Article

Fasting-induced daily torpor in desert hamsters (Phodopus roborovskii)

Authors:
  • Zunyi Normal University
  • Shandong University (Qingdao Campus)
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Abstract

Daily torpor is frequently expressed in small rodents when facing energetically unfavorable ambient conditions. Desert hamsters (Phodopus roborovskii, ~ 20 g) appear to be an exception as they have been described as homeothermic. However, we hypothesized that they can use torpor because we observed reversible decreases of body temperature (Tb) in fasted hamsters. To test this hypothesis we (i) randomly exposed fasted summer-acclimated hamsters to ambient temperatures (Tas) ranging from 5 to 30 °C or (ii) supplied them with different rations of food at Ta 23 °C. All desert hamsters showed heterothermy with the lowest mean Tb of 31.4 ± 1.9 °C (minimum, 29.0 °C) and 31.8 ± 2.0 °C (minimum, 29.0 °C) when fasted at Ta of 23 °C and 19 °C, respectively. Below Ta 19 °C, the lowest Tb and metabolic rate increased and the proportion of hamsters using heterothermy declined. At Ta 5 °C, nearly all hamsters remained normothermic by increasing heat production, suggesting that the heterothermy only occurs in moderately cold conditions, perhaps to avoid freezing at extremely low Tas. During heterothermy, Tbs below 31 °C with metabolic rates below 25% of those during normothermia were detected in four individuals at Ta of 19 °C and 23 °C. Consequently, by definition, our observations confirm that fasted desert hamsters are capable of shallow daily torpor. The negative correlation between the lowest Tbs and amount of food supply shows that heterothermy was mainly triggered by food shortage. Our data indicate that summer-acclimated desert hamsters can express fasting-induced shallow daily torpor, which may be of significance for energy conservation and survival in the wild.

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... It produces up to four litters of up to ten young per year, can breed within 2 months of birth, lives for only 1 or 2 years in the wild, and is clearly r-selected (Kolynchuk, 2015). Desert hamsters are distributed over the harsh deserts of continental Asia and, as adults, use daily torpor to aid survival in their environment (Chi et al., 2016). As they reproduce well into autumn, their young are potentially exposed to adverse environmental conditions and energy shortages in late autumn/early winter, and may require the use of energy savings mechanisms such as torpor to survive over winter into adulthood. ...
... In the morning when the MR of juvenile hamsters indicated that they were in a state of torpor (MR well below 75% of RMR measured in the same individual at the same T a ; Hudson and Scott, 1979;Chi et al., 2016) animals were removed from the chamber and their thermograph was taken and/or their T s was measured immediately as described above. A T s of ≤29.6 • C was considered as an alternative definition of torpor because the mean resting T s before measurements was 34.6 ± 0.6 • C and a fall of T b by 5 • C or more from the resting T b is often used for defining torpor (Ruf and Geiser, 2015). ...
... Animals were handled with gloves to ensure there was no heat transfer from the hand and then returned to the respirometry chamber within 1 min to determine whether they could rewarm from torpor; these measurements were repeated during the arousal process. Torpor duration was defined as the time with MR below 75% of RMR at the same T a (Chi et al., 2016). Some young hamsters were placed individually in cages on sawdust into the incubator at T a 22.0 ± 0.5 • C overnight and it was determined via T s and thermograph measurements whether they could enter and arouse from torpor. ...
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Article
Most mammals and birds are altricial, small and naked at birth/hatching. They attain endothermic thermoregulation at a fraction of their adult size at a vulnerable stage with high heat loss when many could profit from using torpor for energy conservation. Nevertheless, detailed data on the interrelations between torpor expression and development of endothermic thermoregulation are currently restricted to <0.1% of extant endotherms. We investigated at what age and body mass (BM) desert hamsters (Phodopus roborovskii), wild-caught in Inner Mongolia and born in autumn/early winter when environmental temperatures in the wild begin to decrease, are able to defend their body temperature (Tb) at an ambient temperature (Ta) of ~21°C and how soon thereafter they could express torpor. Measurements of surface temperatures via infrared thermometer and thermal camera show that although neonate hamsters (BM 0.9±0.1 g) cooled rapidly to near Ta, already on day 15 (BM 5.5±0.2 g) they could defend a high and constant Tb. As soon as day 16 (BM 5.8±0.2 g), when their maximum activity metabolism (measured as oxygen consumption) approached maxima measured in vertebrates, animals were able to enter torpor for several hours with a reduction of metabolism by >90%, followed by endothermic arousal. Over the next weeks, torpor depth and duration decreased together with a reduction in resting metabolic rate at Ta 30-32°C. Our data show that development of endothermy and torpor expression in this altricial hamster is extremely fast. The results suggest that precocious torpor by juvenile hamsters in autumn and winter is an important survival tool in their vast and harsh Asian desert habitats, but likely also for many other small mammals and birds worldwide.
... Expression of such torpor behaviors seem to be mainly driven by endogenous annual (hibernation) or circadian (daily torpor) rhythms that are mediated by environmental cues such as changes of photoperiod and ambient temperature (T a ) (Lynch et al., 1978;Heldmaier and Steinlechner, 1981;Steinlechner et al., 1986;Geiser and Ruf, 1995;McNab, 2002;Ruf and Geiser, 2015). On another hand, some heterotherms can also display daily torpor as a response to chronic or acute food shortage, which indicates that the initiation of torpor might be directly related to the metabolic fuel availability (Hudson and Scott, 1979;Nestler, 1991;Ruby and Zucker, 1992;Ehrhardt et al., 2005;Diedrich et al., 2015;Chi et al., 2016). ...
... Desert hamsters (Phodopus roborovskii) are one of the smallest dwarf hamsters with a body mass of about 20 g which makes them highly susceptible to food shortage (Ross, 1994;Bao et al., 2002;Zhan and Wang, 2003;Chi and Wang, 2011;Zhang et al., 2015;Chi et al., 2016). Our laboratory work has established that food deprivation did induce shallow torpor within 24 h in summer-acclimated desert hamsters at moderate cold T a of 23°C (Chi et al., 2016). ...
... Desert hamsters (Phodopus roborovskii) are one of the smallest dwarf hamsters with a body mass of about 20 g which makes them highly susceptible to food shortage (Ross, 1994;Bao et al., 2002;Zhan and Wang, 2003;Chi and Wang, 2011;Zhang et al., 2015;Chi et al., 2016). Our laboratory work has established that food deprivation did induce shallow torpor within 24 h in summer-acclimated desert hamsters at moderate cold T a of 23°C (Chi et al., 2016). To investigate the role of metabolic fuel deprivation during the torpor initiation, in the present study summer-acclimated male desert hamsters were injected with various doses of 2DG or MA during their resting phase at T a of 23°C. ...
