Thermoregulation in free‐ranging ground woodpeckers Geocolaptes olivaceus: no evidence of torpor

Heterothermic responses characterised by pronounced hypometabolism and reductions in body temperature (T_b) are one of the most effective ways in which small endotherms can offset the energetic cost of endothermic homeothermy. It remains unclear, therefore, why daily torpor and hibernation are restricted to only a subset of avian lineages. To further our understanding of the phylogenetic distribution of avian torpor, we investigated winter thermoregulation in the southern African ground woodpecker Geocolaptes olivaceus. We considered this species a good candidate for heterothermy, because it is resident year‐round in mountainous regions with cold winters and reliant on small ectothermic prey. We recorded T_b patterns in free‐ranging individuals and measured T_b and metabolic rates in captive individuals. Neither free‐ranging nor captive woodpeckers showed any indication of daily torpor or even shallow rest‐phase hypothermia. All birds maintained bimodally distributed T_b characteristic of classic endothemic homeothermy, with a mean rest‐phase T_b of 37.9 ± 0.2°C and no data below 37.0°C. The mean circadian amplitude of T_b was 4.2°C, equivalent to approximately twice the expected value. There was some evidence of seasonal acclimatisation in T_b, with a small decrease in rest‐phase T_b with the onset of the austral winter. Captive birds showed patterns of resting metabolic rate and T_b consistent with the classic model of endothermic homeothermy. The apparent absence of torpor in G. olivaceus supports the notion that, unlike the case in mammals, many avian taxa that may a priori be expected to benefit from deep heterothermy do not use it.     

Baby in the bathwater: Should we abandon the use of body temperature thresholds to quantify expression of torpor?

Boyles et al. (this issue) argue against the use of body temperature (T_b) thresholds to quantify the expression of torpor in endotherms and our purpose is to provide a counterpoint argument. We contend that T_b thresholds provide valuable information about ecological factors influencing the evolution of thermoregulation. We also point out shortcomings of the so-called heterothermy index proposed as an alternative. However, to be clear, we do agree with Boyles et al. (this issue) that the use of torpor thresholds can limit some aspects of the study of thermoregulation and applaud the more widespread incorporation of theoretical underpinnings proposed by Boyles et al. (this issue) and others.     

Absence of heterothermy in the European red squirrel (Sciurus vulgaris)

The European red squirrel Sciurus vulgaris inhabits areas which undergo profound seasonal declines in food availability and ambient temperature. We measured the body temperature (T_b) of free-ranging S. vulgaris over the course of one year to examine its thermoregulatory strategies and found no evidence of heterothermy, with T_b never dropping below 36.7 °C. A lower average T_b and a reduced active phase are likely to have resulted in some energetic savings, sufficient for survival during the particularly mild winter with unhindered access to food stores. We cannot exclude that a different T_b pattern may be seen in energetically more demanding years, but we can confirm that heterothermy is not an obligatory behaviour in this species to counter energetic bottlenecks. Either S. vulgaris is indeed a strict homeotherm, or the need for torpor is flexibly adjusted.     

Body temperature variation in free-living and food-deprived yellow-necked mice sustains an adaptive framework for endothermic thermoregulation

In many mammalian species, variation in body temperature (T_b) exceeds the values suitable for defining homeothermy, making it justifiable and even necessary to resort to the term “heterothermic”. However, T_b data are only available for ca. 1% of extant mammalian species. We investigated variations in T_b in wild free-living and experimentally food-deprived yellow-necked mice Apodemus flavicollis, during the temperate-zone autumn-winter period. In line with the adaptive framework for endothermic thermoregulation, we hypothesised that T_b in the mice should be adjustable with the energetic cost-benefit trade-off associated with maintaining homeothermy. In laboratory conditions, mice clearly entered a state of daily torpor when food-deprived. Our study thus makes it clear that A. flavicollis is a heterothermic species in which food deprivation results in switching between endothermic and poikilothermic thermoregulation. We also assumed that, in free-living mice, heterothermy increases with elevated environmental challenges, e.g. when the ambient temperature (T_a) decreases. Consistent with this was the inverse correlation noted between variation in T_b in free-living mice and T_a, with most individuals clearly becoming torpid when T_a decreases below 0 °C. It is the increased cost of food hoarding under cold conditions that most likely triggers a state of torpor as a last result. Overall, our study indicates that yellow-necked mice can provide a further example of species sustaining an adaptive framework for endothermic thermoregulation.     

