CC BY
55
Journal of Stress Physiology & Biochemistry, Vol. 8 No. 4 2012, pp. 36-46 ISSN 1997-0838 Original Text Copyright © 2012 by Zhu, Wang
ORIGINAL ARTICLE
Seasonal variations of thermoregulatory and thermogenic properties in Eothenomys miletus and Apodemus chevrieri
Zhu Wan-long, Wang Zheng-kun*
School of life Science of Yunnan Normal University, 650092, China
*Telephone No.: +86 0871 5516068 *E-Mail: zwl [email protected]
Received June 30, 2012
Eothenomys miletus and Apodemus chevrieri are typical species of small mammals inhabiting in Hengduan mountains region. The characteristics of thermoregulation and thermogenesis of two mammals were measured to search their physiological and ecological characteristics of adaptations to this region in different seasons. All results indicated: the body weight of E. miletus and A. chevrieri in summer was separately 47.29±0.73g, 32.74±0.54g, and their body weight in winter was separately 39.28±0.61g, 31.70±0.76g; the thermal neutral zones(TNZ) of E. miletus and A. chevrieri in summer were separately 25~32.5 oC and 25~30 oC, and their TNZ in winter were all of 22.5 ~ 27.5oC; their basal metabolic rates(BMR) in summer were respectively 3.76± 0.07ml O2/g.h, 4.58±0.09mlO2/g.h, and their BMR in winter were respectively 4.46±0.04mlO2/g.h, 5.23±0.01mlO2/g.h; their maximum nonoshivering
thermogenesis(NST) in summer was respectively 5.70±0.18mlO2/g.h, 7.12±0.31mlO2/g.h, and their NST in winter was respectively 6.67±0.05mlO2/g.h, 7.42±0.04mlO2/g.h; their NST scope(NST/BMR) in summer was separately 1.52±0.05, 1.46±0.04, and their NST scope in winter was separately 1.49±0.01, 1.42±0.01. Their thermogenic characteristics and
thermoregulatory styles possibly reflected features of small rodents in Hengduan mountains region which have lower body temperatures and NST scope, higher BMR, Cm and NST and could keep their body temperatures stable in narrower ambient temperatures comparing with other rodents. Body temperature, Cm BMR and NST of A. chevrieri were higher than these of E. miletus. A. chevrieri could keep body temperature stable in a wider range of ambient temperatures than E. miletus. NST scope of E. miletus was higher than it of A. chevrieri. Their TNZ and the ambient temperature range in which they could keep C stable in winter were narrower than these indexes in summer. The body temperature and body weight in winter were lower comparing with the summer. The BMR, F-value and NSTmax in winter were significantly higher than the summer. The TNZ in winter was shifted to the lower ambient temperature comparing with the summer.
