Saving energy via short and shallow torpor bouts.

Maintaining a high and stable body temperature as observed in most endothermic mammals and birds is energetically costly and many heterothermic species reduce their metabolic demands during energetic bottlenecks through the use of torpor. With the increasing number of heterotherms revealed in a diversity of habitats, it becomes apparent that triggers and patterns of torpor use are more variable than previously thought. Here, we report the previously overlooked use of, shallow rest-time torpor (body temperature >30 °C) in African lesser bushbabies, Galago moholi. Body core temperature of three adult male bushbabies recorded over five months showed a clear bimodal distribution with an average active modal temperature of 39.2 °C and a resting modal body temperature of 36.7 °C. Shallow torpor was observed in two out of three males (n = 29 torpor bouts) between June and August (austral winter), with body temperatures dropping to an overall minimum of 30.7 °C and calculated energy savings of up to 10%. We suggest that shallow torpor may be an ecologically important, yet mostly overlooked energy-saving strategy employed by heterothermic mammals. Our data emphasise that torpor threshold temperatures need to be used with care if we aim to fully understand the level of physiological plasticity displayed by heterothermic species.

Obligatory homeothermy of mesic habitat-adapted African striped mice, Rhabdomys pumilio, is governed by seasonal basal metabolism and year-round 'thermogenic readiness' of brown adipose tissue.

Small mammals undergo thermoregulatory adjustments in response to changing environmental conditions. Whereas small heterothermic mammals can employ torpor to save energy in the cold, homeothermic species must increase heat production to defend normothermia through the recruitment of brown adipose tissue (BAT). Here, we studied thermoregulatory adaptation in an obligate homeotherm, the African striped mouse (Rhabdomys pumilio), captured from a subpopulation living in a mesic, temperate climate with marked seasonal differences. Basal metabolic rate (BMR), non-shivering thermogenesis (NST) and summit metabolic rate (Msum) increased from summer to winter, with NST and Msum already reaching maximal rates in autumn, suggesting seasonal preparation for the cold. Typical of rodents, cold-induced metabolic rates were positively correlated with BAT mass. Analysis of cytochrome c oxidase (COX) activity and UCP1 content, however, demonstrated that thermogenic capacity declined with BAT mass. This resulted in seasonal differences in NST being driven by changes in BMR. The increase in BMR was supported by a comprehensive anatomical analysis of metabolically active organs, revealing increased mass proportions in the cold season. The thermoregulatory response of R. pumilio was associated with the maintenance of body mass throughout the year (48.3±1.4 g), contrasting large summer-winter mass reductions often observed in Holarctic rodents. Collectively, bioenergetic adaptation of this Afrotropical rodent involves seasonal organ adjustments influencing BMR, combined with a constant thermogenic capacity dictated by trade-offs in the thermogenic properties of BAT. Arguably, this high degree of plasticity was a response to unpredictable cold spells throughout the year. Consequently, the reliance on such a resource-intensive thermoregulatory strategy may expose more energetic vulnerability in changing environments of food scarcity and extreme weather conditions due to climate change, with major ramifications for survival of the species.

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.

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.

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 21days 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.

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 (M(sum)), 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 (M(b)), BMR, and M(sum) 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 [T(a)] in midwinter, 8.3°C) and the other at a colder inland site (mean daily minimum T(a) in midwinter, -2.8°C). Bishops from both populations significantly increased M(b) 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 M(sum) by approximately 15% in winter, although mass-specific M(sum) 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%), M(sum) (~8%), and mass-specific M(sum) (~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.

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.

Seasonal changes in thermogenesis of a free-ranging afrotherian small mammal, the Western rock elephant shrew (Elephantulus rupestris).

We report on the seasonal metabolic adjustments of a small-sized member of the phylogenetically ancient Afrotheria, the Western rock elephant shrew (Elephantulus rupestris). We recorded body temperature (T (b)) patterns and compared the capacity for adrenergically induced nonshivering thermogenesis (NST) in E. rupestris captured in the wild in summer and winter. Noradrenaline (NA) treatment (0.4-0.5 mg/kg, s.c.) induced a pronounced elevation in oxygen consumption compared to controls (saline), and the increase in oxygen consumption following injection of NA was 1.8-fold higher in winter compared to summer. This suggests that the smaller members of Afrotheria possess functional brown adipose tissue, which changes in thermogenic capacity depending on the season. Torpor was recorded in both seasons, but in winter the incidence of torpor was higher (n = 205 out of 448 observations) and minimal T (b) during torpor was lower (T (b)min: 11.9°C) than in summer (n = 24 out of 674 observations; T (b)min: 26°C). In addition to cold, high air humidity emerged as a likely predictor for torpor entry. Overall, E. rupestris showed a high degree of thermoregulatory plasticity, which was mainly reflected in a variable timing of torpor entry and arousal. We conclude that E. rupestris exhibits seasonal metabolic adjustments comparable to what has been long known for many Holarctic rodents.

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 1-27°C 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 > 24 h and body temperatures < 16 °C, 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.