Surviving the Cold, Dry Period in Africa: Behavioral Adjustments as an Alternative to Heterothermy in the African Lesser Bushbaby (Galago moholi)

Behavioral and physiological adaptations are common and successful strategies used by small endothermic species to adjust to unfavorable seasons. Physiological adaptations, such as heterothermy, e.g., torpor, are usually thought to be more effective energy-saving strategies than behavioral adjustments. The African lesser bushbaby, Galago moholi, is physiologically capable of torpor but expresses heterothermy only under conditions of extreme energy limitation, suggesting that it has evolved alternative strategies to compensate energetic bottlenecks. We hypothesized that Galago moholi survives the unfavorable winter period, without —or only rarely— employing torpid phases to save energy, by using behavioral thermoregulation. We compared the ecology and behavior of Galago moholi in summer and winter by telemetric tracking and examined food availability by determination of arthropod and gum availability. We found a significant increase in huddling behavior and a significant increase in the use of enclosed and insulated sleeping sites during winter, as well as a reduction in nightly activity. Galago moholi hunted for insects significantly less in winter than in summer, and increased gum intake in winter, when gum showed an increase in energy content. The availability of high-quality food, albeit in low quantities, presumably enables Galago moholi to stay normothermic throughout the cold, dry period and to focus on reproduction activities. We propose that Galago moholi favors ecological and behavioral adjustments over torpor because these are sufficient to meet energy requirements of this species, and their advantages (flexibility, unrestricted activity, and reproduction) outweigh the energetic benefits of heterothermy.     

Thermoregulation in African Green Pigeons (Treron calvus) and a re-analysis of insular effects on basal metabolic rate and heterothermy in columbid birds

Columbid birds represent a useful model taxon for examining adaptation in metabolic and thermal traits, including the effects of insularity. To test predictions concerning the role of insularity and low predation risk as factors selecting for the use of torpor, and the evolution of low basal metabolic rate in island species, we examined thermoregulation under laboratory and semi-natural conditions in a mainland species, the African Green Pigeon (Treron calvus). Under laboratory conditions, rest-phase body temperature (T _b) was significantly and positively correlated with air temperature (T _a) between 0 and 35 °C, and the relationship between resting metabolic rate (RMR) and T _a differed from typical endothermic patterns. The minimum RMR, which we interpret as basal metabolic rate (BMR), was 0.825 ± 0.090 W. Green pigeons responded to food restriction by significantly decreasing rest-phase T _b, but the reductions were small (at most ~5 °C below normothermic values), with a minimum T _b of 33.1 °C recorded in a food-deprived bird. We found no evidence of the large reductions in T _b and metabolic rate and the lethargic state characteristic of torpor. The absence of torpor in T. calvus lends support to the idea that species restricted to islands that are free of predators are more likely to use torpor than mainland species that face the risk of predation during the rest-phase. We also analysed interspecific variation in columbid BMR in a phylogenetically informed framework and verified the conclusions of an earlier study which found that BMR is significantly lower in island species compared to those that occur on mainlands.     

Seasonal energetics and torpor use in North American flying squirrels

Seasonal cold temperatures require mammals to use morphological, behavioural, or physiological traits to survive periods of extreme cold and food shortage. Torpor is a physiological state that minimizes energy requirements by decreasing resting metabolic rate (MR) and body temperature (T_b). Many rodent species are capable of torpor, however, evidence in northern and southern flying squirrels (Glaucomys sabrinus and Glaucomys volans, respectively) has remained anecdotal. We experimentally attempted to induce torpor in wild-caught flying squirrels by lowering ambient temperature (T_a) and measuring MR using open-flow respirometry. We also studied seasonal differences in MR and T_b at various T_a. Both MR and T_b provided evidence for torpor in flying squirrels, but only infrequent, shallow torpor. MR decreased infrequently and any decreases were rarely sustained for longer than one hour. We found a significant positive relationship between T_a and T_b only in G. volans, which suggests that G. volans is more susceptible to low T_a compared with G. sabrinus, possibly due to their small body size. We observed no substantive seasonal or interspecific differences in the relation between MR and T_a, with the exception that northern flying squirrels expended more energy at cold T_a during warm season trials than other species-season combinations. The infrequency of torpor use in our experiments suggests that other energy-saving strategies, such as social thermoregulation, may limit the reliance on torpor in this lineage.     