Key words: Eothenomys miletus; Apodemus chevrieri; Thermoregulation; Thermogenesis
ORIGINAL ARTICLE
Seasonal variations of thermoregulatory and thermogenic properties in Eothenomys miletus and Apodemus chevrieri
Zhu Wan-long, Wang Zheng-kun*
School of life Science of Yunnan Normal University, 650092, China
*Telephone No.: +86 0871 5516068 *E-Mail: zwl [email protected]
Received June 30, 2012
Eothenomys miletus and Apodemus chevrieri are typical species of small mammals inhabiting in Hengduan mountains region. The characteristics of thermoregulation and thermogenesis of two mammals were measured to search their physiological and ecological characteristics of adaptations to this region in different seasons. All results indicated: the body weight of E. miletus and A. chevrieri in summer was separately 47.29±0.73g, 32.74±0.54g, and their body weight in winter was separately 39.28±0.61g, 31.70±0.76g; the thermal neutral zones(TNZ) of E. miletus and A. chevrieri in summer were separately 25 ~32.5 °C and 25 ~ 30 °C, and their TNZ in winter were all of 22.5 ~ 27.5°C; their basal metabolic rates(BMR) in summer were respectively 3.76± 0.07ml 02/g.h, 4.58±0.09ml02/g.h, and their BMR in winter were respectively 4.46±0.04ml02/g.h, 5.23±0.01ml02/g.h; their maximum nonoshivering thermogenesis(NST) in summer was respectively 5.70±0.18ml02/g.h, 7.12±0.31ml02/g.h, and their NST in winter was respectively 6.67±0.05ml02/g.h, 7.42±0.04ml02/g.h; their NST scope(NST/BMR) in summer was separately 1.52±0.05,1.46±0.04, and their NST scope in winter was separately 1.49±0.01, 1.42±0.01. Their thermogenic characteristics and thermoregulatory styles possibly reflected features of small rodents in Hengduan mountains region which have lower body temperatures and NST scope, higher BMR, Cm and NST and could keep their body temperatures stable in narrower ambient temperatures comparing with other rodents. Body temperature, Cm BMR and NST of A. chevrieri were higher than these of E. miletus. A. chevrieri could keep body temperature stable in a wider range of ambient temperatures than E. miletus. NST scope of E. miletus was higher than it of A. chevrieri. Their TNZ and the ambient temperature range in which they could keep C stable in winter were narrower than these indexes in summer. The body temperature and body weight in winter were lower comparing with the summer. The BMR, F-value and NSTmax in winter were significantly higher than the summer. The TNZ in winter was shifted to the lower ambient temperature comparing with the summer.
Key words: Eothenomys miletus; Apodemus chevrieri; Thermoregulation; Thermogenesis
Thermoregulation and thermogenesis physical ability, indicated the relationship between
characteristics of small mammals were closely environment and biodiversity (Tomasi and Horton,
related with energy utilization, distribution, life 1992). Small mammals tend to use a variety of
history strategy and its evolution, reflected the physiological and behavioral mechanisms to
adaptation to the environment model and the regulate body temperature, body temperature
regulation is the animal to maintain the body temperature in certain range process by physical (behavior) or physiological way (Ge, 2002). Heat regulation characteristics of small mammals were significant influenced by ecological or behavioral characteristics, and profoundly affects the animal energy distribution and its evolutionary path (Tomasi and Horton, 1992).
Thermoregulation and thermogenesis characteristics of small mammals in different seasons were different, these differences were mainly in body mass, body temperature, BMR, the appearance of these differences is the main cause of the animal stress with low temperature, stress caused by the different food in different seasons. It showed that body mass of small mammals in the winter can be reduced up to 50% (Lovegrov, 2003). The northern three-toed jerboa studies had shown the seasonal temperature from spring to fall gradually reduced, the spring animal resting metabolic rate minimum (Bao et al., 2000). Small mammals, especially rodents, the BMR affected by seasons, some mammals showed high BMR in winter than that in summer, such as Sylvilagus audubonii, Lepus californicus, Lepus townsendi (Degen, 1997). Adaptation of Animal to cold environmental were always used by changes in basal metabolic rate, reduce the heat conduction and increased fur thickness, another way is nonshivering thermogenesis (NST). Nonshivering thermogenesis is constant in animal muscle activity and increased heat production under cold exposure, small mammals using the mechanism is NST, shivering thermogenesis is only in extreme cold as an auxiliary heat source. When body mass was more than 3kg, the importance of NST is very small, but in small mammals, especially less than 200g of the body mass, NST is much more
important than shivering thermogenesis (Heldmaier et al., 1990).