Article
The initiation of torpor is supposed to be related to the availability of metabolic fuels. Studies on metabolic fuel inhibition of glucose by using 2-deoxy-D-glucose (2DG) or fatty acid by mercaptoacetate (MA) in heterothermic mammals produced mixed outcomes. To examine the roles of availability of glucose and fatty acid in the initiation of torpor in desert hamsters (Phodopus roborovskii), we intraperitoneally administrated 2DG and MA to summer-acclimated male hamsters while body temperature (Tb), metabolic rate (MR) and respiratory quotient (RQ) were simultaneously recorded to monitor their thermoregulatory response. 2DG induced a reversible reduction of Tb in desert hamsters both at ambient temperature (Ta) of 23oC and 5oC. At Ta of 23oC, Tb, MR and RQ decreased in a dose-dependent manner with a large Tb-Ta differential (> 6.5oC) and a lowest Tb of 28.0oC which were comparable to those in fasted hamsters. At Ta of 5oC, 2DG-treated hamsters also decreased Tb to the same level as at Ta 23oC, but MR was significantly higher than that at Ta of 23oC at each dose, suggesting doses of 2DG directly affected the hypothalamic Tb set-point. Different from fasted hamsters which maintain normothermic at Ta of 5oC, 2DG-treated hamsters showed a substantial reduction of Tb at Ta 5oC, indicating an overwhelming effect on the thermoregulatory system regardless of Ta. Furthermore, the rapid decrease of Tb and outstretched body posture in 2DG-treated hamsters suggest that the effects of 2DG were not simply mimicking the torpor pathways but that other mechanisms are involved. Interestingly, MA failed to induce a torpor-like state in male desert hamsters. Our results suggest that availability of glucose rather than fatty acid plays an important role for initiation of torpor in desert hamsters.
... Especially in small homeotherms that neither migrate nor become torpid, these structural and physiological changes in favor of an increased nutrient resorption serve as an essential mechanism to compensate for the decreased energy availability during times of increased energy expenditure (Bozinovic and Iturri, 1991). Many of these species also use daily torpor in response to energetic challenges (Eto et al., 2014;Tannenbaum and Pivorun, 1988;Chi et al., 2016). However, although winter acclimatization always comprises multiple, complex and interacting adjustments (Heldmaier and Lynch, 1986), it has never been reported whether and how mechanisms to decrease energy expenditure (such as torpor) work together with mechanisms to increase energy yield (nutrient resorption). ...
... Thus, a comparison of intestinal acclimation between hibernators and daily heterotherms would require a more comprehensive data set of internal and external factors, which emphasizes that daily torpor is more than just a short form of hibernation (Ruf and Geiser, 2015). The complexity and diversity of seasonal acclimatization strategies becomes apparent once again when regarding species such as Phodopus roborovskii, Apodemus speciosus and Peromyscus leucopus, which are capable of torpor expression (Eto et al., 2014;Tannenbaum and Pivorun, 1988;Chi et al., 2016), but increase their intestinal tissue during winter acclimatization (Chi and Wang, 2011;Derting and Noakes, 1995;Eto et al., 2016;Zhu et al., 2011;Green and Millar, 1987). ...
Article
Small mammals exhibit seasonal changes in intestinal morphology and function via increased intestine size and resorptive surface and/or nutrient transport capacity to increase energy yield from food during winter. This study investigated whether seasonal or acute acclimation to anticipated or actual energetic challenges in Djungarian hamsters also resulted in higher nutrient resorption capacities due to changes in small intestine histology and physiology. The hamsters show numerous seasonal energy saving adjustments in response to short photoperiod. As spontaneous daily torpor represents one of these adjustments related to food quality and quantity, it was hypothesized that the hamsters’ variable torpor expression patterns are influenced by their individual nutrient uptake capacity. Hamsters under short photoperiod showed longer small intestines and higher mucosal electrogenic transport capacities for glucose relative to body mass. Similar observations were made in hamsters under long photoperiod and food restriction. However, this acute energetic challenge caused a stronger increase of glucose transport capacity. Apart from that, neither fasting-induced torpor in food-restricted hamsters nor spontaneous daily torpor in short photoperiod-exposed hamsters clearly correlated with mucosal glucose transport capacity. Both seasonally anticipated and acute energetic challenges caused adjustments in the hamsters’ small intestine. Short photoperiod appeared to induce an integration of these and other acclimation processes in relation to body mass to achieve a long-term adjustment of energy balance. Food restriction seemed to result in a more flexible, short-term strategy of maximizing energy uptake possibly via mucosal glucose transport and reducing energy consumption via torpor expression as emergency response.
... Similarly, when held under short photoperiod P. sungorus expressed spontaneous torpor, but not under long photoperiod (Geiser et al., 2013). However, torpor could be induced in a summer-acclimated congener, the desert hamster, P. roborovskii (Chi et al., 2016). Although it has been suggested that induced torpor and spontaneous torpor in P. sungorus differ functionally (Diedrich et al., 2012), some Phodopus species obviously have the ability to enter and arouse from torpor even when summer acclimated. ...
... Andean Hillstar, Oreotrochilus estella, spring and autumn unknown (Carpenter, 1974) Rufous hummingbird, Selasphorus rufus, migratory, winter unknown (Hiebert, 1993) Sunbird, Nectarina famosa, summer (Downs and Brown, 2002) Black-capped chickadee, Poecile atricapilla, spring and autumn unknown (Sharbaugh, 2001) Fat-tailed dunnart, Sminthopsis crassicaudata (Geiser and Baudinette, 1987;Warnecke et al., 2008) Stripe-faced dunnart, Sminthopsis macroura (Geiser and Baudinette, 1987;Körtner and Geiser, 2009) Kowari, Dasyuroides byrnei (Geiser and Baudinette, 1987) Blossom-bat, Syconycteris australis (Geiser et al., 1996;Coburn and Geiser, 1998) Elephant shrew, Elephantulus myurus (Mzilikazi and Lovegrove, 2004) White-footed mouse, Peromyscus leucopus (Lynch et al., 1978) Deer mouse, Peromyscus maniculatus (Tannenbaum and Pivorun, 1989) Desert hamster, Phodopus roborovskii (Chi et al., 2016;Geiser et al., 2019) Spiny mouse, Acomys russatus (Levy et al., 2011) Autumn to spring Tawny frogmouth, Podargus strigoides Owlet-nightjar, Aegotheles cristatus Whip-poorwill, Caprimulgus vociferous, migratory, winter unknown (Lane et al., 2004) Noisy miner, Manorina melanocephala (Geiser, 2019) Brown antechinus, Antechinus stuartii (Geiser, 1988;Hume et al., 2020) Yellow-footed antechinus, Antechinus flavipes (Geiser, 1988;Parker et al., 2019) Sugar glider, Petaurus breviceps (Körtner and Geiser, 2000a;Nowack et al., 2015) Djungarian hamster, Phodopus sungorus (Heldmaier and Steinlechner, 1981) other aspect of seasonal torpor use, the control of its expression differs among species and revealing the responsible cues will require further work. ...