Heterothermy in an Australian passerine, the Dusky Woodswallow (Artamus cyanopterus)

Information regarding passerine heterothermy and torpor is scant, although many species are small and must cope with a fluctuating food supply and presumably would benefit from energy savings afforded by torpor. We studied whether insectivorous Dusky Woodswallows (Artamus cyanopterus; ∼35 g) enter spontaneous torpor (food ad libitum) when held outdoors as a pair in autumn/winter. Woodswallows displayed pronounced and regular daily fluctuations in body temperature (T _b) over the entire study period. The mean T _b ranged from ∼39°C to 40°C (photophase, day time) and ∼33°C to 36°C (scotophase, night time). However, on 88% of bird nights, nocturnal T _b minima fell to < 35°C. The lowest T _b observed in air was 29.2°C. However, when a bird fell into water its T _b dropped further to ∼22°C; this T _b was regulated for several hours and the bird survived. Our observations suggest that heterothermy is a normal part of the daily thermal regime for woodswallows to minimise energy expenditure. Spontaneous nocturnal torpor in captive woodswallows suggests that torpor in the wild may be more pronounced than recorded here because free-living birds are likely challenged by both low food availability and adverse weather.     

Seasonality of torpor and thermoregulation in three dasyurid marsupials

Summary Seasonal variation in the pattern of torpor and temperature regulation was investigated in the closely related arid zone dasyurid marsupialsSminthopsis crassicaudata (17 g),S. macroura (24 g), andDasyuroides byrnei (120 g). The tendency to enter torpor was greater, torpor commenced earlier, torpor duration was longer, and body temperatures (T _b) were lower inSminthopsis spp. than inD. byrnei. The minimum mass-specific rate of oxygen consumption ( ) of torpid animals was similar among the three species despite the differences in minimumT _b. The mass-specific oxygen consumption of normothermic animals was reduced during winter when compared with the summer values in all species, but there was no seasonal variation in normothermicT _b in any species. The tendency to enter torpor was incrased during winter. TorpidSminthopsis spp. had lower values ofT _b and during winter than during summer;D. byrnei did not show seasonal changes in these variables. These results suggest that seasonal changes in the pattern of thermoregulation and torpor in small dasyurids may be more distinct than in larger species.Abbreviations RMR resting metabolic rate - BMR basal metabolic rate     

Body temperature patterns in two syntopic elephant shrew species during winter

We measured body temperature (T_b) in free-ranging individuals of two species of elephant shrews, namely western rock elephant shrews (Elephantulus rupestris) and Cape rock elephant shrews (E. edwardii), during winter in a winter-rainfall region of western South Africa. These syntopic species have similar ecologies and morphologies and thus potential for large overlaps in diet and habitat use. Unexpectedly, they displayed different T_b patterns. Western rock elephant shrews were heterothermic, with all individuals decreasing T_b below 30 °C on at least 34% of nights. The level of heterothermy expressed was similar to other species traditionally defined as daily heterotherms and was inversely related to T_a, as is commonly seen in small heterothermic endotherms. In contrast, Cape rock elephant shrews rarely allowed their T_b to decrease below 30 °C. The level of heterothermy was similar to species traditionally defined as homeotherms and there was no relationship between the level of heterothermy expressed and T_a. In both species, the minimum daily T_b was recorded almost exclusively at night, often shortly before sunrise, although in some individuals minimum T_b occasionally occurred during the day. The interspecific variation in T_b patterns among Elephantulus species recorded to date reiterates the importance of ecological determinants of heterothermy that interact with factors such as body mass and phylogeny.     

