Quantifying torpor in small mammals non-invasively using infrared thermocouples

Measurements of torpor use are pivotal for many research areas concerning the thermal biology of endotherms. Here, I used infrared thermocouples to non-invasively examine torpor patterns in the small marsupial fat-tailed dunnart (Sminthopsis crassicaudata). Sensors were installed inside the nesting chambers to continuously monitor fur temperature in undisturbed animals. Firstly, to verify the measurements, fur temperature was monitored simultaneously with body temperature using internal radio transmitters (n=6). Secondly, I conducted a food restriction study to demonstrate the reliability of the method within a physiological experiment (n=8). Based on the correspondence of simultaneously measured fur and body temperature during torpor bouts, I was able to confirm that infrared thermocouples provide reliable temporal information on torpor patterns. Furthermore, torpor use was successfully monitored over a 20-day food restriction study. The method can easily be adapted to suit other small mammal or bird species and presents a useful, inexpensive approach for examining torpor patterns remotely and non-invasively in the laboratory.     

The use of small subcutaneous transponders for quantifying thermal biology and torpor in small mammals

Remote measurements of body temperature (T_b) in animals require implantation of relatively large temperature-sensitive radio-transmitters or data loggers, whereas rectal temperature (T_rec) measurements require handling and therefore may bias the results. We investigated whether ∼0.1 g temperature-sensitive subcutaneously implanted transponders can be reliably used to quantify thermal biology and torpor use in small mammals. We examined (i) the precision of transponder readings as a function of temperature and (ii) whether subcutaneous transponders can be used to remotely record subcutaneous temperature (T_sub). Five adult male dunnarts (Sminthopsis macroura, body mass 24 g) were implanted with subcutaneous transponders to determine T_sub as a function of time and ambient temperature (T_a), and in comparison to thermocouple readings of T_rec. Transponder temperature was highly correlated with water bath temperature (r²=0.96–0.99) over a range of approximately 10.0–40.0 °C. Transponders provided reliable data (±0.6 °C) over the T_sub of 21.4–36.9 °C and could be read from a distance of up to 5 cm. Below 21.4 °C, accuracy was reduced to ±2.8 °C, but individual transponder accuracy varied. Consequently, small subcutaneous transponders are useful to remotely quantify thermal physiology and torpor patterns without having to disturb the animal and disrupt torpor. Even at T_sub<21.4 °C where the accuracy of the temperature readings was reduced, transponders do provide reliable data on whether and when torpor is used.     

Daily torpor and hibernation in birds and mammals

Many birds and mammals drastically reduce their energy expenditure during times of cold exposure, food shortage, or drought, by temporarily abandoning euthermia, i.e. the maintenance of high body temperatures. Traditionally, two different types of heterothermy, i.e. hypometabolic states associated with low body temperature (torpor), have been distinguished: daily torpor, which lasts less than 24 h and is accompanied by continued foraging, versus hibernation, with torpor bouts lasting consecutive days to several weeks in animals that usually do not forage but rely on energy stores, either food caches or body energy reserves. This classification of torpor types has been challenged, suggesting that these phenotypes may merely represent extremes in a continuum of traits. Here, we investigate whether variables of torpor in 214 species (43 birds and 171 mammals) form a continuum or a bimodal distribution. We use Gaussian‐mixture cluster analysis as well as phylogenetically informed regressions to quantitatively assess the distinction between hibernation and daily torpor and to evaluate the impact of body mass and geographical distribution of species on torpor traits. Cluster analysis clearly confirmed the classical distinction between daily torpor and hibernation. Overall, heterothermic endotherms tend to be small; hibernators are significantly heavier than daily heterotherms and also are distributed at higher average latitudes (～35°) than daily heterotherms (～25°). Variables of torpor for an average 30 g heterotherm differed significantly between daily heterotherms and hibernators. Average maximum torpor bout duration was >30‐fold longer, and mean torpor bout duration >25‐fold longer in hibernators. Mean minimum body temperature differed by ～13°C, and the mean minimum torpor metabolic rate was ～35% of the basal metabolic rate (BMR) in daily heterotherms but only 6% of BMR in hibernators. Consequently, our analysis strongly supports the view that hibernators and daily heterotherms are functionally distinct groups that probably have been subject to disruptive selection. Arguably, the primary physiological difference between daily torpor and hibernation, which leads to a variety of derived further distinct characteristics, is the temporal control of entry into and arousal from torpor, which is governed by the circadian clock in daily heterotherms, but apparently not in hibernators.     