Hengduan Mountains region is located the boundary between the Palaearctic region and the Oriental region, is the proper alp and gorge region; has abundant mammals, is been considered "the harbor in fourth ice age" (Wu and Wang, 1985). Small mammals' may show a different physiological and ecological character since the geographical diversity and climate diversity in Hengduan Mountains region. E. miletus is the inherent species in Hengduan mountains region, has special status in Microtus. It is also the host of rat epidemic disease of Yunnan province, who distributed in Jianchuan, Heqin, Baoshang et al of Yunnan province. Apodemus chevrieri is the inherent species in Hengduan mountains region (Zheng, 1993). Here we measure seasonal changes in thermogenesis including body mass, BMR, NST from E. miletus and A. chevrieri. We hypothesize that, similar to other small mammals, E. miletus and A. chevrieri will change their thermogenesis seasonally. We predict that E. miletus and A. chevrieri will show a decrease in BM and increase in thermogenesis in the cold season.
MATERIALS AND METHODS
Samples
E. miletus and A. chevrieri were captured in farmland (26°15'-26°45'N; 99°40-99°55E; altitude 2,590m) in Jianchuan County, Yunnan province, 2011. Mean yearly temperature was 9.1°C; mean monthly temperature ranges form -4.0°C in January to 24.1°C in July.
A total of 152 included summer (June 2011) (n=80) and winter (December 2011) (n=72) of E. miletus, a total of 151 included summer (June 2011) (n=79) and winter (December 2011) (n=72) of A.
chevrieri. Between capture and metabolic analysis, the animals were kept individually in plastic cages (350x300x250mm3) in a room with natural temperature and photoperiod, summer (23.9 oC), winter (-3.8 oC). Food and water were provided ad libitum. All pregnant, lactating or young individuals were excluded.
Measurement of metabolic rates
Metabolic rates were measured by using AD ML870 open respirometer (AD Instruments, Australia) at 25oC within the TNZ (thermal neutral zone), gas analysis were using ML206 gas analysis instrument, the temperature was controlled by SPX-300 artificial climatic engine (±0.5oC), the metabolic chamber volume is 500ml, flow is 200 ml/min. Animals were stabilized in the metabolic chamber for at least 60 min prior to the BMR measurement, oxygen consumption was recorded for more than 60-min at 5-min intervals. Two stable consecutive lowest readings were taken to calculate BMR. Calculate method of metabolic rate is detailed by Hills (Hill 1972).
Nonshivering thermogenesis (NST) was induced by subcutaneous injection of norepinephrine (NE) (Shanghai Harvest Pharmaceutical Co. Ltd) and measured at 25 oC. Two consecutive highest recordings of oxygen consumption more than 60 min at each measurement were taken to calculate the NST (Heldmaier, 1971). The doses of NE were approximately 0.8-1.0 mg/kg according to dose-dependent response curves that were carried out before the experiment.
Thermal conductance(C) and F value
Thermal conductance was evaluated as C=RMR/ (Tb-Ta) (McNab, 1980). In this equation, RMR is the basal metabolic rate (ml 02/g.h), Tb is the body temperature (oC), Ta is the environment
temperature(oC) » F value can be calculated as F=(BMR/Kleiber predicted BMR)/ (C/Bradly predicted C) (McNab,1970). In this equation, predicted BMR was Kleiber's (1961) body mass predicted value; predicted C was Bradly's(1980)body mass predicted value.
Statistical analysis
Data were analyzed using SPSS 15.0 software package. Prior to all statistical analyses, data were examined for assumptions of normality and homogeneity of variance, using Kolmogorov-Smirnov and Levene tests, respectively, including analysis of covariance(ANC0VA), repeat metrical regression and independent t test. Results are reported as mean ± standard deviation for each species. Predicted BMR was Kleiber's (1961) body mass predicted value; predicted C were Herried (1967) and Bradly's (1980) body mass predicted value. Results were presented as mean ± SEM, and P < 0.05 was considered to be statistically significant.
RESULTS
Body mass
Body mass in E. miletus was 47.29±0.73g (n=80) in summer, was 39.28±0.61g (n=72) in winter, showed significant difference between different seasons (t=8.734, P<0.01), body mass in summer was 22.47% higher than that in Winter. Body mass in A. chevrieri was 32.74±0.54g (n=79) in summer, was 31.70±0.76g (n=72) in winter, showed
significant difference between different seasons (t=1.012, P>0.05), body mass in summer was 8.58% higher than that in Winter (Table 1).
