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.     

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     

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.     

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.     

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.     

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.     

Cool running: locomotor performance at low body temperature in mammals

Mammalian torpor saves enormous amounts of energy, but a widely assumed cost of torpor is immobility and therefore vulnerability to predators. Contrary to this assumption, some small marsupial mammals in the wild move while torpid at low body temperatures to basking sites, thereby minimizing energy expenditure during arousal. Hence, we quantified how mammalian locomotor performance is affected by body temperature. The three small marsupial species tested, known to use torpor and basking in the wild, could move while torpid at body temperatures as low as 14.8-17.9°C. Speed was a sigmoid function of body temperature, but body temperature effects on running speed were greater than those in an ectothermic lizard used for comparison. We provide the first quantitative data of movement at low body temperature in mammals, which have survival implications for wild heterothermic mammals, as directional movement at low body temperature permits both basking and predator avoidance.     

A simplified telemetry system for monitoring body temperature in small animals

An inexpensive but reliable telemetry system for long-term, sequential monitoring of body temperature in up to 20 laboratory animals is described. The system consists of frequency-modulated (FM) temperature transmitters, remote-controlled power switches to extend battery life, a multi-channel telemetry receiver, and a frequency counter interfaced with a personal computer to record data. Analysis of body temperature data obtained from four New Zealand White rabbits confirms the reliability and value of this system.