The responses of metabolic rate and neuropeptides to food deprivation in striped hamsters (Cricetulus barabensis) with different basal metabolic rate.

High basal metabolic rate (BMR) is related to a powerful metabolic engine even under food shortage, which can lead to high levels of daily energy expenditure and requires more energy for maintenance in small mammals. To test the hypothesis that animals with different BMR levels respond differently to food shortage, we compared the changes in metabolism, morphology, and gene expression in response to food deprivation (FD) in male-striped hamsters (Cricetulus barabensis) with low (L)- or high (H)-BMR levels. After 36 hr of FD, energy expenditure, metabolic rate (MR), mass of body composition, and leptin and agouti-related peptide gene expressions in the white adipose tissues and the hypothalamus, respectively, decreased significantly in hamsters. The energy expenditure of H-BMR hamsters was reduced more than that of L-BMR hamsters after 36 hr of FD. Furthermore, MR was significantly reduced by FD, and that of the H-BMR group decreased more than that of the L-BMR group during the daytime. Therefore, our data suggest that striped hamsters with different BMR display different responses to variations in food availability. During FD, MR in H-BMR hamsters was more flexible than that in L-BMR animals and L-BMR hamsters could not reduce their MR any lower.

Precocious Torpor in an Altricial Mammal and the Functional Implications of Heterothermy During Development.

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.

Brown adipose tissue plays thermoregulatory role within the thermoneutral zone in Mongolian gerbils (Meriones unguiculatus).

Brown adipose tissue (BAT) plays an important role in thermoregulation and many metabolic processes in small mammals, especially in cold adaptation. However, in warm adaptation, ambient temperature cannot directly activate BAT by sympathetic nervous system. Mongolian gerbils exhibit a wider thermoneutral zone (26.5-38.9 °C). We hypothesized that BAT atrophied near the lower critical temperature and further atrophied near the upper critical temperature. Male gerbils were acclimated to 23 °C, 27 °C or 37 °C, respectively, for 3 weeks. Results showed that regulatory non-shivering thermogenesis did not change in gerbils acclimated to 27 °C compared with 23 °C group, whereas it was reduced by 43.5% in gerbils acclimated to 37 °C. Bigger lipid droplet in BAT was observed in gerbils acclimated to 27 °C and 37 °C compared with 23 °C group, while the expression of uncoupling protein 1 and tyrosine hydroxylase was only reduced in gerbils acclimated to 37 °C. Further, thermoneutral acclimation did not change BAT thermogenesis by down-regulation of peroxisome proliferator-activated receptor gamma coactivator-1α, PR domain containing 16, peroxisome proliferator-activated receptor-α or peroxisome proliferator activated receptor-γ gene expression in BAT. In addition, body temperature was reduced in gerbils acclimated to 37 °C compared with 23 °C group, which was associated with a decreased resting metabolic rate and regulatory non-shivering thermogenesis. In conclusion, BAT does not atrophy near the lower critical temperature, whereas it atrophies near the upper critical temperature, suggesting that BAT may play thermoregulatory role within the TNZ in Mongolian gerbils.

Thyroid hormones mediate metabolic rate and oxidative, anti-oxidative balance at different temperatures in Mongolian gerbils (Meriones unguiculatus).

Oxidative damage is a potential physiological cost of thermoregulation during seasonal adjustments to air temperature (Ta) in small mammals. Here, we hypothesized that Ta affects serum thyroid hormone levels and these hormones can mediate the changes in metabolic rate and oxidative damage. Mongolian gerbils (Meriones unguiculatus) were acclimated at different Tas (5 °C, 23 °C and 37 °C) for 3 weeks. Serum tri-iodothyronine (T3) levels increased at 5 °C but decreased at 37 °C compared to the control (23 °C). Protein carbonyls increased in liver at 37 °C compared with control, however, lipid damage (malonaldehyde, MDA) in both serum and liver was unrelated to Ta. After the effects of different Tas on thyroid hormone levels and oxidative damage markers were determined, we further investigate whether thyroid hormones mediated metabolic rate and oxidative damage. Another set of gerbils received 0.0036% L-thyroxin (hyperthyroid), 0.04% Methylimazol (hypothyroid) or water (control). Hypothyroid group showed a 34% reduction in resting metabolic rate (RMR) also 42% and 26% increases in MDA and liver protein carbonyl respectively, whereas hyperthyroid group had higher RMR, liver mass and superoxide dismutase (SOD) compared to control. Serum T3 or T3/T4 levels were correlated positively with RMR, liver mass, and SOD, but negatively with MDA and uncoupling protein 2 (UCP2). We concluded that high Ta induced hypothyroidism, decreased RMR and increased oxidative damage, whereas low Ta induced hyperthyroidism, increased RMR and unchanged oxidative damage. These data supported our hypothesis that thyroid hormones can be a cue to mediate metabolic rate and different aspects of oxidative and antioxidant activities at different Tas.