Ticks of four-toed elephant shrews and Southern African hedgehogs.

Several studies on ticks infesting small mammals, including elephant shrews, have been conducted in South Africa; however, these studies have included only a single four-toed elephant shrew and no hedgehogs. This study thus aimed to identify and quantify the ixodid ticks infesting four-toed elephant shrews and Southern African hedgehogs. Four-toed elephant shrews (Petrodromus tetradactylus) were trapped in dense shrub undergrowth in a nature reserve in north-eastern KwaZulu-Natal. They were separately housed, first in cages and later in glass terraria fitted with wire-mesh bases to allow detached ticks to fall through for collection. Southern African hedgehogs (Atelerix frontalis) were hand caught on a farm in the eastern region of the Northern Cape Province and all visible ticks were collected by means of tweezers while the animals were anaesthetised. The ticks from each animal were preserved separately in 70% ethanol for later identification and counting. The immature stages of five ixodid tick species were collected from the elephant shrews, of which Rhipicephalus muehlensi was the most common. It has not been recorded previously on any species of elephant shrew. Three ixodid tick species were collected from the hedgehogs. Large numbers of adult Haemaphysalis colesbergensis, which has not been encountered previously on hedgehogs, were collected from these animals. Four-toed elephant shrews are good hosts of the larvae and nymphs of R. muehlensi, and Southern African hedgehogs are good hosts of adult H. colesbergensis.

Heterothermy in the southern African hedgehog, Atelerix frontalis.

Most research on mammalian heterothermic responses in southern Africa tends to be laboratory based and biased towards rodents and smaller members of the Afrotheria. In this study, we continuously measured body temperature of southern African hedgehogs (Atelerix frontalis) between April and August 2009 (-10°C < T (a) < 43°C), kept under semi-captive conditions. A. frontalis showed a high propensity for torpor with animals spending up to 84% of the measurement period torpid. During this study, A. frontalis displayed the lowest T (b min) (ca 1°C) yet recorded in an Afrotropical placental heterotherm. Bout lengths of between 0.7 h (40 min) and 116.3 h (4.8 days) were recorded. Differences in bout length were observed between lighter individuals compared with an individual exhibiting a higher body mass at the onset of winter, with low M (b) individuals exhibiting daily torpor whereas a heavier individual exhibited torpor bouts that were indicative of hibernation. Our results suggest that heterothermic responses are an important feature in the energy balance equation of this species and that body mass at the onset of winter may determine the patterns of heterothermy utilised in this species.

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 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.

The molecular and biochemical basis of nonshivering thermogenesis in an African endemic mammal, Elephantulus myurus.

Uncoupling protein 1 (UCP1) mediated nonshivering thermogenesis (NST) in brown adipose tissue (BAT) is an important avenue of thermoregulatory heat production in many mammalian species. Until recently, UCP1 was thought to occur exclusively in eutherians. In the light of the recent finding that UCP1 is already present in fish, it is of interest to investigate when UCP1 gained a thermogenic function in the vertebrate lineage. We elucidated the basis of NST in the rock elephant shrew, Elephantulus myurus (Afrotheria: Macroscelidea). We sequenced Ucp1 and detected Ucp1 mRNA and protein restricted to brown fat deposits. We found that cytochrome c oxidase activity was highest in these deposits when compared with liver and skeletal muscle. Consistent with a thermogenic function of UCP1 isolated BAT mitochondria showed increased state 4 respiration in the cold, as well as palmitate-induced, GDP-sensitive proton conductance, which was absent in liver mitochondria. On the whole animal level, evidence of thermogenic function was further corroborated by an increased metabolic response to norepinephrine (NE) injection. Cold acclimation (18 degrees C) led to an increased basal metabolic rate relative to warm acclimation (28 degrees C) in E. myurus, but there was no evidence of additional recruitment of NE-induced NST capacity in response to cold acclimation. In summary, we showed that BAT and functional UCP1 are already present in a member of the Afrotheria, but the seasonal regulation and adaptive value of NST in Afrotherians remain to be elucidated.

Lack of torpor in free-ranging southern lesser galagos, Galago moholi: ecological and physiological considerations.

Studies investigating heterothermy under natural conditions are particularly scarce for tropical species. However, heterothermy patterns in tropical and subtropical environments often differ markedly from those observed in arctic and temperate species. The investigation of heterothermy in strepsirhine primates has focussed largely on the Malagasy cheirogaleids. In addition, a physiological verification of torpor occurrence in mainland strepsirhines is important with regard to arguments pertaining to the colonization of Madagascar by strepsirhine primates. We measured body temperatures of 11 free-ranging Galago moholi, between February 2002 and September 2003, for 3 consecutive months for each animal. No incidents of heterothermy were recorded throughout the study period. We considered how physiological and ecological aspects of G. moholi biology might have obviated the use of torpor. It was suggested that the breeding pattern observed in G. moholi prevented torpor use whilst increasing fecundity, and that the ecological costs of torpor far outweighed the energetic costs. This study highlights the need for more studies on free-ranging animals to elucidate the physiological, ecological and phylogenetic constraints and determinants of torpor use. Furthermore, if convincing arguments are to be made regarding the possible role of heterothermy in species dispersal, more data from free-ranging animals are needed.