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Article
Daily torpor and hibernation (multiday torpor) are the most efficient means for energy conservation in endothermic birds and mammals and are used by many small species to deal with a number of challenges. These include seasonal adverse environmental conditions and low food/water availability, periods of high energetic demands, but also reduced foraging options because of high predation pressure. Because such challenges differ among regions, habitats and food consumed by animals, the seasonal expression of torpor also varies, but the seasonality of torpor is often not as clear-cut as is commonly assumed and differs between hibernators and daily heterotherms expressing daily torpor exclusively. Hibernation is found in mammals from all three subclasses from the arctic to the tropics, but is known for only one bird. Several hibernators can hibernate for an entire year or express torpor throughout the year (8% of species) and more hibernate from late summer to spring (14%). The most typical hibernation season is the cold season from fall to spring (48%), whereas hibernation is rarely restricted to winter (6%). In hibernators, torpor expression changes significantly with season, with strong seasonality mainly found in the sciurid and cricetid rodents, but seasonality is less pronounced in the marsupials, bats and dormice. Daily torpor is diverse in both mammals and birds, typically is not as seasonal as hibernation and torpor expression does not change significantly with season. Torpor in spring/summer has several selective advantages including: energy and water conservation, facilitation of reproduction or growth during development with limited resources, or minimisation of foraging and thus exposure to predators. When torpor is expressed in spring/summer it is usually not as deep and long as in winter, because of higher ambient temperatures, but also due to seasonal functional plasticity. Unlike many other species, subtropical nectarivorous blossom-bats and desert spiny mice use more frequent and pronounced torpor in summer than in winter, which is related to seasonal availability of nectar or water. Thus, seasonal use of torpor is complex and differs among species and habitats.
... Some mammalian species are able to decrease metabolic rate and T b , and enter torpor (such as Phodopus sungorus and P. rovorovskii) or hibernation (such as Spermophilus dauricus) to save energy and survive in winter (McNab, 2002;Chi et al., 2016;Ren et al., 2022). However, the non-hibernating small mammals (e.g., Lasiopodomys brandtii and Meriones unguiculatus) must increase metabolic rate including obligatory thermogenesis (basal/resting metabolic rate, BMR/RMR, with a difference of fasting for the former and no fasting for the latter before measurement) in the liver and other metabolic organs, and regulatory thermogenesis (mainly nonshivering thermogenesis, NST) in brown adipose tissue (BAT) and skeletal muscle to maintain thermal homeostasis in winter or during cold acclimation (Cannon and Nedergaard, 2004;Zhang and Wang, 2006;Nowack et al., 2017;Bal et al., 2018). ...
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The endotherms, particularly the small mammals living in the polar region and temperate zone, are faced with extreme challenges for maintaining stable core body temperatures in harsh cold winter. The non-hibernating small mammals increase metabolic rate including obligatory thermogenesis (basal/resting metabolic rate, BMR/RMR) and regulatory thermogenesis (mainly nonshivering thermogenesis, NST, in brown adipose tissue and skeletal muscle) to maintain thermal homeostasis in cold conditions. A substantial amount of evidence indicates that the symbiotic gut microbiota are sensitive to air temperature, and play an important function in cold-induced thermoregulation, via bacterial metabolites and byproducts such as short-chain fatty acids and secondary bile acids. Cold signal is sensed by specific thermosensitive transient receptor potential channels (thermo-TRPs), and then norepinephrine (NE) is released from sympathetic nervous system (SNS) and thyroid hormones also increase to induce NST. Meanwhile, these neurotransmitters and hormones can regulate the diversity and compositions of the gut microbiota. Therefore, cold-induced NST is controlled by both Thermo-TRPs—SNS—gut microbiota axis and thyroid—gut microbiota axis. Besides physiological thermoregulation, small mammals also rely on behavioral regulation, such as huddling and coprophagy, to maintain energy and thermal homeostasis, and the gut microbial community is involved in these processes. The present review summarized the recent progress in the gut microbiota and host physiological and behavioral thermoregulation in small mammals for better understanding the evolution and adaption of holobionts (host and symbiotic microorganism). The coevolution of host-microorganism symbionts promotes individual survival, population maintenance, and species coexistence in the ecosystems with complicated, variable environments.
... The existence of more than two strategies or even a continuum from homeothermy through to poikilothermy has been suggested van Breukelen and Martin, 2015). Some endothermic species are only able to increase variation of T b minimally (Chaplin et al., 1984;Yoda et al., 2000;Nieminen et al., 2013), whereas the classical heterotherms include some that can enter shallower or deeper torpor during comparable fooddeprivation experiments (Walton and Andrews, 1981;Lovegrove et al., 2001;Nespolo et al., 2010;Chi et al., 2016;Boratynśki et al., 2018). Adaptive heterothermy is thus variable, but is probably a universal phenomenon among endotherms, including those considered classical homeotherms, or animals in general (Angilletta et al., 2006(Angilletta et al., , 2010. ...
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Article
Theoretical modelling predicts that the thermoregulatory strategies of endothermic animals range from those represented by thermal generalists to those characteristic for thermal specialists. While the generalists tolerate wide variations in body temperature (Tb), the specialists maintain Tb at a more constant level. The model has gained support from inter-specific comparisons relating to species and population levels. However, little is known about consistent among-individual variation within populations that could be shaped by natural selection. We studied the consistency of individual heterothermic responses to environmental challenges in a single population of yellow-necked mice (Apodemus flavicollis), by verifying the hypothesis that Tb variation is a repeatable trait. To induce the heterothermic response, the same individuals were repeatedly food deprived for 24 h. We measured Tb with implanted miniaturised data loggers. Before each fasting experiment, we measured basal metabolic rate (BMR). Thus, we also tested whether individual variation of heterothermy correlates with individual self-maintenance costs, and the potential benefits arising from heterothermic responses that should correlate with body size/mass. We found that some individuals clearly entered torpor while others kept Tb stable, and that there were also individuals that showed intermediate thermoregulatory patterns. Heterothermy was found to correlate negatively with body mass and slightly positively with the BMR achieved 1–2 days before fasting. Nonetheless, heterothermy was shown to be highly repeatable, irrespective of whether we controlled for self-maintenance costs and body size. Our results indicate that specialist and generalist thermoregulatory phenotypes can co-exist in a single population, creating a heterothermy continuum.
... Hibernating mammals exhibit an annual temperature rhythm [78,79] and alter the diversity and composition of gut microbiota over the circannual hibernation cycle [20,80]. Most mammals such as mice, desert hamsters (Phodopus roborovskii), and even humans show daily body temperature rhythm [81,82] and the diurnal variation of gut microbiota has been reported in mice [83,84]. A recent study showed that a 2-3°C increase in ambient temperature can cause a 34% loss in gut bacterial diversity in a vertebrate ectotherm, the common lizard (Zootoca vivipara) [85]. ...