Correction to: Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure.

Following publication of the original article [1], the authors reported an error in the caption of Fig. 4.

Huddling Conserves Energy, Decreases Core Body Temperature, but Increases Activity in Brandt's Voles (Lasiopodomys brandtii).

Huddling as social thermoregulatory behavior is commonly used by small mammals to reduce heat loss and energy expenditure in the cold. Our study aimed to determine the effect of huddling behavior on energy conservation, thermogenesis, core body temperature (Tb) regulation and body composition in Brandt's voles (Lasiopodomys brandtii). Adult captive-bred female Brandt's voles (n = 124) (~50 g) in 31 cages with 4 individuals each were exposed to cool (23 ± 1°C) and cold (4 ± 1°C) ambient temperatures (Ta) and were allowed to huddle or were physically separated. The cold huddling (Cold-H) groups significantly reduced food intake by 29% and saved digestible energy 156.99 kJ/day compared with cold separated groups (Cold-S); in cool huddling groups (Cool-H) the reduction in food intake was 26% and digestible energy was saved by 105.19 kJ/day in comparison to the separated groups (Cool-S). Resting metabolic rate (RMR) of huddling groups was 35.7 and 37.2% lower than in separated groups at cold and cool Tas, respectively. Maximum non-shivering thermogenesis (NSTmax) of huddling voles was not affected by Ta, but in Cold-S voles it was significantly increased in comparison to Cool-S. Huddling groups decreased wet thermal conductance by 39% compared with separated groups in the cold, but not in the cool Ta. Unexpectedly, huddling voles significantly decreased Tb by 0.25 - 0.50°C at each Ta. Nevertheless, activity of Cold-H voles was higher than in Cold-S voles. Thus, huddling is energetically highly effective because of reduced metabolic rate, thermogenic capacity and relaxed Tb regulation despite the increase of activity. Therefore, Brandt's voles can remain active and maintain their body condition without increased energetic costs during cold exposure. This study highlights the ecological significance of huddling behavior for maintenance of individual fitness at low costs, and thus survival of population during severe winter in small mammals.

Huddling remodels gut microbiota to reduce energy requirements in a small mammal species during cold exposure.

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 ß-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.

Thermal biology of two sympatric gerbil species: The physiological basis of temporal partitioning.

Sympatric species can coexist through ecological resource partitioning as for example for habitat, food or time. However, a detailed understanding of the basic thermal physiology, crucial for temporal partitioning, is currently lacking, especially for the desert rodents. Here, we compare the physiological performance with regard to thermal energetics and morphological traits of two sympatric gerbils from the Gobi desert of Inner Mongolia, China. The diurnally active Meriones unguiculatus and the nocturnally active M. meridianus. The diurnal M. unguiculatus had more brown adipose tissue (BAT) mass and capacity for non-shivering thermogenesis (NST), a higher resting metabolic rate (RMR) at low ambient temperatures (Ta) and a higher upper critical temperature of the thermal neutral zone (TNZ) than the nocturnal M. meridianus. The overall thermal conductance and lower critical temperatures of M. unguiculatus were also higher than that of M. meridianus, permitting the former to maintain a stable body temperature (Tb) when exposed to high Ta. Laboratory-bred M. meridianus also showed higher daily water intake. We found no differences in body mass, and total evaporative water loss (TEWL) between the two species captured from the natural environment. These results suggest that the diurnal M. unguiculatus have a higher tolerance of high Tas, whereas M. meridianus can save more energy at low Tas. Therefore, from the view point of energy conservation, our results suggest that the nocturnal ecophenotype in M. meridianus is constrained by a lower ability for heat resistance, but this is not the case for the diurnal M. unguiculatus.

2-Deoxy-D-glucose, not mercaptoacetate, induces a reversible reduction of body temperature in male desert hamsters (Phodopus roborovskii).

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 23°C and 5°C. At Ta of 23°C, Tb, MR and RQ decreased in a dose-dependent manner with a large Tb-Ta differential (> 6.5°C) and a lowest Tb of 28.0°C which were comparable to those in fasted hamsters. At Ta of 5°C, 2DG-treated hamsters also decreased Tb to the same level as at Ta 23°C, but MR was significantly higher than that at Ta of 23°C at each dose, suggesting doses of 2DG directly affected the hypothalamic Tb set-point. Different from fasted hamsters which maintain normothermic at Ta of 5°C, 2DG-treated hamsters showed a substantial reduction of Tb at Ta 5°C, 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.