BMR
The relation between BMR and Ta (5 oC ~35 oC) of E. miletus in summer is represented by the following equation: BMR =7.643-0.118Ta (r=-0.821,
P<0.01). Using W073 rectification, the relation is: BMR =21.548- 0.334 Ta (r=-0.825, P<0.01). The relation between BMR and Ta (5 °C ~35 °C) of A. chevrieri in summer is represented by the following equation: BMR =8.167-0.106Ta (r= -0.824, P<0.01). Using W073 rectification, the relation is: BMR =20.965-0.276Ta (r=-0.869, P<0.01) (Fig 1).
Using analysis of repeat metrical regression, when Ta between 25 °C and 32.5 °C, BMR in E. miletus were not significant correlation (P>0.05) in summer, so the thermal neutral zone (TNZ) was 25 oC and 32.5 oC. In the TNZ, BMR of E. miletus was 3.76± 0.07ml 02/g.h. In the TNZ, by the ANC0VA, BMR of E. miletus and body mass showed significant correlation: BMR=20.4181W-0'446 (r=-0.613,P<0.01). Using analysis of repeat metrical regression, when Ta between 25 oC and 30 oC, BMR in A. chevrieri were not significant correlation (P>0.05) in summer, so the thermal neutral zone (TNZ) was 25 oC and 30 oC. In the TNZ, BMR of A. chevrieri was 4.58±0.09 ml02/g.h. In the TNZ, by the ANC0VA, BMR of A. chevrieri and body mass showed significant correlation: BMR=33.0554W-0'5703 (r=-0.767,P<0.01).
The relation between BMR and Ta(5 oC ~35 oC) of E. miletus in winter is represented by the following equation: BMR=8.497-0.106Ta (r=-0.884, P<0.01). Using W073 rectification, the relation is: BMR=21.016 - 0.267Ta (r=-0.736, P<0.01). The relation between BMR and Ta (5 oC ~35 oC) of A. chevrieri in winter is represented by the following equation: BMR=8.497-0.106Ta (r=-0.884, P<0.01). Using W073 rectification, the relation is: BMR=22.075-0.293Ta (r=-0.828, P<0.01).
Using analysis of repeat metrical regression, when Ta between 22.5 oC and 27.5 oC, BMR in E. miletus were not significant correlation (P>0.05) in winter, so the thermal neutral zone (TNZ) was 22.5
oC and 27.5 oC. In the TNZ, BMR of E. miletus was 4.46±0.04 ml02/g.h о In the TNZ, by the ANC0VA, BMR of E. miletus and body mass showed significant correlation: BMR=1.046W0389 (r=0.935, P<0.01). Using analysis of repeat metrical regression, when Ta between 22.5 oC and 27.5 oC, BMR in A. chevrieri were not significant correlation (P>0.05) in winter, so the thermal neutral zone (TNZ) was 22.5 oC and 27.5 oC. In the TNZ, BMR of A. chevrieri was 5.23±0.01 ml02/g.h о In the TNZ, by the ANC0VA, BMR of A. chevrieri and body mass showed significant correlation: BMR=4.677W0 034 (R=0.932, P<0.01).
BMR showed significant difference between different seasons in E. miletus (t=6.701, P<0.01), it also showed significant difference between different seasons in A. chevrieri (t=6.337, P<0.01). NST
NST of E. miletus was 5.70±0.18ml 02/g .h in 25 oC in summer , was Heldmaier's body mass predicted value's 112.31±2.54%. NST of A. chevrieri was 7.12±0.31 ml 02/g .h in 25 oC in summer, was Heldmaier's body mass predicted value's 118.29±3.55%. NST of E. miletus was 6.67±0.05 ml 02/g .h in 25 oC in winter, was Heldmaier's body mass predicted value's 127.44±1.35%. NST of A. chevrieri was 7.42±0.04 ml 02/g.h in 25 oC in summer , was Heldmaier's body mass predicted value's 107.29±2.75% (Table 1).