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Background: Huddling is highly evolved as a cooperative behavioral strategy for social mammals to maximize their fitness in harsh environments. Huddling behavior can change psychological and physiological responses. The coevolution of mammals with their microbial communities confers fitness benefits to both partners. The gut microbiome is a key regulator of host immune and metabolic functions. We hypothesized that huddling behavior altered energetics and thermoregulation by shaping caecal microbiota in small herbivores. Brandt's voles (Lasiopodomys brandtii) were maintained in a group (huddling) or as individuals (separated) and were exposed to warm (23 ± 1 °C) and cold (4 ± 1 °C) air temperatures (Ta). Results: Voles exposed to cold Ta had higher energy intake, resting metabolic rate (RMR) and nonshivering thermogenesis (NST) than voles exposed to warm Ta. Huddling voles had lower RMR and NST than separated voles in cold. In addition, huddling voles had a higher surface body temperature (Tsurface), but lower core body temperature (Tcore) than separated voles, suggesting a lower set-point of Tcore in huddling voles. Both cold and huddling induced a marked variation in caecal bacterial composition, which was associated with the lower Tcore. Huddling voles had a higher α and β-diversity, abundance of Lachnospiraceae and Veillonellaceae, but lower abundance of Cyanobacteria, Tenericutes, TM7, Comamonadaceae, and Sinobacteraceae than separated voles. Huddling or cold resulted in higher concentrations of short-chain fatty acids (SCFAs), particularly acetic acid and butyric acid when compared to their counterparts. Transplantation of caecal microbiota from cold-separated voles but not from cold-huddling voles induced significant increases in energy intake and RMR compared to that from warm-separated voles. Conclusions: These findings demonstrate that the remodeling of gut microbiota, which is associated with a reduction in host Tcore, mediates cold- and huddling-induced energy intake and thermoregulation and therefore orchestrates host metabolic and thermal homeostasis. It highlights the coevolutionary mechanism of host huddling and gut microbiota in thermoregulation and energy saving for winter survival in endotherms.
Article
Nonresponding Siberian hamsters Phodopus sungorus do not develop the winter phenotype with white fur, low body mass (mb) and spontaneous torpor use in response to short photoperiod. However, their thermoregulatory response to fasting remains unknown. We measured body temperature and mb of 12 nonresponders acclimated to short photoperiod and then to cold, and fasted four times for 24h. Four individuals used torpor and in total we recorded 19 torpor bouts, which were shallow, short, and occurred at night. Moreover fasting increased the heterothermy index in all hamsters. Low mb was not a prerequisite for torpor use and mb loss correlated with neither heterothermy index nor torpor use. This is the first evidence that individuals which do not develop the winter phenotype, can use torpor or increase body temperature variability to face unpredictable, adverse environmental conditions. Despite the lack of seasonal changes, thermoregulatory adjustments may increase winter survival probability of nonresponders.
Chapter
The weather of most geographical regions changes substantially with the seasons. Therefore, alterations in the thermal environment, rainfall and other environmental variables require a responsive adjustment of the physiology of animals to enable survival. However, geographic regions of the world differ substantially in their seasonal challenges. Whereas temperate and high latitude/altitude regions are characterised by warm Tas in summer and often high primary productivity, Tas in winter are low resulting in little or no primary productivity. Untimely, this low Ta and low productivity occur in the season when energy expenditure of animals often is high. In contrast, tropical areas may remain rather warm in winter, but often show strong seasonal changes in rainfall with almost all precipitation in summer and none in winter (Dausmann and Warnecke 2016). In subtropical areas the high summer heat may limit plant productivity. During the mild subtropical winter nectar production can be much higher than in summer (Ford 1989). In deserts Tas are often too hot, evaporation too high and/or precipitation too low in summer for significant plant growth, whereas winters can be rather mild during the day, at least in deserts not too far from the equator, as for example in the Australian deserts. The seasonal change in photoperiod, a reliable environmental signal for seasonal change in physiology, also differs enormously between high and low latitudes. Such regional differences are reflected in the seasonal expression of torpor.
Chapter
In this chapter, the diversity of heterotherms, where they live and how they differ from each other is covered in detail. When data from free-ranging animals were available these were used preferentially, but information on captive animals is also included. As the extent of available data differs substantially among taxa, the information provided reflects what is known about a specific group to a large extent. To put the information on heterothermic endotherms into context with other organisms, I will address terrestrial ectotherms first.
Chapter
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The Djungarian hamster is a rodent species that expresses both spontaneous daily torpor (SDT) when acclimated to winter conditions as well as fasting-induced torpor (FIT) during summer. In an earlier report we argued that these two thermoregulatory phenomena differ in several parameters. In the present study, we further complete this comparison by showing that metabolic rate patterns differ between both SDT and FIT. SDT bouts were significantly longer and deeper compared to FIT bouts. Additionally, respiratory quotient measures support the view that SDT is entered from a state of energetic balance while FIT appears to be an emergency shutdown of energy demanding thermogenesis due to a shortage of energy sources. In a second experiment, we also confirm that brief periods of food restriction during the hamsters’ torpor season increase the frequency of SDT, but do not affect its depth or duration. Although winter-acclimated animals could flexibly alter torpor frequency in order to stay in energetic balance, we also found evidence for torpor expression patterns that resembled FIT, rather than SDT. Consequently, if energetic challenges cannot be compensated with increased SDT expression any longer, the hamsters seem to be driven in a negative energy balance resulting in FIT as a last resort.
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Radiotelemetry is used to quantify behavioral, ecological, and physiological variables of animals. Because of technological limitations, relative transmitter size generally increases with decreasing body mass of the study animal, and the recommended transmitter mass of <5% of body mass often prohibits work on small mammals. We compared burst running speed, important for predator avoidance, in 2 small marsupials, Sminthopsis crassicaudata (fat-tailed dunnart) and Planigale gilesi (Giles' planigale), without and with implanted transmitters. In both species maximum running speed was not affected by the transmitters, whose mass ranged from 6.4% to 14.1% of body mass. Further, relative transmitter mass was not correlated with maximum running speed. Consequently, transmitters well above 5% of body mass need not affect locomotor performance of small terrestrial mammals.
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Data on desert hamster Phodopus roborovskii winter activity and seasonal patterns of reproduction are scarce. During 9 years we maintain a colony of desert hamsters under natural temperature and light regimes. These natural conditions suggest that the data on breeding activity may be in a good accordance with that in the wild. None of observed animals showed signs of torpor or hibernation in winter - even at about 40 deg. C below zero. The first peak of breeding (2.4 litters born per 10 pairs and 3.5 pups per litter in average) occurs in April and the second one (2.9 - 2.6 litters per 10 pairs and 3.9 - 3.6 pups per litter in average) in June - July. In autumn and early winter, the intensity of breeding declines to 0.1 - 0.4 litters per 10 pairs but does not cease completely. All adult males have visible testes and all adult females have opened vaginas entries through the year. The averaged males' plasma level of testosterone, being maximal in summer, declines in autumn and early winter, but single hamsters keep their testosterone high even under shortest photoperiod and during cold months. In spring, average testosterone level significantly increases but does not reach summer values.
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Study of ecological adaptations, including torpor, related to survival through the adverse conditions of the autumn-winter season is important for both the estimation of the body reserves in mammals in general and the search for the ways to increase the cold-stress resistance in humans. The changes in the body temperature during the period from October to May were studied in hamsters of six species under the natural photoperiod and temperature conditions. Incidental winter torpor (a drastically decreased physiological activity) was detected in all species except Cricetulus griseus; in three of them, it had not been observed before. No specific combination of conditions causing torpor was identified. Apparently, it is determined by individual characteristics of the animal. Torpors were the most frequent in January, at temperatures from −15 to −5°C; their depth was positively correlated with the ambient temperature. Since torpor is a rare event, it is assumed to be a stored resource of the body allowing animal to save energy and occurring only in extreme situations.