Cytoskeletal Regulation Dominates Temperature-Sensitive Proteomic Changes of Hibernation in Forebrain of 13-Lined Ground Squirrels

13-lined ground squirrels, Ictidomys tridecemlineatus, are obligate hibernators that transition annually between summer homeothermy and winter heterothermy – wherein they exploit episodic torpor bouts. Despite cerebral ischemia during torpor and rapid reperfusion during arousal, hibernator brains resist damage and the animals emerge neurologically intact each spring. We hypothesized that protein changes in the brain underlie winter neuroprotection. To identify candidate proteins, we applied a sensitive 2D gel electrophoresis method to quantify protein differences among forebrain extracts prepared from ground squirrels in two summer, four winter and fall transition states. Proteins that differed among groups were identified using LC-MS/MS. Only 84 protein spots varied significantly among the defined states of hibernation. Protein changes in the forebrain proteome fell largely into two reciprocal patterns with a strong body temperature dependence. The importance of body temperature was tested in animals from the fall; these fall animals use torpor sporadically with body temperatures mirroring ambient temperatures between 4 and 21°C as they navigate the transition between summer homeothermy and winter heterothermy. Unlike cold-torpid fall ground squirrels, warm-torpid individuals strongly resembled the homeotherms, indicating that the changes observed in torpid hibernators are defined by body temperature, not torpor per se. Metabolic enzymes were largely unchanged despite varied metabolic activity across annual and torpor-arousal cycles. Instead, the majority of the observed changes were cytoskeletal proteins and their regulators. While cytoskeletal structural proteins tended to differ seasonally, i.e., between summer homeothermy and winter heterothermy, their regulatory proteins were more strongly affected by body temperature. Changes in the abundance of various isoforms of the microtubule assembly and disassembly regulatory proteins dihydropyrimidinase-related protein and stathmin suggested mechanisms for rapid cytoskeletal reorganization on return to euthermy during torpor-arousal cycles.     

Thyroid hormone status affects expression of daily torpor and gene transcription in Djungarian hamsters (Phodopus sungorus)

Thyroid hormones (TH) play a key role in regulation of seasonal as well as acute changes in metabolism. Djungarian hamsters (Phodopus sungorus) adapt to winter by multiple changes in behaviour and physiology including spontaneous daily torpor, a state of hypometabolism and hypothermia. We investigated effects of systemic TH administration and ablation on the torpor behaviour in Djungarian hamsters adapted to short photoperiod. Hyperthyroidism was induced by giving T4 or T3 and hypothyroidism by giving methimazole (MMI) and sodium perchlorate via drinking water. T3 treatment increased water, food intake and body mass, whereas MMI had the opposite effect. Continuous recording of body temperature revealed that low T3 serum concentrations increased torpor incidence, lowered T_b and duration, whereas high T3 serum concentrations inhibited torpor expression. Gene expression of deiodinases (dio) and uncoupling proteins (ucp) were analysed by qPCR in hypothalamus, brown adipose tissue (BAT) and skeletal muscle. Expression of dio2, the enzyme generating T3 by deiodination of T4, and ucps, involved in thermoregulation, indicated a tissue specific response to treatment. Torpor per se decreased dio2 expression irrespective of treatment or tissue, suggesting low intracellular T3 concentrations during torpor. Down regulation of ucp1 and ucp3 during torpor might be a factor for the inhibition of BAT thermogenesis. Hypothalamic gene expression of neuropeptide Y, propopiomelanocortin and somatostatin, involved in feeding behaviour and energy balance, were not affected by treatment. Taken together our data indicate a strong effect of thyroid hormones on torpor, suggesting that lowered intracellular T3 concentrations in peripheral tissues promote torpor.     

Norepinephrine Controls Both Torpor Initiation and Emergence via Distinct Mechanisms in the Mouse

Some mammals, including laboratory mice, enter torpor in response to food deprivation, and leptin can attenuate these bouts of torpor. We previously showed that dopamine β-hydroxylase knockout (Dbh −/−) mice, which lack norepinephrine (NE), do not reduce circulating leptin upon fasting nor do they enter torpor. To test whether the onset of torpor in mice during a fast requires a NE-mediated reduction in circulating leptin, double mutant mice deficient in both leptin (ob/ob) and DBH (DBL MUT) were generated. Upon fasting, control and ob/ob mice entered torpor as assessed by telemetric core T_b acquisition. While fasting failed to induce torpor in Dbh −/− mice, leptin deficiency bypassed the requirement for NE, as DBL MUT mice readily entered torpor upon fasting. These data indicate that sympathetic activation of white fat and suppression of leptin is required for the onset of torpor in the mouse. Emergence from torpor was severely retarded in DBL MUT mice, revealing a novel, leptin-independent role for NE in torpor recovery. This phenotype was mimicked by administration of a β₃ adrenergic receptor antagonist to control mice during a torpor bout. Hence, NE signaling via β₃ adrenergic receptors presumably in brown fat is the first neurotransmitter-receptor system identified that is required for normal recovery from torpor.     