NST showed significant difference between different seasons in E. miletus (t=-4.878, P<0.01), it also showed significant difference between different seasons in A. chevrieri (t=-4.441, P<0.01). The value of NSTmax/BMR were 1.52±0.05 and 1.46±0.04 for E. miletus and A. chevrieri in summer, and were 1.49±0.01 and 1.42±0.01 in winter, respectively.
Thermal conductance(C) and F value
Down the TNZ, thermal conductance of E. miletus and Ta show ed no significant correlation in summer, average value was 0.28±0.005 ml 02/g.h. oC, was Herried's body mass predicted value's 191.13±2.60%, was Bradly's body mass predicted value's 196.44±2.59%. Up the 30 oC , thermal conductance increased when the environment temperature ascended , the relation between the thermal conductance of E. miletus and Ta was: C=0.2226+0.0053Ta (r=0.822, P<0.01) (Fig 2). Down the TNZ, thermal conductance of A. chevrieri and Ta showed no significant correlation in summer, average value was 0.32±0.009 02/g.h. oC, was Herried's body mass predicted value's 186.85±5.06%, was Bradly's body mass predicted value's 186.58±5.09%. Up the 30 oC, thermal conductance increased when the environment temperature ascended , the relation between the thermal conductance of A. chevrieri and Ta was: C=0.2125+0.0086Ta (R=0.881, P<0.01) (Fig 2). In the TNZ, F value of E. miletus in summer was 0.88±0.05. In 5 oC and 35 oC, F value of E. miletus declined when the environment temperature ascended, they showed significant correlation: F=3.745-0.099Ta (r=-0.997, P<0.01); In the TNZ, F value of A. chevrieri in summer was 1.10±0.05. In 5 oC and 35 oC, F value of A. chevrieri declined when the environment temperature ascended, they showed significant correlation: F=4.085- 0.108Ta (r= 0.991, P<0.01) (Table 1).
Down the TNZ, thermal conductance of E. miletus and Ta show ed no significant correlation in winter, average value was 0.31±0.005 ml 02/g.h. oC, was Herried's body mass predicted value's 186.85±3.07%, was Bradly's body mass predicted value's187.89±3.27%. Up the 27.5 oC , thermal conductance increased when the environment temperature ascended, the relation between the thermal conductance of E. miletus and Ta was: C=0.039Ta-0.201 (r=0.787, P<0.01) (Fig 2). Down the TNZ, thermal conductance of A. chevrieri and Ta showed no significant correlation in winter, average value was 0.32±0.005 02/g.h. oC, was Herried's body mass predicted value's 189.25±3.94%, was Bradly's body mass predicted value's 189.36±4.42%. Up the 30 oC, thermal conductance increased when the environment temperature ascended , the relation between the thermal conductance of A. chevrieri and Ta was: C=0.026Ta-0.001 (r=0.866, P<0.01) (Fig 2). In the TNZ, F value of E. miletus in winter was 1.03± 0.05. In 5 oC and 35 oC, F value of E. miletus declined when the environment temperature ascended, they showed significant correlation: F=3.853-0.108Ta (r=0.987, P<0.01); In the TNZ, F value of A. chevrieri in winter was 1.10±0.05. In 5 oC and 35 oC, F value of A. chevrieri declined when the environment temperature ascended, they showed significant correlation: F=3.922-0.1Ta (r=0.974,
P<0.01).
