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

Thesis (Ph.D.)-University of KwaZulu-Natal, Pietermaritzburg, 2005.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

Heterothermy in Afrotropical mammals and birds : a review

Recent years have seen a rapid increase in the number of Afrotropical endotherms known to avoid mismatches between energy supply and demand by using daily torpor and/or hibernation. Among mammals, heterothermy has been reported in 40 species in six orders, namely Macroscelidea, Afrosoricida, Rodentia, Eulipotyphla, Primates and Chiroptera. These species span a range in body mass of 7–770 g, with minimum heterothermic body temperatures ranging from 1–278C and bout length varying from 1 h to 70 days. Daily torpor is the most common form of heterothermy, with true hibernation being observed in only seven species, Graphiurus murinus, Graphiurus ocularis, Atelerix frontalis, Cheirogaleus medius, Cheirogaleus major, Microcebus murinus and Microcebus griseorufus. The traditional distinction between daily torpor and hibernation is blurred in some species, with free-ranging individuals exhibiting bouts of 424 h and body temperatures 5168C, but none of the classical behaviours associated with hibernation. Several species bask in the sun during rewarming. Among birds, heterothermy has been reported in 16 species in seven orders, and is more pronounced in phylogenetically older taxa. Both in mammals and birds, patterns of heterothermy can vary dramatically among species occurring at a particular site, and even among individuals of a single species. For instance, patterns of heterothermy among cheirogalid primates in western Madagascar vary from daily torpor to uninterrupted hibernation for up to seven months. Other examples of variation among closely-related species involve small owls, elephant shrews and vespertilionid bats. There may also be variation in terms of the ecological correlates of torpor within a species, as is the case in the Freckled Nightjar Caprimulgus tristigma.The Mammal Research Institute, University of Pretoriahttp://icb.oxfordjournals.org/ab201

Seasonal metabolic variation in two populations of an Afrotropical euplectid bird

Many birds exhibit seasonal phenotypic flexibility in basal metabolic rate (BMR) and summit metabolism (Msum), but very little information is available for species from subtropical latitudes or for conspecific populations from sites that vary in climate. We measured body mass (Mb), BMR, and Msum in summer and winter in two populations of the southern red bishop Euplectes orix, a passerine that is widespread in southern Africa. One population occurs at a comparatively warmer coastal site (mean daily minimum air temperature [Ta] inmidwinter, 8.3 C) and the other at a colder inland site (mean daily minimum Ta in midwinter, 2.8 C). Bishops from both populations significantly increased Mb in winter. However, seasonal metabolic adjustments differed considerably between the populations. The inland population significantly increased BMR by approximately 58%, mass-specific BMR by approximately 31%, and Msum by approximately 15% in winter, although massspecific Msum did not change significantly. In contrast, the coastal population showed no significant seasonal change in BMR and significant winter reductions in mass-specific BMR (∼15%), Msum (∼8%), and mass-specific Msum (∼15%). The interpopulation differences in the magnitude and direction of seasonal mass-specific BMR changes are qualitatively consistent with global patterns, although the increase shown by the inland population is larger than expected. Our data reveal that avian seasonal metabolic adjustments can vary greatly within subtropical species depending on the climatic conditions experienced by the birds, and our findings reiterate the need to better understand metabolic flexibility in species that inhabit lower latitudes.The National Research Foundation (NRF) to N.M. and A.E.M.http://www.journals.uchicago.edu/toc/pbz/currentam2013ab201

Phenotypic flexibility in body mass, basal metabolic rate and summit metabolism in southern red bishops (Euplectes orix) : responses to short term thermal acclimation

Avian basal metabolic rate (BMR) and summit metabolism (Msum) vary within individuals in response to seasonal acclimatization in free-ranging birds, and thermal acclimation under laboratory conditions. We examined relationships between acclimation air temperature (Tacc) and body mass (Mb), BMR and Msum in female southern red bishops (Euplectes orix) from a relatively mild coastal site and a seasonally colder, inland site. Following acclimation for 21 days to Tacc = 10, 22 or 35 °C, Mb, BMR and Msum were all significantly and negatively related to Tacc. The significant relationship between BMR and Tacc did not remain after Mb was included as a covariate, whereas that between Msum and Tacc did. A subsequent reverse acclimation protocol, where bishops were acclimated to a second Tacc value and then re-acclimated to the first, revealed that short-term changes in Mb and BMR were completely reversible, but changes in Msum were only partially reversible. Following the reverse-acclimation protocol, metabolic expansibility (Msum/BMR) varied significantly with air temperature, being greatest at Tacc = 35 °C. Our data suggest that the intraspecific variation in seasonal metabolic variation previously reported for this species is at least partly driven by factors other than temperature.The National Research Foundation (NRF) for N.M. and A.E.Mhttp://www.elsevier.com/locate/cbpahb2013ab201

Solar radiation during rewarming from Torpor in elephant shrews : supplementation or substitution of endogenous heat production?