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Hibernation and daily torpor are two distinct forms of torpor, and although they are related, it is not known how and in which sequence they evolved. As the pattern of torpor expressed by the oldest marsupial order the opossums (Didelphimorphia) may provide insights into the evolution of torpor, we aimed to provide the first quantitative data on the thermal biology and torpor expression of the rare Patagonian opossum (Lestodelphys halli). It is the opossum with the southernmost distribution, has a propensity of autumnal fattening, and therefore, is likely to hibernate. We captured two male Lestodelphys, which while in captivity displayed strong daily fluctuations of body temperatures (Tb) measured with implanted miniature data loggers even when they remained normothermic. In autumn and early winter, torpor was expressed occasionally when food was available, but cold exposure and food withdrawal increased torpor use. The mean Tb throughout the study was 32.2 ± 1.4 °C, the minimum Tb measured in torpid Lestodelphys was 7.7 °C, average torpor bout duration was 10.3 h, and the maximum torpor bout duration was 42.5 h. Thus, the pattern of torpor expressed by Lestodelphys was intermediate between that of daily heterotherms and hibernators suggesting that it may represent an ancestral opportunistic torpor pattern from which the derived patterns of daily torpor and seasonal hibernation diverged.
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In Phodopus sungorus spontaneous shallow daily torpor occurred only during winter. Frequency of torpor was not affected by low ambient temperature but the seasonal cueing seems primarily dependent on photoperiodic control. Maximum torpor frequency was found in January with 30% of all hamsters living inside or outside being torpid at a time. It is calculated that torpor will reduce long term energy requirements of Phodopus by only 5%. Therefore it is concluded that torpor is not primarily aimed to reduce energy requirements but to guarantee survival of a fraction of a population during short periods of extreme cold load or inaccessability of food.
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Torpor is the physiologically controlled reduction of metabolic rate and body temperature experienced by small birds and mammals when facing periods of low temperature and/or food shortage. In this study, we provide a first quantitative description of torpor in the relict marsupial Dromiciops gliroides by: (1) characterizing body temperature (T B) and torpor patterns, (2) evaluating the combined effects of ambient temperature and different levels of food restriction on torpor incidence and (3) exploring the metabolic depression during torpor. D. gliroides exhibited short bouts of torpor on a daily basis, during which T B decreased close to ambient temperature. During the active phase, T B also exhibited pronounced variation (range 34–38°C). In order to evaluate the consistency of torpor, we computed the repeatability of T B. Using the whole dataset, repeatability was significant (τ = 0.28). However, when torpid individuals were excluded from the analysis, repeatability was non-significant: some individuals were more prone to experience torpor than others. Our results indicate that this species also exhibits short bouts of daily torpor, whose depth and duration depends on the joint effects of T A and food availability. At T A = 20°C, the maximum torpor incidence was found at 70–80% food reduction, while at both extremes of the food continuum (100 and 0–10% food reduction) individuals were completely active, although considerable variation in T B was recorded. At T A = 10°C, individuals developed a deep form of torpor that was independent of the amount of food provided. On average, torpid D. gliroides reduced their metabolic rate up to 92% of their active values. In general, our results suggest that T A was the most immediate determinant of torpor, followed by energy availability.
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Many animal species employ natural hypothermia in seasonal (hibernation) and daily (torpor) strategies to save energy. Facultative daily torpor is a typical response to fluctuations in food availability, but the relationship between environmental quality, foraging behaviour and torpor responses is poorly understood. We studied body temperature responses of outbred ICR (CD-1) mice exposed to different food reward schedules, simulating variation in habitat quality. Our main comparison was between female mice exposed to low foraging-cost environments and high-cost environments. As controls, we pair-fed a group of inactive animals (no-cost treatment) the same amount of pellets as high-cost animals. Mice faced with high foraging costs were more likely to employ torpor than mice exposed to low foraging costs, or no-cost controls (100% versus 40% and 33% of animals, respectively). While resting-phase temperature showed a non-significant decrease in high-cost animals, torpor was not associated with depressions in active-phase body temperature. These results demonstrate (i) that mice show daily torpor in response to poor foraging conditions; (ii) that torpor incidence is not attributable to food restriction alone; and (iii) that high levels of nocturnal activity do not preclude the use of daily torpor as an energy-saving strategy. The finding that daily torpor is not restricted to conditions of severe starvation puts torpor in mice in a more fundamental ecological context.
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During daily torpor and hibernation metabolic rate is reduced to a fraction of the euthermic metabolic rate. This reduction is commonly explained by temperature effects on biochemical reactions, as described by Q 10 effects or Arrhenius plots. This study shows that the degree of metabolic suppression during hypothermia can alternatively be explained by active downregulation of metabolic rate and thermoregulatory control of heat production. Heat regulation is fully adequate to predict changes in metabolic rate, and Q 10 effects are not required to explain the reduction of energy requirements during hibernation and torpor.
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Although it is well established that during periods of torpor heterothermic mammals and birds can reduce metabolic rates (MR) substantially, the mechanisms causing the reduction of MR remain a controversial subject. The comparative analysis provided here suggests that MR reduction depends on patterns of torpor used, the state of torpor, and body mass. Daily heterotherms, which are species that enter daily torpor exclusively, appear to rely mostly on the fall of body temperature (Tb) for MR reduction, perhaps with the exception of very small species and at high torpor Tb, where some metabolic inhibition may be used. In contrast, hibernators (species capable of prolonged torpor bouts) rely extensively on metabolic inhibition, in addition to Tb effects, to reduce MR to a fraction of that observed in daily heterotherms. In small hibernators, metabolic inhibition and the large fall of Tb are employed to maximize energy conservation, whereas in large hibernators, metabolic inhibition appears to be employed to facilitate MR and Tb reduction at torpor onset. Over the ambient temperature (Ta) range where torpid heterotherms are thermo-conforming, the Tb-Ta differential is more or less constant despite a decline of MR with Ta; however, in thermo-regulating torpid individuals, the Tb-Ta differential is maintained by a proportional increase of MR as during normothermia, albeit at a lower Tb. Thermal conductance in most torpid thermo-regulating individuals is similar to that in normothermic individuals despite the substantially lower MR in the former. However, conductance is low when deeply torpid animals are thermo-conforming probably because of peripheral vasoconstriction.
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We studied how food abundance and consumption regulates torpor use and internal organ size in the Chilean mouse-opossum Thylamys elegans (Dielphidae), a small nocturnal marsupial, endemic in southern South America. We predicted that exposure to food rations at or above the minimum energy levels necessary for maintenance would not lead to any signs of torpor, while reducing food supply to energy levels below maintenance would lead to marked increases in frequency, duration and depth of torpor bouts. We also analyzed the relationship between food availability and internal organ mass. We predicted a positive relationship between food availability and internal organ size once the effect of body size is removed. Animals were randomly assigned to one of two groups and fed either 70, 100 or 130% of their daily energy requirement (DER). We found a positive and significant correlation between %DER and body temperature, and also between %DER and minimum body temperature. In contrast, for torpor frequency, duration and depth, we found a significant negative correlation with %DER. Finally, we found a significant positive correlation between the %DER and small intestine and ceacum dry mass. We demonstrate that when food availability is limited, T. elegans has the capacity to reduce their maintenance cost by two different mechanisms, that is, increasing the use of torpor and reducing organ mass.