The effect of aggression I: The increases of metabolic cost and mobilization of fat reserves in male striped hamsters.

Aggression can benefit individuals by enhancing their dominance and thereby their ability to acquire and retain resources that increase survival or fitness. Engaging in aggressive behavior costs energy and how animals manage their energy budget to accommodate aggression remains unclear. We conducted three experiments to examine changes in physiological, behavioral and hormonal markers indicative of energy budget in male striped hamsters subject to resident-intruder aggression tests. Body temperature, metabolic rate and serum corticosterone levels significantly increased in resident hamsters immediately after the introduction of intruders. Energy intake did not change, but the metabolic rate of residents increased by 16.1% after 42-days of repeated encounters with intruders. Residents had significantly decreased body fat content and serum thyroxine (T4) levels, and a considerably elevated tri-iodothyronine (T3)/T4 ratio compared to a control group that had no intruders. Attack latency considerably shortened, and the number of attack bouts and total duration of attacks, significantly increased in residents on day 42 compared to day 1 of experiments. These findings may suggest that the conversion of T4 to T3 is involved in defensive aggression behavior. The mobilization of fat reserves resulting in lean body mass is probably common response to the increased metabolic cost of aggression in small mammals. Aggressive behavior, which is important for the successful acquisition and defense of resources, may be of significance for adaptation and evolution of metabolic rate.

The roles of metabolic thermogenesis in body fat regulation in striped hamsters fed high-fat diet at different temperatures.

The metabolic thermogenesis plays important roles in thermoregulation, and it may be also involved in body fat regulation. The thermogenesis of brown adipose tissue (BAT) is largely affected by ambient temperature, but it is unclear if the roles in body fat regulation are dependent on the temperature. In the present study, uncoupling protein 1 (ucp1)-based BAT thermogenesis, energy budget and body fat content were examined in the striped hamsters fed high fat diet (HF) at cold (5°C) and warm (30°C) temperatures. The effect of 2, 4-dinitrophenol (DNP), a chemical uncoupler, on body fat was also examined. The striped hamsters showed a notable increase in body fat following the HF feeding at 21°C. The increased body fat was markedly elevated at 30°C, but was significantly attenuated at 5°C compared to that at 21°C. The hamsters significantly increased energy intake at 5°C, but consumed less food at 30°C relative to those at 21°C. Metabolic thermogenesis, indicated by basal metabolic rate, UCP1 expression and/or serum triiodothyronine levels, significantly increased at 5°C, but decreased at 30°C compared to that at 21°C. A significant decrease in body fat content was observed in DNP-treated hamsters relative to the controls. These findings suggest that the roles of metabolic thermogenesis in body fat regulation largely depend on ambient temperature. The cold-induced enhancement of BAT thermogenesis may contribute the decreased body fat, resulting in a lean mass. Instead, the attenuation of BAT thermogenesis at the warm may result in notable obesity.

Limits to sustained energy intake XXV: milk energy output and thermogenesis in Swiss mice lactating at thermoneutrality.

Previous studies at 21 °C and 5 °C suggest that in Swiss mice sustained energy intake (SusEI) and reproductive performance are constrained by the mammary capacity to produce milk. We aimed to establish if this constraint also applied at higher ambient temperature (30 °C). Female Swiss mice lactating at 30 °C had lower asymptotic food intake and weaned lighter litters than those at 21 °C. Resting metabolic rate, daily energy expenditure, milk energy output and suckling time were all lower at 30 °C. In a second experiment we gave mice at 30 °C either 6 or 9 pups to raise. Female performance was independent of litter size, indicating that it is probably not controlled by pup demands. In a third experiment we exposed only the mother, or only the offspring to the elevated temperature. In this case the performance of the mother was only reduced when she was exposed, and not when her pups were exposed, showing that the high temperature directly constrains female performance. These data suggest that at 30 °C SusEI and reproductive performance are likely constrained by the capacity of females to dissipate body heat, and not indirectly via pup demands. Constraints seem to change with ambient temperature in this strain of mouse.

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

Daily torpor is frequently expressed in small rodents when facing energetically unfavorable ambient conditions. Desert hamsters (Phodopus roborovskii, ~20g) 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.

Effect of food restriction on energy budget in warm-acclimated striped hamsters.

