Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology
Thermogenic changes with chronic cold exposure in the naked mole-rat (Heterocephalus glaber)☆
Introduction
Non-shivering thermogenesis is commonly employed in response to acute cold stress in small mammals living in both tropical and temperate areas (Heldmaier, 1993, Haim et al., 1998, Li et al., 2001). However, adaptive changes in the capacity for non-shivering thermogenesis (NST) are critical for the survival of small mammals in temperate environments where pronounced seasonal differences in ambient temperature (Ta) prevail (Hayes, 1989, Heldmaier, 1993, Haim and Izhaki, 1993, Nespolo et al., 2001). Endogenous heat production via sympathetically mediated NST is enhanced in response to cold, thus compensating for increased heat loss to the environment (Williams, 1968, Hissa and Hirsimaki, 1971). Brown adipose tissue (BAT) is the major site for this sympathetic-induced NST response (Foster and Frydman, 1978, Foster and Frydman, 1979, Carneheim et al., 1984, Himms-Hagen, 1990). An acute cold stimulus increases thermogenesis in existing BAT, whilst chronic cold exposure markedly increases the capacity for NST via proliferation and neural recruitment of BAT (Himms-Hagen, 1990). As such the NST response of non-hibernating rodents following chronic cold exposure is commonly 1.5-fold greater than the maximal induced NST response prior to cold exposure (Wunder and Gettinger, 1996).
Naked mole-rats (Heterocephalus glaber) are hairless rodents, unable to effectively regulate body temperature (Tb), such that despite the employment of endogenous thermogenic mechanisms (e.g. NST and shivering) these mammals thermoconform to their environment (Buffenstein and Yahav, 1991, Hislop and Buffenstein, 1994). These atypical mammalian features reflect the evolutionary history and lifestyle of naked mole-rats; these animals live in large colonies in a thermally buffered underground habitat in tropical North East Africa (Lavocat, 1978, Jarvis, 1981, Brett, 1991, Buffenstein, 1996). In their natural milieu there is little need to be cold-tolerant and naked mole-rats are able to rely of ectothermic mechanisms (such as huddling and thigmothermy) to maintain a constant Tb. When these animals are housed in the laboratory under simulated burrow temperatures of 31–32 °C, and subjected to acute variations in Ta, metabolism increases by more than 50% over basal levels for every 1 °C drop in Ta below ‘apparent thermoneutrality’ (as Tb is never regulated) till approximately 29 °C (Buffenstein and Yahav, 1991). At this comparatively warm temperature rates of heat production relative to basal metabolic rate (BMR) are of similar magnitude to those exhibited by other cold-stressed laboratory rodents at an Ta of approximately 5 °C (Dicker et al., 1995, Hammond et al., 1996).
Naked mole-rats appear to be extremely sensitive to prolonged exposure to cooler conditions and respond with marked changes in thermoregulatory profiles (Woodley, 2000), thyroid hormone concentrations (Buffenstein et al., 2001), lung morphology (Maina et al., 2001) and reproductive function (Woodley, 2000). These animals react to prolonged cold exposure in a similar manner to that shown by most mammals: Food consumption is 1.4-fold greater and BMR is elevated (Woodley, 2000) suggesting that average daily energy expenditure is raised. Furthermore, these animals exhibit a ‘left shift’ in the metabolism/temperature rate curves, such that the lower critical temperature of the ‘apparent thermoneutral zone’ (TNZ) is decreased; the TNZ is extended from 31–34 to 27–34 °C, and the slope of RMR/Ta is reduced (Woodley, 2000). These features minimize energy expenditure under cold conditions (Cossins and Bowler, 1987). Peak metabolism in that study (Woodley, 2000) was of a similar magnitude to that previously noted under various conditions (Buffenstein and Yahav, 1991, Hislop and Buffenstein, 1994, Urison and Buffenstein, 1995), implying that maximal metabolic rate was unchanged, and that naked mole-rats may not be able to (or might not choose to) adjust their endothermic capacity and thus may be unresponsive to chronic cold conditions. We investigated whether or not, these animals respond to prolonged cold-stress by increasing BAT thermogenic capacity by monitoring changes in oxygen consumption (Vo2) and Tb following noradrenaline (NA) intervention.
Section snippets
Animal care and maintenance
All animals used in this study were born in captivity from progenitors collected in Kenya (0°38′N/37°40′E) in 1980. They were housed in pairs in standard laboratory rat cages in which lengths of perspex tubing were provided for burrows. Nesting material included sawdust and shredded paper. Animals were housed under continuous dim incandescent lighting as previously described by Jarvis (1991). Animals were fed an ad libitum diet of chopped fresh fruit and vegetables as well as a high energy,
Results
Cold-acclimated animals had higher (P<0.01) baseline Vo2 measurements, however, NA-induced Vo2 values were similar (P>0.05) to that of control naked mole-rats (Fig. 1). Regardless of housing Ta, NA intervention induced significant increases in Vo2 (P<0.001; Fig. 1). Furthermore, the housing Ta did not affect either the maximal Vo2 of NST or the resultant increase in Tb (Fig. 1 and Fig. 2). There was no significant difference (P>0.05) in Vo2 following saline intervention in either group (Fig. 1).
Discussion
Chronic cold exposure did not increase NST capacity in the naked mole-rat. This is contrary to the findings for most small mammals, where cold exposure induces BAT hyperplasia (Bukowiecki et al., 1982) and concomitant increases in NST capacity (e.g. Foster and Frydman, 1978, Foster and Frydman, 1979, Heldmaier and Buchberger, 1985, Rafael et al., 1986, Wunder and Gettinger, 1996). Since baseline metabolic rates were greater in the cold-acclimated animals, the percent increase in Vo2 above
Acknowledgements
We thank the staff of the Central Animal Service of the University of the Witwatersrand, especially Mr Wilson Chai for his expert care of the animals. We also thank Shane Maloney, Duncan Mitchell and Craig Hartford for useful discussion during this study. This work was funded by an FRD grant to RB.
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This paper was originally presented at ‘Chobe 2001’; The Second International Conference of Comparative Physiology and Biochemistry in Africa, Chobe National Park, Botswana – August 18–24, 2001. Hosted by the Chobe Safari Lodge and the Mowana Safari Lodge, Kasane; and organised by Natural Events Congress Organizing ([email protected]).