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The Phodopus roborovskii individuals on Hunshandake sandy land of Inner Mongolia were trapped monthly, and the contents in their cheek pouch and stomach were analyzed to study the food consumption and feeding characters of P. roborovskii on the sandy land. The results showed that plant seeds were the main food of P. roborovskii, contributing more than 85% of the food consumption. P. roborovskii also took insects, plant leaves and stems as its food. The daily food consumption of P. roborovskii was highly correlated with its body weight, and the per unit body weight of juvenile P. roborovskii consumed more food than that of the adult. The functional relationship of daily food consumption (D) and body mass (M) could be expressed by D = 1.422 x InM - 1.780. Based on the population structure of P. roborovskii, its daily food consumption was calculated as about 2 g of plant seeds.
Chapter
Torpor is the most effective means of energy conservation available to mammals and birds. Torpor is often viewed as a state of utter inactivity devoid of any behavioral aspects. However, recent work has shown that even torpid individuals do express behaviors. Torpid mammals can move at low body temperatures from a torpor site into the sun to passively rewarm and minimize energy expenditure. Social torpor involves coordinated interaction among individuals, and some species even eat or mate while torpid. Behaviors expressed before the torpor season include selection of suitable hibernacula and storage or hoarding of appropriate and sufficient amounts of fuel.
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The body temperature () of Mus musculus fed ad libitum was labile and varied between 36.0 ± 0.3 and 39.3 ± 0.3 C at ambient temperatures () ranging from 2.5 to 38.0 C. The thermal neutral oxygen consumption was 1.47 ml O₂/g.h, which occurred between the lower critical temperature of 31.0 C and the upper critical temperature of 35.0 C. The thermal conductance decreased from a high of 0.26 ml O₂/g.h.C to a low of 0.15 ml O₂/g-h-C as the decreased from 31.0 to 2.5 C. The conductance increased from the lower to the upper limits of the thermal neutral zone, reaching a maximum of 0.43 ml O₂/g·h·C at a of 35.0 C. The highest conductance was 0.74 ml O₂/g·h·C at a of 38.0 C. The lability of increased with a restriction of the daily food ration, averaging 34.5 ± 0.3 C and ranged between 22.0 and 37.0 C at of 19-20 C. Five of 14 animals on ad libitum food allotments became torpid within 24 h after food was withheld. Heat production appeared to be suppressed during entry into torpor, which was attributed to a reduction in shivering. The "critical " of torpid mice was 16-19 C. Oxygen consumption was directly related to at a of 31 C and above, but it remained relatively constant at between 31 and 16 C. The - gradient and oxygen consumption of torpid mice increased at below 16 C. The length of the torpor period was inversely related to between 23 and 16 C but was frequently interrupted with spontaneous arousals at a below 16 C. During arousal, the oxygen consumption at a particular was greater than at the corresponding during entry into torpor. Arousal was frequently accompanied by a metabolic peak, followed by a decrease of and a decline in oxygen consumption. The arousal rate ranged between 0.11 C and 0.25 C/ min and appeared to be independent of the at which arousal took place. Torpid animals could not right themselves, stand, and shiver until their reached 18 C. They could gather and ingest seeds at a of 24 C and behaved similarly to normothermic animals when the was above 26 C.
Article
Short-day (9 light:15 dark), cold-acclimated Peromyscus leucopus known to enter torpor (no. = 24) and P. leucopus never observed in torpor (no. = 12) were compared with and without a 5-g nest at 13, 7, and 1 C over 9 wk. Oxygen consumption and body temperature were monitored approximately hourly for 2-3 days under each treatment. A second group of short-day, cold-acclimated mice (13 torpid and 14 nontorpid) were monitored for oxygen consumption with and without a 5-g nest at 13 C, first individually and 10 days later as huddles of three. For individual mice, the time required to enter torpor (3.0-4.5 h), duration of torpor (4-5 h), and minimum body temperature during torpor (21-23 C) remained fairly constant at different ambient temperatures. The metabolic rate [cm³O₂/(g · h)] necessary to maintain minimum body temperature during torpor without a nest was 2.1 at 13, 3.0 at 7, and 3.7 at 1 C, while metabolic rates during the normothermic period at these temperatures were 4.8, 5.5, and 6.7, respectively. A similar trend, but with lower values, occurred with a nest. Without a nest, torpid mice had a mean daily metabolic rate which was 20% less at 13, 21% at 7, and 9% at 1 C than the corresponding value of nontorpid animals. Torpid mice with a 5-g nest reduced metabolic rate at those temperatures by 43%, 44%, and 34%, respectively, relative to nontorpid mice without a nest. Daily torpor and huddling together provided a 58% energetic saving at 13 C relative to individually housed, nontorpid mice. The addition of a nest fostered a 74% daily energy savings versus nontorpid, individual mice without a nest.
Article
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 30g 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.
Article
Most living beings change their behavior and physiology on a daily basis (24 h), with rhythmicity a fundamental property of living matter. Circadian rhythm is one of the important behavioral and physiological properties of wild animals. The desert hamster (Phodopus roborovskii) is a small rodent species which inhabits mainly desert and semi-arid environments in Inner Mongolia, China. Although field observations have shown that this species is mainly active at night, we know little about their biology and ecology, especially ecological physiology. In order to understand more about the behavioral and physiological adaptations of desert rodents, 8 desert hamsters (4 males and 4 females, weighing 20. 4 - 27.5 g and aged between 11 and 13 months) were individually caged and kept under a temperature of (23±1)°C and a photoperiod of (16L:8D). Transmitters (ER-4000, Mini Mitter, USA) were implanted in the abdominal cavity of each hamster, and their body temperatures and activities were monitored for 24 h using a Vital View system. Their metabolic rates were also measured for 24 h using a TSE respirometry system (LabMaster, Germany). Our results showed that the average body temperature of the desert hamster is (37. 27±0. 39)°C during the night and (36. 11±0. 18)°C during the day. Their average metabolic rate is (4. 65 ±1. 10)mLO2· g-1·h-1 and (3. 09 ±0. 42) mLO2· g-1·h-1 during the night and day, respectively, and their average activity is (237±145) counts /0. 1h during the night and(38±5) counts /0. 1h during the day. Although ultradian activity rhythms were found over periods of 4, 6, 8, and 12 h, their amplitudes were much smaller than that of the 24h-circadian rhythm, which had a peak at (22. 7±0. 6) h. A similar pattern was observed for body temperature, which peaked at (23. 1±0. 5)h. Based on our analyses, body temperature, activity and metabolic rate all showed circadian rhythms and synchronization, with maxima during the night and minima during the day. These are typical properties of nocturnal animals, and support the idea that the desert hamster is a typical nocturnal rodent species. Behavioral observations in the field support this conclusion. Our results suggest that the desert hamster could be an ideal model for the study of the evolution and mechanisms of circadian rhythms inr wild animals.
Article
Core body temperatures in 14 Peromyscus maniculatus nubiterrae were assessed via biotelemetry within a few days after their capture in the southern Appalachians during summer months. With both food and water available ad lib., no mice displayed spontaneous daily torpor. Partial restriction of food, with no reduction in water, induced reversible torpor bouts in every individual. The mean duration of torpor was 4.0 ± 0.3 h, with a mean minimum body temperature of 22.7 ± 0.8 C. These torpor characteristics are not substantially different from those recorded in these mice during other seasons at lower ambient temperatures, suggesting that stress-induced torpor, unlike spontaneous daily torpor, is retained as a short-term survival mechanism throughout the year in this montane subspecies.