Many small mammals bask in the sun during rewarming from heterothermy, but the implications of this behaviour for their energy balance remain little understood. Specifically, it remains unclear whether solar radiation supplements endogenous metabolic thermogenesis (i.e., rewarming occurs through the additive effects of internally-produced and external heat), or whether solar radiation reduces the energy required to rewarm by substituting (i.e, replacing) metabolic heat production. To address this question, we examined patterns of torpor and rewarming rates in eastern rock elephant shrews (Elephantulus myurus) housed in outdoor cages with access to either natural levels of solar radiation or levels that were experimentally reduced by means of shade cloth. We also tested whether acclimation to solar radiation availability was manifested via phenotypic flexibility in basal metabolic rate (BMR), non-shivering thermogenesis (NST) capacity and/or summit metabolism (Msum). Rewarming rates varied significantly among treatments, with elephant shrews experiencing natural solar radiation levels rewarming faster than conspecifics experiencing solar radiation levels equivalent to approximately 20% or 40% of natural levels. BMR differed significantly between individuals experiencing natural levels of solar radiation and conspecifics experiencing approximately 20% of natural levels, but no between-treatment difference was evident for NST capacity or Msum. The positive relationship between solar radiation availability and rewarming rate, together with the absence of acclimation in maximum non-shivering and total heat production capacities, suggests that under the conditions of this study solar radiation supplemented rather than substituted metabolic thermogenesis as a source of heat during rewarming from heterothermy.The National Research Foundation and the University of Pretoria.http://www.plosone.orgam201

Torpor on Demand: Heterothermy in the Non-Lemur Primate Galago moholi

Hibernation and daily torpor are energy- and water-saving adaptations employed to survive unfavourable periods mostly in temperate and arctic environments, but also in tropical and arid climates. Heterothermy has been found in a number of mammalian orders, but within the primates so far it seems to be restricted to one family of Malagasy lemurs. As currently there is no evidence of heterothermy of a primate outside of Madagascar, the aim of our study was to investigate whether small primates from mainland Africa are indeed always homeothermic despite pronounced seasonal changes in weather and food availability., which inhabits a highly seasonal habitat with a hot wet-season and a cold dry-season with lower food abundance, was investigated to determine whether it is capable of heterothermy. We measured skin temperature of free-ranging individuals throughout the cool dry season using temperature-sensitive collars as well as metabolic rate in captured individuals. Torpor was employed by 15% of 20 animals. Only one of these animals displayed heterothermy in response to natural availability of food and water, whereas the other animals became torpid without access to food and water. are physiologically capable of employing torpor. However they do not use it as a routine behaviour, but only under adverse conditions. This reluctance is presumably a result of conflicting selective pressures for energy savings versus other ecological and evolutionary forces, such as reproduction or territory defence. Our results support the view that heterothermy in primates evolved before the division of African and Malagasy Strepsirhini, with the possible implication that more primate species than previously thought might still have the potential to call upon this possibility, if the situation necessitates it

Does torpor of elephant shrews differ from that of other heterothermic mammals?

Torpor bouts of elephant shrews are intermediate in duration to those of daily heterotherms and hibernating mammals, but their body temperatures (Tbs) and metabolic rates are very low and similar to those of hibernating mammals. We quantified the thermal physiology of the Cape rock elephant shrew ('Elephantulus edwardii'), a species endemic to high-altitude regions of South Africa, where winters are cold and wet, and tested whether it displays multiday torpor characteristic of hibernators at low ambient temperature (Ta). 'E. edwardii' regularly displayed torpor over a wide range of Tas. Occurrence of torpor and duration of torpor bouts increased with decreasing Ta. Whereas normothermic Tb was stable, Tb in torpid individuals fell with Ta. The mean Tb - Ta differential at the minimum Tb was 0.7°C, and the mean minimum Tb at Ta 8.9°C was 9.3°C. Duration of torpor bouts ranged from 6.5 to 44 h and was correlated negatively with Ta and Tb during torpor. Time required for the reduction of Tb to a Tb - Ta differential of 1-day torpor bouts than those lasting ≤1 day, suggesting that the duration of a bout might be determined at the beginning, not during, a bout. The nature of heterothermy in E. edwardii seems qualitatively similar to that of other elephant shrews, although torpor is somewhat deeper and longer in this species. Temporal patterns of torpor in E. edwardii differ from those of most cold-climate hibernators, likely for ecological rather than physiological reasons