Comparison of hibernation, estivation and daily torpor in the edible dormouse, Glis glis

Three major forms of dormancy in mammals have been classified: hibernation in endotherms is characterised by reduced metabolic rate (MR) and body temperature (T _b) near ambient temperature (T _a) over prolonged times in the winter. Estivation is a similar form of dormancy in a dry and hot environment during summertime. Daily torpor is defined as reduced MR and T _b lower than 32 °C, limited to a duration of less than 24 h. The edible dormouse (Glis glis) is capable for all three distinct forms of dormancy. During periods of food restriction and/or low T _a, daily torpor is displayed throughout the year, alternating with hibernation and estivation in winter and summer respectively. We recorded T _b, O₂-consumption and CO₂-production in unrestrained dormice at different T _a's for periods of up to several months. Cooling rate and rate of metabolic depression during entrance into the torpid state was identical in all three forms of dormancy. The same was true for thermal conductance, maximum heat production, duration of arousal and cost of an arousal. The only difference between hibernation and daily torpor was found in the bout duration. A daily torpor bout lasted 3–21 h, a hibernation bout 39–768 h. As a consequence of prolonged duration, MR, T _b and also the T _b − T _a gradient decreased to lower values during hibernation bouts when compared to daily torpor bouts. Our findings suggest that all three forms of dormancy are based on the same physiological mechanism of thermal and metabolic regulation. Accepted: 27 June 2000     

The “minimal boundary curve for endothermy” as a predictor of heterothermy in mammals and birds: a review

According to the concept of the “minimal boundary curve for endothermy”, mammals and birds with a basal metabolic rate (BMR) that falls below the curve are obligate heterotherms and must enter torpor. We examined the reliability of the boundary curve (on a double log plot transformed to a line) for predicting torpor as a function of body mass and BMR for birds and several groups of mammals. The boundary line correctly predicted heterothermy in 87.5% of marsupials (n = 64), 94% of bats (n = 85) and 82.3% of rodents (n = 157). Our analysis shows that the boundary line is not a reliable predictor for use of torpor. A discriminate analysis using body mass and BMR had a similar predictive power as the boundary line. However, there are sufficient exceptions to both methods of analysis to suggest that the relationship between body mass, BMR and heterothermy is not a causal one. Some homeothermic birds (e.g. silvereyes) and rodents (e.g. hopping mice) fall below the boundary line, and there are many examples of heterothermic species that fall above the boundary line. For marsupials and bats, but not for rodents, there was a highly significant phylogenetic pattern for heterothermy, suggesting that taxonomic affiliation is the biggest determinant of heterothermy for these mammalian groups. For rodents, heterothermic species had lower BMRs than homeothermic species. Low BMR and use of torpor both contribute to reducing energy expenditure and both physiological traits appear to be a response to the same selective pressure of fluctuating food supply, increasing fitness in endothermic species that are constrained by limited energy availability. Both the minimal boundary line and discriminate analysis were of little value for predicting the use of daily torpor or hibernation in heterotherms, presumably as both daily torpor and hibernation are precisely controlled processes, not an inability to thermoregulate.     

Stage of pregnancy dictates heterothermy in temperate forest-dwelling bats

Bats face high energetic requirements, as powered flight is costly and they have a disadvantageous surface-to-volume-ratio. To deal with those requirements energy saving mechanisms, such as heterothermy (torpor), have evolved. Torpor during pregnancy, however, reduces rates of foetal development and consequently prolongs pregnancy. Therefore, heterothermy has a great effect on reproduction, as an unhindered parturition can only be assured by high body temperatures. Regardless of these adverse affects of torpor the energetic requirements of bats during reproduction urge for energy savings and bats are known to enter torpor during pregnancy. The species in the current study differ in their torpor patterns and thus their heterothermic strategy. However, we hypothesized, that species-specific heterothermic behaviour should be revoked at the end of pregnancy. We analyzed skin temperatures of Myotis bechsteinii, Myotis nattereri and Plecotus auritus during pregnancy and found no differences in torpor depth between species during the last phase of pregnancy. Furthermore, we could show that individuals entered torpor frequently during pregnancy and only minimized torpor during the last stage of pregnancy. This suggests that close to the end of pregnancy, heterothermy is restricted but not species-specific and the required energy is allocated otherwise.     