Article
Both ventilation frequency (f) and the rate of oxygen consumption ( $dot{V}o_{2}$ ) change dramatically as Selasphorus hummingbirds enter and arouse from torpor. Changes in f and $dot{V}o_{2}$ are generally coincident, but the proportional changes in the two parameters are not identical, and their relationship varies at different ambient temperatures ( $T_{a}$ ) and between entry and arousal Ventilation frequency and $dot{V}o_{2}$ , may be substantially decoupled, particularly during the latter stages of entry into torpor and also during arousals of birds with steady-state torpor body temperatures ( $T_{b}$ ) > 20° C Contrary to what generally has been reported in birds, the time of active inspiration ( $T_{INV}$ ) in hummingbirds usually exceeds the time of expiration ( $T_{EX}$ ). The large decrease in f that occurs as hummingbirds go torpid is accomplished by lengthening $T_{INV}$ , by slightly increasing $T_{EX}$ , and by inserting a nonventilatory pause (NVP) into the inspiratoryportion of the ventilation cycle. The NVP occurs in the middle of inspiration such that inspiratory air flow occurs in two separate stages. At the lowest f's seen in torpor (1-2 breaths/min), ventilation occurs in bursts of breaths separated by NVPs that lengthen into apneas lasting up to 5 min.
Article
Hibernation is widely regarded as an adaptation to seasonal energy shortage, but the actual influence of energy availability on hibernation patterns is rarely considered. Here we review literature on the costs and benefits of torpor expression to examine the influence that energy may have on hibernation patterns. We first establish that the dichotomy between food- and fat-storing hibernators coincides with differences in diet rather than body size and show that small or large species pursuing either strategy have considerable potential scope in the amount of torpor needed to survive winter. Torpor expression provides substantial energy savings, which increase the chance of surviving a period of food shortage and emerging with residual energy for early spring reproduction. However, all hibernating mammals periodically arouse to normal body temperatures during hibernation. The function of these arousals has long been speculated to involve recovery from physiological costs accumulated during metabolic depression, and recent physiological studies indicate these costs may include oxidative stress, reduced immunocompetence, and perhaps neuronal tissue damage. Using an optimality approach, we suggest that trade-offs between the benefits of energy conservation and the physiological costs of metabolic depression can explain both why hibernators periodically arouse from torpor and why they should use available energy to minimize the depth and duration of their torpor bouts. On the basis of these trade-offs, we derive a series of testable predictions concerning the relationship between energy availability and torpor expression. We conclude by reviewing the empirical support for these predictions and suggesting new avenues for research on the role of energy availability in mammalian hibernation.
Article
The circadian rhythm of animals is an adaptation to predictable variation in environmental conditions. Multiple internal oscillators may allow animals to cope with environmental oscillations in different frequencies. Heat stress and dramatic differences between night and day temperatures are the main selective pressures of the diel activity of desert mammals, particularly small-sized rodents. We tested the hypotheses that the diel activities of desert hamsters (Phodopus roborovskii) would be entrained by ambient humidity and temperature. We predicted that increases in night temperature and humidity would improve the propensity to perform activities of the hamster. We observed hourly activities of desert hamsters under semi natural conditions for 24 consecutive hours, with seven replicates in 7 different days. We fit generalized linear mixed models to observed proportions of active hamsters, temperatures, and relative humidity. Observed diel activities of desert hamsters consisted of three harmonic oscillations in the periodicities of 24hours, 12hours, and 6hours, respectively. Furthermore, probabilities to perform activities were positively related to night temperature and humidity. Therefore, the diel activities of desert hamsters are synchronized by atmospheric humidity, temperatures, and environmental cues of ultradian fluctuations.
Article
1.1. Tb in lab-born Peromyscus maniculatus and P. leucopus was monitored via surgically implanted transmitters during exposure to 10°C and 9L:15D.2.2. With food available ad lib, no significant interspecific differences in the incidence, frequency, and patterns of spontaneous daily torpor were found.3.3. Restriction of food to 75% daily ration increased the incidence of torpor in both species, and induced longer, deeper torpor bouts.4.4. A significantly greater proportion of P. maniculatus responded to rationing by becoming torpid. Furthermore, induced torpor boults in this species were more profound than those in P. leucopus.5.5. This differential response is consistent with differences in these species respective environments.
Article
Many biological variables related to energy turnover including torpor, the most efficient energy-saving mechanism available to mammals, scale with body size, but the implications for animals living in their natural environment remain largely unknown. We used radio-telemetry to obtain the first data on the activity patterns and torpor use of two sympatric, free-ranging dasyurid marsupials, the stripe-faced dunnart Sminthopsis macroura (16.6±1.5 g) and the more than six-times larger kowari Dasyuroides byrnei (109.4±16.4 g), during winter in arid Queensland, Australia. Eight dunnarts and six kowaries were surgically implanted with temperature-sensitive radio-transmitters and monitored for 14–59 days. Both species commenced activity shortly after sunset, but while kowaries remained active through most of the night, dunnarts usually returned to their burrows before midnight. In dunnarts, short activity was associated with the frequent use of daily torpor (99.1% of observation days). Torpor often commenced at night, with body temperature (Tb) decreasing to a minimum of 11.3 °C, and torpor lasted up to 26 h. In contrast, only 50% of the kowaries entered torpor and torpor was brief (maximum 4 h), shallow (minimum Tb 25.3 °C) and restricted to the daytime rest-phase. Our study suggests that in winter, the smaller dunnarts can remain active only during the warmer first half of the night and energy-saving torpor becomes part of their daily routine. In contrast, it appears that the larger kowaries are less affected by cold winter nights and can maintain high night-time activity levels and commence reproduction already in winter. Hence, they enter torpor only occasionally and only during the rest phase.
Article
Summary Most studies of the thermoregulatory ecology of bats have been limited to laboratory experiments or studies of individuals roosting in artificial structures. We investigated the interaction between thermoregulatory behaviour and roost choice in reproductive female Western Long-Eared Bats, Myotis evotis (H. Allen), roosting solitarily in natural rock crevices. The study was conducted in the badlands of the South Saskatchewan River Valley, Alberta, Canada, during 1997 and 1998. Individuals used torpor every day and the amount of time spent in torpor was primarily influenced by the amount of time available to do so. Minimum body temperature was influenced by ambient temperature, although the form of this relationship differed between pregnant and lactating females. Pregnant females used deep torpor more frequently than lactating females. All individuals roosted in rock crevices but pregnant and lactating females chose roosts that were different in structure and thermal characteristics. Pregnant females chose horizontal roosts that cooled at night but warmed quickly during the day, thus allowing passive rewarming from torpor. Lactating females chose vertical roosts that stayed warm at night when non-volant pups were present, thereby minimizing thermoregulatory costs to the young. The behaviours observed are adaptive, but differ from those of other temperate-zone insectivorous bats that have been studied in the past. This highlights the importance of studying free-ranging animals living in natural habitat if we are to have an accurate view of thermoregulatory strategies and the importance of roost characteristics for roost-site selection.