The capacity of small mammals to sustain periods of food shortage largely depends on the adaptive regulation of energy budget in response to the decrease in food supply. In addition to food availability, ambient temperature (Ta) is an important factor affecting the rates of both energy intake and expenditure. To examine the effect of Ta on energy strategy and the capacity to sustain food shortage, striped hamsters were exposed to a warm condition (30°C) and were then restricted to 70% of ad libitum food intake. Body mass, energy intake and expenditure and physiological markers indicative of thermogenesis were measured. Warm exposure had no effect on body mass and digestibility, but decreased energy intake, basal metabolic rate and maximum nonshivering thermogenesis. The mitochondria protein content, cytochrome c oxidase activity and uncoupling protein 1 level of brown adipose tissue were significantly lower in hamsters at 30°C than at 21°C. Food restriction induced a significant decrease in body mass, but the decreased body mass was attenuated at 30°C relative to 21°C. This suggests that striped hamsters could not compensate for the limited food supply by decreasing daily energy expenditure at 21°C, whereas they could at 30°C. The significant reductions in the rates of metabolism and thermogenesis in warm-acclimated hamsters increase the capacity to cope with food shortage. Although, it remains uncertain whether this response represents some generalized evolutionary adaptation, the Ta-dependent adjustment in the capacity to survive food restriction may reflect that warm acclimation plays an important role in adaptive regulation of both physiology and behavior in response to the variations of food availability.

Environmental metabolomics reveal geographic variation in aerobic metabolism and metabolic substrates in Mongolian gerbils (Meriones unguiculatus).

Mongolian gerbils (Meriones unguiculatus) have a large-scale distribution in northern China. Geographic physiological variations which related to energy and water metabolism are critical to animals' local adaptation and distribution. However, the underlying biochemical mechanism of such variation and its role in adaptation remains largely unknown. We used GC-MS metabolomics approach to investigate the biochemical adaptation of Mongolian gerbils from xeric (desert), transition (desert steppe) and mesic (typical steppe) environments. Gerbils in desert population had lower resting metabolic rate (RMR) and total evaporative water loss (TEWL) than mesic population. Serum metabolomics revealed that concentrations of five tricarboxylic acid cycle intermediates (citrate, cis-aconitate, α-ketoglutarate, fumarate and malate) were lower in desert population than mesic population. Gastrocnemius metabolomics and citrate synthase activity analysis showed a lower concentration of citrate and lower citrate synthase activity in desert population. These findings suggest that desert dwelling gerbils decrease RMR and TEWL via down-regulation of aerobic respiration. Gastrocnemius metabolomics also revealed that there were higher concentrations of glucose and glycolytic intermediates, but lower concentrations of lipids, amino acids and urea in desert population than mesic population. This geographic variation in metabolic substrates may enhance metabolic water production per oxygen molecule for desert population while constraining aerobic respiration to reduce RMR and TEWL.

Seasonal changes of body mass and energy budget in striped hamsters: the role of leptin.

Proper adjustments of physiology and behavior are required for small mammals to cope with seasonal climate change. The aim of this study was to examine the role of leptin in the regulation of body mass and energy budget in striped hamsters. We first investigated seasonal changes in body mass, energy budget, and serum leptin levels in hamsters acclimated to outdoor natural daylight and ambient temperature. Then we assessed the effect of leptin administration on energy budget, serum lipoprotein lipase (LPL) and hepatic lipase (HL) activities, and gene expression of uncoupling protein 1 (UCP1) in brown adipose tissue and of hypothalamic neuropeptides associated with the regulation of energy balance in hamsters maintained at 21° and 5°C. Hamsters showed constant body mass throughout the four seasons but significantly increased food intake and thermogenesis in winter, compared to summer. Minimum body fat was observed in winter, and minimum serum leptin was found in autumn. Hamsters housed at 5°C showed higher energy intake, upregulated gene expression of UCP1 and hormone-sensitive lipase, and lower fat content and LPL and HL activity than the animals maintained at 21°C. Leptin administration had no effect on energy intake but increased maximal thermogenic capacity, as indicated by upregulated UCP1 gene expression at both 21° and 5°C. Body fat and activity of LPL and HL were decreased in hamsters treated with leptin. The results suggest that leptin plays an important role in the seasonal regulation of thermogenic capacity and body composition in striped hamsters. Leptin may be involved in increasing maximal thermogenesis in the cold rather than acting as a starvation signal to increase energy intake.

The shift of thermoneutral zone in striped hamster acclimated to different temperatures.