Table 1 Effects of the body mass, seasons thermogenic abilities in E. miletus and A. chevrieri in different
Summer Winter P value
E. miletus
Body mass (g) 47.29±0.73 39.28±0.61 <0.01
BMR (ml 02/g.h) 3.76± 0.07 4.46±0.04 <0.01
NST (ml 02/g.h) 5.70±0.18 6.67±0.05 <0.01
Thermal conductance(C) 0.28±0.005 0.31±0.005 >0.05
F value 0.88±0.05 1.03± 0.05 >0.05
Apodemus chevrieri
Body mass (g) 32.74±0.54 31.70±0.76 >0.05
BMR (ml 02/g.h) 4.58±0.09 5.23±0.01 <0.01
NST (ml 02/g.h) 7.12±0.31 7.42±0.04 <0.01
Thermal conductance(C) 0.32±0.009 0.32±0.005 >0.05
F value 1.10±0.05 1.26±0.05 <0.05
Figure 1: The relationship between basal metabolic rate and ambient temperatures in E. miletus and A. chevrieri in different seasons
Figure 2: The relationship between thermal conductance and ambient temperatures in E. miletus and A. chevrieri in different seasons
DISCUSSION
Body mass
Ambient temperature plays an important role in animals' physiology and behaviors. It has been demonstrated that many small mammals, such as Phodopus sungorus, Sorex, respond to winter-associated environmental cues by reducing body mass (Genoud, 1988; Zhan and Wang, 2004; Liu et al., 2003). Our present results showed that cold temperature is an important environmental cue that can influence E. miletus and A. chevrieri to reduce their body mass significantly. Body mass decline in winter conditions is considered to be an adaptive mechanism for the reduction of absolute energy requirements when stress occurs (Heldmaier et al., 1986; Downs, 1985; Wunder, 1985).
BMR and NST
BMR of mammals associate with the selective factors, such as climate, habitat (Rezende et al.,2004). Generally speaking, BMR of mammals in
torrid zone are lower than them in temperature zone, and BMR of mammals in temperature zone are lower than them in frigid zone. Animals live in frigid zone, especially in polar region, most animals have higher BMR (Koteja and Weiner, 1993). BMR in E. miletus and A. chevrieri were higher compare with some small mammals, BMR of two species in summer were Kleiber's body mass predicted value's 287.36±4.32%, 320.49±4.96%, respectively. They are higher than some rodents lived in low altitude in north region, Microtus pennsylvanicus(141%), M.ochrogaster (129%), M.richardson (131%), M.breweri (110.4%) (Kurta and Ferkin, 1991), also higher than M. oeconomus (214%) which live in alpine region(Wang and Wang, 2000). All of these may cope with their adaptation characteristics of two species: although two species habitat's latitude are lower than some species live in north region, but their habitat's altitude are close, along with the increase of altitude, manace of low temperature
gradually increase, it is equal to increased the latitude (Wang et al., 1994 ) , so two species have higher BMR levels. Furthermore, because of the daily difference in temperature are greater in Hengduan mountains region, two species suffer high temperature and low temperature every day, and the ability of their non-shivering thermogenesis (NST) are relatively lower, it lead to adopt high metabolic rate to fit the menace of low temperature. In addition, the habitat of two species has no snow cover in winter and abundant food resource, so these also provide some conditions for them to adopt higher energy strategy (McNab, 1986).
The variations in body mass were associated with changes in energy intake and expenditure. It is evident that many winter-active small mammals enhance NST for survival in the cold or winter (Heldmaier et al. 1986; Jansky, 1973). In present study, NST of E. miletus and A. chevrieri showed seasonal plasticity, E. miletus and A. chevrieri in the wild increased NST in cold seasons; it was also similar to other small mammals living in cold regions (Bao et al., 2001; Li et al., 1994; Haim and Izbaki, 1993). These results supported the hot disappearing limit hypothesis; animals increased heat production in winter, heat loss was increased, energy intake has also increased, animals decreased heat production in summer, heat loss was restricted, energy intake has also limited.