Article
1.Thermoregulatory behavior of fed and fasted desert hamsters (Phodopus roborovskii) acclimated to summer- [16 light (L):8 dark (D), ambient temperature (Ta)=26.5 °C] and winter-like (8L:16D, Ta=10 °C) conditions was studied. Body temperature (Tb), selected temperature and activity were measured in hamsters placed in a thermal gradient system for 48 h.2.Acclimation to winter-like days led to the decrease in body mass by 14% and in body temperature by 1 °C. On the contrary, selected Ta was higher by about 3 °C than in summer-like acclimated hamsters. Fasting affected only temperatures selected by night in winter-like acclimated hamsters.3.Winter-like acclimation led to physiological changes, which may facilitate surviving long winter season. In the face of food shortage, behavioral thermoregulation may markedly reduce the energetic cost of normothermy.
Article
The adjustments in thermal physiology and energetics were investigated in male desert hamsters (Phodopus roborovskii) which were acclimated to 5°C for 4 weeks. Mean core body temperature in cold acclimated animals decreased by 0.21°C compared with controls. Further analysis revealed that the decrease mainly occurred in the scotophase, while in the photophase core body temperature remained constant during the whole cold acclimation. Thermogenic capacity, represented by resting metabolic rate and nonshivering thermogenesis increased in cold acclimated hamsters from initial values of 1.38 ± 0.05 and 5.32 ± 0.30 to 1.77 ± 0.08 and 8.79 ± 0.31 mlO(2) g(-1) h(-1), respectively. After cold acclimation, desert hamsters maintained a relative stable body mass of 21.7 ± 0.1 g very similar to the controls kept at 23°C (21.8 ± 0.1 g). The mean values of food intake and digestible energy (metabolisable energy) in cold acclimated hamsters were 5.3 ± 0.1 g day(-1) and 76.3 ± 0.9 kJ day(-1) (74.8 ± 0.9), respectively, which were significantly elevated by 76.7 and 80.4% compared to that in control group. The apparent digestibility was 81.0 ± 0.3% in cold acclimated animals which was also higher than the 79.7 ± 0.2% observed in controls. This increase corresponded with adaptive adjustments in morphology of digestive tracts with 20.2 and 36.8% increases in total length and wet mass, respectively. Body fat mass and serum leptin levels in cold acclimated hamsters decreased by 40.7 and 67.1%, respectively. The wheel running turns and the onset of wheel running remained unchanged. Our study indicated that desert hamsters remained very active during cold acclimation and displayed adaptive changes in thermal physiology and energy metabolism, such as enhanced thermogenic and energy processing capacities.
Article
Basal metabolic rate (BMR) has been shown to be a highly flexible phenotypic trait both between and within species, but the physiological, biochemical and molecular mechanisms are still unclear. Brandt's voles (Lasiopodomys brandtii) and Mongolian gerbils (Meriones unguiculatus) are two sympatric rodent species in Inner Mongolian grasslands of China. It has been shown that Brandt's voles have higher metabolic rate than Mongolian gerbils. In this study, we elucidated the inter-specific variation in BMR integratively from the molecular levels to whole organism. Our results showed that differences in organ mass were not good predictors for the observed variations in BMR, while variations in the activity of thyroid hormones and the metabolic biochemical markers of tissues, such as mitochondria density, cytochrome c oxidase activity and state 4 respiration, were strongly correlated with variations in BMR, and there was also a positive relationship between residuals of T(3)/T(4) and state 4 respiration, suggesting that thyroid hormones play an important role in the determination of BMR variations.
Article
Siberian hamsters express torpor spontaneously after several weeks of exposure to short days. In long days, torpor is expressed only when food intake is restricted. Hamsters maintained in a long photoperiod (16 h light/day) at 15 degrees C expressed daily torpor during food restriction both before and after bilateral ablation of the suprachiasmatic nucleus (SCN). Hamsters housed in short days (8 h light/day, ambient temperature 15 degrees C) and fed ad libitum displayed torpor before, but not after, ablation of the SCN (SCNX). Torpor was reinstated in all short-day SCNX hamsters during postoperative food restriction and persisted in several animals even after ad libitum feeding was reinstated. Torpor was entrained to the light-dark cycle in both long- and short-day hamsters preoperatively but appeared to occur in a temporally random fashion in SCNX animals. SCNX hamsters, unlike control animals, displayed multiple torpor bouts per 24 h. The SCN is not essential for the expression of torpor but plays a crucial role in its temporal organization.
Article
1. The daily torpor was measured by oxygen uptake in Djungarian hamsters during adaptation to a short photoperiod (SP: 10L, 14D) at 20 °C. In these constant conditions the torpor presented metabolic characteristics and a daily time course independent of the duration of adaptations to SP. 2. The frequency of torpor bouts increased during SP exposure and its maximum was reached after about 130 days. The frequency of torpor was greater in males than in females. 3. The incidence of torpor was increased by constant dark exposure and this is discussed as a protective mechanism for the individual animal's ability to survive. 4. The temporal organization of daily torpor was demonstrated to be directly synchronized by the day-night cycle and to be controlled by an endogenous circadian function.
1. 1. In winter spontaneous torpor occured only in mice that had been acclimated to cold weather the preceding fall. 2. 2. Daily spontaneous torpor was very frequent from late fall to early spring. Minimum thoracic temperatures averaged 17·3°C and minimum heart rate was 60 beats/min. 3. 3. All mice became torpid when fasted in late spring and summer. Fasting-induced torpor differed from spontaneous torpor in a slower rate of arousal, higher minimum thoracic temperature and irregular heart rhythm.
Article
This study compared torpor as a response to food deprivation and low ambient temperature for the introduced house mouse (Mus musculus) and the Australian endemic sandy inland mouse (Pseudomys hermannsburgensis). The house mouse (mass 13.0+/-0.48 g) had a normothermic body temperature of 34.0+/-0.20 degrees C at ambient temperatures from 5 degrees C to 30 degrees C and a basal metabolic rate at 30 degrees C of 2.29+/-0.07 mL O2 g(-1) h(-1). It used torpor with spontaneous arousal at low ambient temperatures; body temperature during torpor was 20.5+/-3.30 degrees C at 15 degrees C. The sandy inland mouse (mass 11.7+/-0.16 g) had a normothermic T(b) of 33.0+/-0.38 degrees C between T(a) of 5 degrees C to 30 degrees C, and a BMR of 1.45+/-0.26 mL O2 g(-1) h(-1) at 30 degrees C. They became hypothermic at low T(a) (T(b) about 17.3 degrees C at T(a)=15 degrees C), but did not spontaneously arouse. They did, however, survive and become normothermic if returned to room temperature (23 degrees C). We conclude that this is hypothermia, not torpor. Consequently, house mice (Subfamily Murinae) appear to use torpor as an energy conservation strategy whereas sandy inland mice (Subfamily Conilurinae) do not, but can survive hypothermia. This may reflect a general phylogenetic pattern of metabolic reduction in rodents. On the other hand, this may be related to differences in the social structure of house mice (solitary) and sandy inland mice (communal).
  • Q.-S Chi
Q.-S. Chi et al. / Comparative Biochemistry and Physiology, Part A 199 (2016) 71–77