Relationships between body temperature,thermal conductance,Q 10 and energy metabolism during daily torpor and hibernation in rodents

Summary In the present paper we examine the ability of rodents to maintain body temperature (T _B ) following the marked reductions in metabolic heat production associated with torpor. Previously published values for metabolic rate (M),T _B and ambient temperature (T _A ) were used to calculate thermal conductances (C') during normothermy and torpor in rodents capable of daily torpor (11 species) and hibernation (18 species). Values ofC' for torpid animals are uniformly lower thanC' in normothermic animals. In addition,C' of normothermic and torpid rodents decreases with increasing body mass (BM). However, the slope of the relationship betweenC' and BM is almost 4-fold greater for normothermic than for torpid animals. Thus, the ability of torpid rodents to conserve body heat by reducingC' decreases with increasing mass. Rodents that use daily torpor tend to be small and they tend to maintainT _B well aboveT _A during torpor. Hibernators tend to be larger and regulateT _B relatively close toT _A . Thus, the reductions inC' appear to be closely correlated with the level ofT _B regulation during torpor. We suggest that the changes inC' represent a suite of physiological adaptations that have played a central role in the evolution of torpor, enabling rodents to regulateT _B aboveT _B during periods of very low heat production. Based on the approach used here we address the controversy of whether reductions inM during torpor are due entirely to temperature effects or whether metabolic inhibition in addition to temperature effects may be important. We suggest that the controversy has been confused by usingQ ₁₀ to evaluate the relationship ofM andT _B in endotherms. What is perceived as metabolic inhibition (i.e.,Q ₁₀>3) is confounded by changes in the relationship ofM andT _B due to reductions inC' and reductions in the difference betweenT _B andT _A . Unfortunately, changes inM andT _B cannot be used to quantify changes in metabolic state in endotherms. Thus, neitherQ ₁₀ nor the approach used here can be used to make valid statements about the metabolic regulatory processes associated with torpor. Other methods, perhaps at the cell or tissue level, are needed.Abbreviations T _B body temperature - T _A ambient temperature - C' thermal conductance - C _n normothermicC whenT _A is above a lower critical temperature - C _t torporC when animals are in daily torpor or hibernation - M metabolic rate - BM body mass - WVPD water vapor pressure deficit     

Ontogeny and phylogeny of endothermy and torpor in mammals and birds

Endothermic thermoregulation in small, altricial mammals and birds develops at about one third to half of adult size. The small size and consequently high heat loss in these young should result in more pronounced energetic challenges than in adults. Thus, employing torpor (a controlled reduction of metabolic rate and body temperature) during development would allow them to save energy. Although torpor during development in endotherms is likely to occur in many species, it has been documented in only a few. In small, altricial birds (4 orders) and marsupials (1 order), which are poikilothermic at hatching/birth, the development of competent endothermic thermoregulation during cold exposure appears to be concurrent with the capability to display torpor (i.e. poikilothermy is followed by heterothermy), supporting the view that torpor is phylogenetically old and likely plesiomorphic. In contrast, in small, altricial placental mammals (2 orders), poikilothermy at birth is followed first by a homeothermic phase after endothermic thermoregulation is established; the ability to employ torpor develops later (i.e. poikilothermy-homeothermy-heterothermy). This suggests that in placentals torpor is a derived trait that evolved secondarily after a homeothermic phase in certain taxa perhaps as a response to energetic challenges. As mammals and birds arose from different reptilian lineages, endothermy likely evolved separately in the two classes, and given that the developmental sequence of torpor differs between marsupials and placentals, torpor seems to have evolved at least thrice.     

Central regulation of temperature in hibernation and normothermia

Normothermic hibernators respond proportionally to both peripheral and brain temperature changes like other mammals. Their quantitative responsiveness to peripheral and brain temperature inputs are consistent with body-size relationships seen in other vertebrates. The basic temperature regulatory mechanisms seen in seasonal hibernators are not altered with season although certain response parameters, such as vasomotion, are not obvious in prehibernating marmots.     