Thermal conductance(C) and F value
Thermal conductance of two species maintain invariability between 5 oC and 25 oC, higher than typical species of north region obviously, are close to the level of species live in torrid zone, such as Tupaia belangeri (199.9%) (Wang et al., 1994). 0ne hand, it is relate to theirs behaviors; another hand, it is connect with the difference in temperature of
theirs habitat. Because of particular geography and climate in Hengduan mountains region, two species endure more menace of low temperature, tolerance of hot temperature were feeble, so it appeared excessive hot temperature and thermal conductance increase when the environment temperature was low (Wang et al., 2006). F value is show the ability of thermoregulation (Gordon, 1993), can be weight the relatively ability of energy metabolism of mammals in different temperatures. F value in E. miletus and A. chevrieri were lower than rats live in north region, such as Microtus pennsylvanicus, M.ochrogaster, M.richardson, but higher than species live in torrid zone (Kurta and Ferkin, 1991; Wang et al., 1999). All of these illuminate that ability of maintain body temperature invariableness of two species were finite.
In conclusion, thermogenic characteristics and thermoregulatory styles in E. miletus and A. chevrieri possibly reflected features of small rodents in Hengduan mountains region which have lower body temperatures and NST scope, higher BMR, Cm and NSTmax and could keep their body temperatures stable in narrower ambient temperatures comparing with other rodents. Body temperature, Cm BMR and NSTmax of A. chevrieri were higher than these of E. miletus. A. chevrieri could keep body temperature stable in a wider range of ambient temperatures than E. miletus. NST scope of E. miletus was higher than it of A. chevrieri. Their TNZ and the ambient temperature range in which they could keep C stable in winter were narrower than these indexes in summer. The body temperature and body weight in winter were lower comparing with the summer. The BMR, F-value and NSTmax in winter were significantly higher than the summer. The TNZ in winter was shifted to
the lower ambient temperature comparing with the
summer.
ACKNOWLEDGMENTS
This research was financially supported by
National Science Foundation of China (No.
31260097), Project of Basic research for application
in Yunnan Province (2011FZ082).
REFRENCES
Ashoff, J. (1981) Thermal conductance in mammals and birds: Its dependence on body size and circadian phase. Comp. Biochem. Physiol., 69A: 611-619.
Bao, W.D., Wang, D.H., Wang, Z.W. (2000) Seasonal changes of the resting metabolic rate in the northern three Toed Jerboa(Dipus Sagitta) in kubuqi desert, Ordos plateau. Acta Zoologica Sinica, 46: 146-153.
Bao, W.D., Wang, D.H., Wang, Z.W. (2001) Seasonal changes of non-shivering thermogenesis in fore rodents from kubuqi desert of Inner Mongolia. Acta Theriologica Sinica. 21(1): 101 -106.
Bradly, S.R., Deavers, D.R. (1980) A re-examination of the relationship between thermal conductance and body weight in mammals. Comp Biochem Physiol, 65A: 465-476.
Degen, A.A. (1997) Ecophysiology of small desert mammals. Berlin: Springer-Verlag, 163-263.
Downs, C.T., Perrin, M.R. (1995) The thermal biology of white-tailed rat Mystromys albicaudatus, a cricetine relic in southern temperature African grassland. Comp Biochem Physiol, 110A(1): 65-69.
Ge F. (2002) Modern ecology. Science Press, Beijing.
Genoud, M. (1988) Energetic strategies of shrews:ecological constraints and evolutionary
implications. Mammal. Rev. 18(4): 173-193.
Gordon, C.J. (1993) Temperature regulation in laboratory rodents. Cambridge University Press: 1-276.
Haim, A., Izbaki, H. (1993) The ecological significance of resting metabolic rate and nonshivering thermogenesis for rodents. J Therm Biol, 18(2): 71-91.
Heldmaier, G. (1971) Zitterfreie warmebidung und korpergrosse bei sagetieren. Z. Vergl. Physiol., 73: 222-248.
