheria, the most basal of the eutherian lineage. I determined whether the phylogenetic placement of E. myurus and reliance on passive heating might result in a decreased capacity for NST relative to other eutherians. I investigated the capacity for NST in winter acclimated E. myurus by measuring the thermogenic response to noradrenalin (NA) injection. I used phylogenetically independent analyses to compare E. myurus NST capacity with other eutherians. E. myurus had an NST capacity that was no different from other eutherian mammals. Although they displayed a NST capacity that was 74% of that expected on the basis of body mass, this value was not significantly different from phylogenetically independent allometric predictions. Although heterothermy is almost always considered in the context of how the environment affects function , its use may offer insights into topics such as island biogeography and species dispersal. For example, there have been suggestions that heterothermy might have played an important role in the successful colonization of Madagascar by strepsirrhine primates. To my knowledge no studies exist as yet that provide a physiological verification of this suggestion. Currently no data exist on thermoregulation and heterothermy in any free-ranging African strepsirrhines. The lesser bushbaby, Galago moholi, is a small nocturnal strepsirrhine primate that experiences severe winters and drastic food reduction during winter and is a candidate employer of torpor. I measured body temperatures of 11 free-ranging lesser bushbabies, Galago moholi, captured at different times between February 2002 - September 2003. I did not record any incidents of heterothermy throughout the study period. Why does G. moholi not employ heterothermy? I consider several alternatives; phylogenetic placement, physiological and ecological factors that might preclude the use of torpor in this species. I suggest that the breeding pattern observed in G. moholi obviates torpor use whilst increasing fecundity, which would be adaptive if the animals are confronted with high predation risks. Much is currently known about the advantages of torpor use. This study highlights the need to consider and investigate those physiological, ecological and phylogenetic factors that might constrain species from utilizinq heterothermy. Furthermore, this study highlights the potential for thermoregulatory studies to offer insights into topics as widely separated as evolution of endothermy to species dispersal and island biogeography.