Temperature affects all biological functions and will therefore modulate ecologically significant interactions between animals and their environment. Here, we examined the effect of ambient temperature (Ta) on the thermal biology and energy budget in striped hamsters acclimated to cold (5°C), warm (21°C) and hot temperatures (31°C). Thermoneutral zone (TNZ) was 22.5-32.5°C, 25-32.5°C and 30-32.5°C in the cold-, warm- and hot-acclimated hamsters, respectively. The cold acclimation decreased the lower critical temperature and made the TNZ wider, and hot exposure elevated the lower critical temperature, resulting in a narrow TNZ. Within the TNZ, cold-acclimated hamsters showed a significantly higher rate of metabolism and thermogenesis than those acclimated to hot temperature. Digestive enzymes activities, including intestinal sucrase, maltase, L-alanine aminopeptidase-N and leucine aminopeptidase were higher in the cold than in the hot. The changes in metabolic rate and thermogenesis at different temperatures were in parallel with cytochrome c oxidase activity and uncoupling protein 1 gene expression of brown adipose tissue. This suggests that the shift of the lower critical temperature of TNZ is possibly associated with the rate of metabolism and thermogenesis, as well as with the digestive capacity of the gastrointestinal tract at different Ta. The upper critical temperature of TNZ may be independent of the changes in Ta. The changes of lower critical temperature of TNZ are an important strategy in adaption to variations of Ta.

Limits to sustained energy intake. XIX. A test of the heat dissipation limitation hypothesis in Mongolian gerbils (Meriones unguiculatus).

We evaluated factors limiting lactating Mongolian gerbils (Meriones unguiculatus) at three temperatures (10, 21 and 30°C). Energy intake and daily energy expenditure (DEE) increased with decreased ambient temperature. At peak lactation (day 14 of lactation), energy intake increased from 148.7±5.7 kJ day(-1) at 30°C to 213.1±8.2 kJ day(-1) at 21°C and 248.7±12.3 kJ day(-1) at 10°C. DEE increased from 105.1±4.0 kJ day(-1) at 30°C to 134.7±5.6 kJ day(-1) at 21°C and 179.5±8.4 kJ day(-1) at 10°C on days 14-16 of lactation. With nearly identical mean litter sizes, lactating gerbils at 30°C exported 32.0 kJ day(-1) less energy as milk at peak lactation than those allocated to 10 or 21°C, with no difference between the latter groups. On day 14 of lactation, the litter masses at 10 and 30°C were 12.2 and 9.3 g lower than those at 21°C, respectively. Lactating gerbils had higher thermal conductance of the fur and lower UCP-1 levels in brown adipose tissue than non-reproductive gerbils, independent of ambient temperature, suggesting that they were attempting to avoid heat stress. Thermal conductance of the fur was positively related to circulating prolactin levels. We implanted non-reproductive gerbils with mini-osmotic pumps that delivered either prolactin or saline. Prolactin did not influence thermal conductance of the fur, but did reduce physical activity and UCP-1 levels in brown adipose tissue. Transferring lactating gerbils from warm to hot conditions resulted in reduced milk production, consistent with the heat dissipation limit theory, but transferring them from warm to cold conditions did not elevate milk production, consistent with the peripheral limitation hypothesis, and placed constraints on pup growth.

Thermal physiology and energetics in male desert hamsters (Phodopus roborovskii) during cold acclimation.

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.

The energy budget, thermogenic capacity and behavior in Swiss mice exposed to a consecutive decrease in temperatures.

The limitation on sustainable energy intake (SusEI) is important because it establishes the upper energetic limit on the ability of animals to disperse, survive and reproduce. However, there are still arguments about what factors impose that limitation. Thermoregulation in cold environments imposes great energy demands on small mammals. A cold-exposed animal has been suggested to be a model suitable for testing these factors. Here, we examined the changes in food intake and digestible energy intake (DEI) as measures of SusEI, thermogenic capacity and behavioral patterns in Swiss mice exposed to consecutively lower ambient temperatures from 23 to -15°C. Cold-exposed mice showed significant decreases in body mass, fat content of the carcass and body temperature, and increases in DEI compared with controls. The time spent on feeding significantly increased with decreasing temperatures, and time spent on general activity decreased following cold exposure. Resting metabolic rate, nonshivering thermogenesis and serum tri-iodothyronine levels significantly increased in mice exposed to lower temperatures in comparison with controls, whereas these thermogenic variables were not significantly different between 0 and -15°C. It might suggest that SusEI in cold exposed Swiss mice was constrained peripherally by the capacity to produce heat and also by the ability to dissipate body heat, but to a different extent. Moderate cold exposure might result in a relaxation of the heat dissipation limit (HDL), allowing the animals to increase food intake to meet cold stress. When animals are exposed to severe cold, the thermogenenic capacity might reach a ceiling, failing to compensate for the heat loss and which would finally result in lower body temperature and considerable weight loss. This might indicate that the HDL was set at a higher level than peripheral limits for Swiss mice exposed to a consecutive decrease in ambient temperatures.