Heldmaier, G., Boeckler, H., Buchberger, A. (1986) Seasonal variation of thermogenesis. In: Edited by B C Heller et al., Living in the Cold: Physiological and Biochemstrial Adaptations. Elsevier Science Publishing Co., Inc. pp.361-372.
Heldmaier, G., Klaus, S., Wiesenberg, R. (1990) Seasonal adaptation of thermoregulatory heat production in small mammals. In: Bligh J., Voigt Keds. Thermoreceptor and Temperature Regulation. Berlin Springer Press, 235-243.
Hill, R.W. (1972) Determination of oxygen consumption by use of the paramagnetic oxygen analyzer. J Applied Physiology. 33(2): 261-263
Jansky, L. (1973) Nonshivering thermogenesis and its thermoregulatory significance. Biol. Rev., 48: 85-132.
Kleiber, M. (1961) The Fire of Life. New York, Wiley: 1-454.
Koteja, P., Weiner, J. (1993) Mice, voles and hamsters: metabolic rates and adaptive
strategies in muroid rodents. Oikos 66: 505514.
Kurta, A., Ferkin, M. (1991) The correlation of
demography and metabolic rate: a test using the vole (Microtus breweri) and the meadow vole (Microtus pennsylvanicus). Oecologia, 87: 102-105.
Li, Q.F., Li, N., Sun, R.Y. (1994) The adaptive thermogenesis of Brandt's Voles(Microtus brandti) during cold exposure. Acta Theriologica Sinica. 14(4): 286-293.
Liu, J.S., Wang, D.H., Sun, R.Y. (2003) Metabolism and thermoregulation in striped hamsters(Cricetulus barabensis) from the Northeast of China. Acta Zoologica Sinica, 49(4): 451-457.
Lovegrove, B.G. (2003) The influence of climate on the basal metabolic rate of small mammals: a slow-fast metabolic continuum. J. Comp. Physiol. 173B: 87-112.
McNab, B.K. (1970) Body weight and the energetics of temperature regulation. J. Biol., 53: 329348.
McNab, B.K. (1986) The influence of food habits on energetics of eutherian mammals. Ecological Monographs, 56(1): 1-19.
Renzende, E.L., Bozinovic, F., Garland T. Jr. (2004) Climatic adaptation and the evolution of basal and maximum rates of metabolism in rodents. Evolution, 58(6): 1361-1374.
Tomasi, T.E, Horton, T.H. (1992) Mammalian Energetics: Interdisciplinary views of
metabolism and reproduction. Ithaca and
London: Comdtock Publishing Associates, 1276.
Wu, Z.Y., Wang, H.S. (1985) Physical Geography of China-Plant Geography[M]. Beijing: Science press
Wang, Z.K., Liu, L., Liang, Z.Q. (1999) Thermogenic characteristics and body temperature regulation in the oriental voles(Eothenmys miletus). Acta Theriologica Sinica. 19(4): 276286.
Wang, D.H., Wang, Z.W. (2000) Body temperature regulation and evaporative water loss in Root Vole(Microtus oeconomus). Acta Theriologica Sinica, 20(1): 37-47.
Wang, Z.K., Sun, R.Y., Li, Q.F. (1994) Characteristics of the resting metabolic rate of tree shrew, Tupaia belangeri. Journal of the Beijing Normal University, 30(3): 408-414.
Wunder, B.A. (1985) Energetics and thermoregulation In: Tamarin R H ed. Biology of New World Microtus: 812-843.
Zhan, X.M., Wang, D.H. (2004) Energy metabolism and thermoregulation of the desert Hamster(Phodopus roborovskii) in Hunshandake desert of Inner Mongolia, China. Acta Theriologica Sinica, 24(2): 152-159.
Zheng, S.H. (1993) Rodentine fossil in quaternary period in Sichuan and Guizhou. Beijing: Science press.