Noradrenalin induces thermogenesis in a phylogenetically ancient eutherian mammal, the rock elephant shrew, Elephantulus myurus.

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 non-shivering thermogenesis (NST). In marsupials, heat is primarily produced through shivering and NST in skeletal muscle because BAT is either absent or appears to be non-functional. The most basal group of the eutherian lineage are the Afrotheria. Rock elephant shrews, Elephantulus myurus are amongst the smallest members of the Afrotheria and are also known to use exogenous passive heating. The aim of this study was to determine whether the reliance on passive heating compromised the capacity for thermogenesis in E. myurus. We measured the thermogenic response to noradrenalin (NA) injection in E. myurus acclimated to short photoperiod. The thermogenic response at 25 degrees C was 1.58 ml O(2) g(-1) h(-1). We used phylogenetically independent analyses to establish how this thermogenic response compared to other eutherians that display classical NST. The thermogenic response of E. myurus was not significantly different from phylogenetically independent allometric predictions. However, it is unclear whether this thermogenic response is indicative of classical NST and molecular data are required to verify the presence of BAT and UCPs in elephant shrews.

Daily torpor in free-ranging rock elephant shrews, Elephantulus myurus: a year-long study.

Under laboratory conditions, rock elephant shrews, Elephantulus myurus, use daily torpor under both short and long photoperiod acclimation. However, use of heterothermy often differs under field and laboratory conditions. We investigated the use of torpor in free-ranging elephant shrews from May 2001 to May 2002. The elephant shrews were capable of daily torpor throughout the year, with torpor most prevalent during winter. We recorded two torpor bouts during early summer (November). We recorded a total of 467 torpor bouts during the year. The mean torpor minimum body temperature (Tbmin) for the whole year was 15.3 degrees +/-4.4 degrees C, and the mean bout length was 8.6+/-3.5 h. These values 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 h in duration, and Tbmin decreased below 10 degrees C. Torpor was highly correlated with low ambient temperature and photoperiod. Torpor was also correlated with invertebrate abundance after controlling for photoperiod effects. During the year in which this study was conducted, the rainfall was 14% below long-term average. Historical rainfall records show that summer rainfall during strong El Nino years is up to 40% below the long-term average. During these drought years, the frequency of summer torpor may be higher, highlighting the need for long-term physiological data in free-ranging animals.

Reproductive activity influences thermoregulation and torpor in pouched mice, Saccostomus campestris.

The Afrotropical pouched mouse Saccostomus campestris displays sexual disparity in the use of daily torpor; males reluctantly enter torpor. We tested the hypothesis that males may compensate for a limited heterothermic capacity with lower basal and resting metabolic rates relative to females. We also investigated the association between gonadal activity (testosterone) and the propensity for daily torpor. Body temperature and oxygen consumption were measured at various ambient temperatures and were compared between sexes under ad libitum and restricted-diet treatments. Whereas no significant sex differences were observed in body temperature and oxygen consumption under ad libitum treatment, there were pronounced differences in heterothermic responses under food restriction. Females employed torpor more frequently and also had lower minimum torpor body temperatures (ca. 25 degrees C) than males (ca. 29 degrees C). Testosterone inhibited torpor in males, whereas the majority of saline-treated animals employed torpor under both ad libitum and restricted-diet treatments. This study demonstrated that the limited capacity of male S. campestris to enter torpor is a consequence of reproductive activity and that opportunistic breeding and the absence of seasonal testes regression compromises the capacity to conserve energy through daily torpor.

Exogenous passive heating during torpor arousal in free-ranging rock elephant shrews, Elephantulus myurus.

In the laboratory rock elephant shrews (Elephantulus myurus; mean body mass 56.6 g) displayed the lowest torpor T b min yet recorded (ca. 5°C) in a placental daily heterotherm. It was unknown whether these low T bs were characteristic of daily heterothermy in free-ranging animals. It was also unclear how cost effective these low T bs were since considerable energy is required to arouse from low T bs on a daily basis. We continuously measured body temperature once every hour for 85 days in 13 free-ranging E. myurus from May to August 2001 (winter) in Weenen Game Reserve, KwaZulu-Natal, South Africa. We recorded a total of 412 torpor bouts. Free-ranging E. myurus had a high propensity for torpor with females displaying higher torpor frequency than males. The lowest T b recorded was 7.5°C at T a=2.7°C and the minimum torpor T b was strongly correlated with ambient temperature. Torpor arousal was tightly coupled with ambient temperature cycles. Low torpor T b min at low T as was therefore cost-effective because the animals offset the high cost of arousal through exogenous passive heating. Laboratory studies under constant ambient temperatures may therefore underestimate the energetic benefits of torpor in free-ranging small mammals that inhabit regions where seasonality is moderate.