Winter body temperature patterns in free-ranging Cape ground squirrel, Xerus inauris: no evidence for torpor

The body temperature (T _b) of Cape ground squirrels (Xerus inauris, Sciuridae) living in their natural environment during winter has not yet been investigated. In this study we measured abdominal T _b of eight free-ranging Cape ground squirrels over 27 consecutive days during the austral winter. Mean daily T _b was relatively stable at 37.0 ± 0.2°C (range 33.4 to 40.2°C) despite a marked variation in globe temperature (T _g) (range −7 to 37°C). Lactating females (n = 2) consistently had a significantly higher mean T _b (0.7°C) than non-lactating females (n = 3) and males. There was a pronounced nychthemeral rhythm with a mean active phase T _b of 38.1 ± 0.1°C and a mean inactive phase T _b of 36.3 ± 0.3°C for non-lactating individuals. Mean daily amplitude of T _b rhythm was 3.8 ± 0.2°C. T _b during the active phase closely followed T _g and mean active phase T _b was significantly correlated with mean active phase T _g (r ² = 0.3–0.9; P < 0.01). There was no evidence for daily torpor or pronounced hypothermia during the inactive phase, and mean minimum inactive phase T _b was 35.7 ± 0.3°C for non-lactating individuals. Several alternatives (including nocturnal huddling, an aseasonal breeding pattern and abundant winter food resources) as to why Cape ground squirrels do not employ nocturnal hypothermia are discussed.     

An optimum body size for mammals? Comparative evidence from bats

1. The distribution of body sizes among mammalian species has been modelled by Brown, Marquet & Taper (1993), who suggest that reproductive power (the rate at which energy from the environment is channelled into offspring production) is maximized at a size of 100 g, and the observed size distribution among species reflects the way reproductive power depends on size. The model makes a testable prediction about life-history allometries: namely, that components of reproductive power should not scale linearly with body size but should change sign at the optimum size.
2. A large set of life-history data from a single clade of small mammals, the bats (Order: Chiroptera), was analysed to test this key prediction. The analyses in this study offer no support for the idea that allometries of reproductive power change sign in bats, either at 100 g or at any other size. Furthermore the life-history allometries of bats, which are mostly below the 100 g optimum, were broadly the same as in mammalian taxa larger than the optimum size.
3. These findings together contradict a key prediction of Brown et al. 's (1993) model to explain the skewed body size distribution across mammalian species.     

Interactions between the parasitic protozoa of small mammals

In the wild, small mammals are frequently infected with more than one parasite. Laboratory studies have revealed complex interactions between parasites and also between parasitic protozoa and viruses or bacteria. In general, infection with many parasites is accompanied by a period of immunodepression during which superimposed infections are favoured, giving rise to more intense and prolonged secondary infections while the original infection is unaffected. On the other hand, organisms that activate macrophages may protect die host against a subsequent infection. These kinds of interactions have been investigated in the laboratory using Trypanosoma musculi, T. lewisi, Giardia muris, Spironucleus muris, Babesia microti and Heligmosomoides polygyrus , all of which occur in British small mammals, suggesting that such interactions occur in the field, are worth investigating and should be considered in epidemiological studies.     

The macroevolutionary relationship between diet and body mass across mammals

Body mass and diet are two fundamental ecological parameters that influence many other aspects of an animal's biology. Thus, the potential physiological and ecological processes linking size and diet have been the subject of extensive research, although the broad macroevolutionary relationship between the two traits remains largely unexplored phylogenetically. Using generalized Ornstein–Uhlenbeck models and data on over 1350 species of mammal, we reveal that evolutionary changes in body mass are consistently associated with dietary changes across mammals. Best‐fitting models find that herbivores are substantially heavier than other dietary groups and that omnivores are frequently intermediate in mass between herbivores and carnivores. Interestingly, although flying and swimming both place very different physical constraints on mass, bats still follow the general mammalian pattern but marine mammals do not. Such differences may be explained by reduced gravitational constraints on size in water along with ecological differences in food availability between aquatic and terrestrial realms, allowing marine carnivores to become the largest mammals on earth. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 173–184.