Torpor on Demand: Heterothermy in the Non-Lemur Primate Galago moholi

Background: Hibernation and daily torpor are energy- and water-saving adaptations employed to survive unfavourable periods mostly in temperate and arctic environments, but also in tropical and arid climates. Heterothermy has been found in a number of mammalian orders, but within the primates so far it seems to be restricted to one family of Malagasy lemurs. As currently there is no evidence of heterothermy of a primate outside of Madagascar, the aim of our study was to investigate whether small primates from mainland Africa are indeed always homeothermic despite pronounced seasonal changes in weather and food availability. Methodology/Principal Findings: One of the nearest relatives of Malagasy lemurs, the African lesser bushbaby, Galago moholi, which inhabits a highly seasonal habitat with a hot wet-season and a cold dry-season with lower food abundance, was investigated to determine whether it is capable of heterothermy. We measured skin temperature of free-ranging individuals throughout the cool dry season using temperature-sensitive collars as well as metabolic rate in captured individuals. Torpor was employed by 15 % of 20 animals. Only one of these animals displayed heterothermy in response to natural availability of food and water, whereas the other animals became torpid without access to food and water. Conclusions/Significance: Our results show that G. moholi are physiologically capable of employing torpor. However they do not use it as a routine behaviour, but only under adverse conditions. This reluctance is presumably a result of conflictin

Torpor as an emergency solution in 'Galago moholi': heterothermy is triggered by different constraints

The expression of heterothermy in the African lesser bushbaby, 'Galago moholi', seems to be strikingly different to most other heterotherms: 'G. moholi' uses its ability to enter torpor only rarely and torpor is only used by a small fraction of the population. The aim of this study was, therefore, to summarize the parameters of torpor use in 'G. moholi' to conclude the general patterns and discuss them in comparison to other heterotherms to elucidate possible causes and constraints that underlie these differences in deployment of heterothermy. Our study was carried out on wild animals using temperature loggers and open-flow respirometry for measurements of body temperature and metabolic rate, respectively. 'G. moholi' uses torpor only as a last resort and not as a routine, seasonal behavior. Nevertheless, we found that the general physiological patterns of torpor, e.g., torpor bout duration or entry and arousal times from torpor, were mainly consistent with those described for other nocturnal daily heterotherms. The greatest difference found was the unusual low rewarming rates during arousal from torpor, probably due to already depleted internal energy stores and thus inability to mobilize sufficient energy for endogenous heating. We therefore conclude that while general physiological parameters of heterothermy seem to have remained conserved in heterotherms, the underlying causes which elicit this physiological response, and thus the extent of expression and timing of heterothermy, have evolved very differently in different groups, depending on body mass and the specific habitat and lifestyle of the species

Nonshivering thermogenesis in the African lesser bushbaby, 'Galago moholi'

The capacity for nonshivering thermogenesis (NST) plays an important role during arousal from torpid states. Recent data on heterotherms inhabiting warmer regions, however, suggest that passive rewarming reduces the need of metabolic heat production during arousal significantly, leading to the question: to what extent do subtropical or tropical heterotherms depend on NST? The African lesser bushbaby, 'Galago moholi', enters torpid states as an emergency response only, but otherwise stays normothermic throughout the cold and dry winter season. In addition, this species shows unusual rewarming difficulties during arousal from torpor on cold days. We therefore examined the seasonal adjustments of the capacity for NST of naturally acclimatized G. moholi by stimulation with noradrenaline (NA) injection. Dissection of two adult female bushbabies revealed that 'G. moholi' possesses brown adipose tissue, and NA treatment (0.5 mg kg-1, s.c.) induced a significant elevation in oxygen consumption compared with control (saline) injection. However, the increase in oxygen consumption following injection of NA was not significantly different between winter and summer. Our results show that the ability to produce heat via NST seems to be available throughout the year and that 'G. moholi' is able to change NST capacity within a very short time frame in response to cold spells. Together with results from studies on other (Afro-)tropical heterotherms, which also indicate low or even absent seasonal difference in NST capacity, this raises the question of whether the definition of NST needs to be refined for (Afro-)tropical mammals