Thermoregulatory responses in seasonally acclimatized captive Southern White-faced Scops-owls

Seasonal thermoregulatory responses that are associated with cold tolerance have been reported for many species that inhabit regions where winters are severe (e.g. Holarctic), but relatively few studies have focused on species from regions where the climate is more unpredictable (e.g. Southern Africa). In this study, metabolic rate (VO₂) and body temperature (T_b) was measured during summer and winter in captive Southern White-faced Scops-owl (Ptilopsis granti), to test for thermoregulatory responses representing energy conservation in winter. During winter the Southern White-faced Scops-owls increased resting metabolic rate (RMR) by 45% to regulate a set point T_b—a result similar to what had been shown in small passerines from the Holarctic region. Increased RMR and increased conductance at cold T_a's are suggestive of improved cold tolerance. Basal metabolic rate (BMR) was 0.60 mL O₂ g⁻¹ h⁻¹ and showed no seasonal flexibility. Thus, contrary to expectation, the Southern White-faced Scops-owls showed seasonal thermoregulatory responses that are unlikely to represent energy conservation which was expected for a medium-sized bird inhabiting unpredictable climates in Southern Africa.     

Seasonal effects on metabolism and thermoregulation abilities of the Red-winged Starling (Onychognathus morio)

Basal metabolic rate (BMR) of birds is beginning to be viewed as a highly flexible physiological trait influenced by environmental fluctuations, and in particular changes in ambient temperatures (T_a). Southern Africa is characterized by an unpredictable environment with daily and seasonal variation. This study sought to evaluate the effects of seasonal changes in T_a on mass-specific resting metabolic rate (RMR), BMR and body temperature (T_b) of Red-winged Starlings (Onychognathus morio). They have a broad distribution, from Ethiopia to the Cape in South Africa and are medium-sized frugivorous birds. Metabolic rate (VO₂) and T_b were measured in wild caught Red-winged Starlings after a period of summer and winter acclimatization in outdoor aviaries. RMR and BMR were significantly higher in winter than summer. Body mass of Starlings was significantly higher in winter compared with summer. The increased RMR and BMR in winter indicate improved ability to cope with cold and maintenance of a high T_b. These results show that the metabolism of Red-winged Starlings are not constant, but exhibit a pronounced seasonal phenotypic flexibility with maintenance of a high T_b.     

Oral bezafibrate induces daily torpor and FGF21 in mice in a PPAR alpha dependent manner

Fibroblast growth factor 21 (FGF21) is a hormone released from the liver that mediates many of the physiological responses of fasting, such as lipolysis and ketogenesis. FGF21 is induced by the nuclear receptor PPARα when bound to its endogenous agonist, free fatty acid, or to the synthetic agonist, bezafibrate. To determine whether PPARα agonists mediate the metabolic suppression and accompanying fall in body temperature (T_b) in a bout of torpor that occurs in mice in response to fasting, C57Bl/6J mice (wildtype) and PPARα −/− mice were implanted with temperature telemeters and fed either a control (CON) diet or one containing a PPARα agonist, bezafibrate (BEZA), for 2 weeks, followed by a fast. Wildtype mice on the BEZA diet had a striking phenotype: most entered spontaneous torpor bouts without caloric restriction towards the end of the 2 weeks. This is the first demonstration that an additive to food could induce spontaneous bouts of daily torpor. However, PPARα −/− did not express this phenotype. Moreover, wildtype mice on the BEZA diet had twice the length of torpor bouts in response to a fast as did wildtype mice on the CON diet. PPARα −/− mice did enter bouts of fasting-induced torpor, but these were unaffected by the BEZA diet. The BEZA diet induced the level of FGF21 in the blood to fasting levels only in wildtype mice. Collectively, these findings suggest that a BEZA diet mimics the fasted state in both induction of FGF21 and in thermoregulation and does so in a pathway dependent on PPARα.