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Is the naked mole-rat Hererocephalus glaber an endothermic yet poikilothermic mammal?
J. therm.Biol. Vol. 16, No. 4, pp. 227-232, 1991 Printed in Great Britain.All rights reserved
0306-4565/91 $3.00+ 0.00 Copyright© 1991 PergamonPress plc
IS THE N A K E D MOLE-RAT H E T E R O C E P H A L U S GLABER A N E N D O T H E R M I C YET POIKILOTHERMIC M A M M A L ? ROCHELLE BUFFENSTEINand SHLOMOYAHAV Department of Physiology, Medical School, University of Witwatersrand, 7 York Road, Parktown 2193, Johannesburg, South Africa
(Received 25 August 1990; accepted in revisedform 19 January 1991)
Abstract--1. Thermoregulatory changes with ambient temperature (Ta) were monitored in Heterocephalus glaber between 12 and 37°C. 2. At all Tas monitored, body temperature (Tb) was directly proportional to T~ (Tb = 0.568 + 1.016 T~). 3. Below T~ 29°C, 1?O2 varied in a typically poikilothermic pattern, whereas above 29°C, I702 followed a typically endothermic pattern. 4. At T~s between 31 and 34°C, 1702was minimal (1.00 _+0.09 ml/g/h), skin temperature was 1.8 _+0.6°C lower than Tb and evaporative water loss accounted for 173.7 _ 51.0% of the metabolic heat produced. 5. The high rates of heat transfer are such that individual naked mole-rats cannot regulate Tb over the entire range of measured /'as and, as such, are poikilothermic mammals. Key Word Index: Poikilothermic mammal; endothermy; skin temperature; high evaporative water loss; body temperature
INTRODUCTION
The naked mole-rat, Heterocephalus glaber is a strictly subterranean (chthonic) mammal found only in the tropical semi-arid zones of north east Africa (De Graaff, 1981). Here, it lives in the extensive maze of poorly ventilated plugged burrows. Atmospheric conditions within the burrow differ from those above ground, in that the relative humidity is higher and both hypoxic and hypercapnic conditions may be encountered. Burrow conditions, nevertheless, are relatively stable throughout the year with a diel temperature range of less than 2°C (Bennett et al., 1988) and similar seasonal constancy (Gorou, 1970). The naked mole-rat is a remarkable mammal in many ways. Firstly, it is eusocial, living in colonies of up to 300 individuals with a strict division of labour culminating in a single breeding female (Jarvis, 1981). Secondly, it has the longest lifespan known of any animal under 100g in weight, living more than 16 years in captivity (Jarvis and Bennett, 1990a, b). These animals are also effectively naked, having only tactile vibrissae, and possess a skin that is loosely folded, lacks sweat glands and is very permeable to water (Tucker, 1981). These latter features are thought to contribute significantly to the "poor thermoregulatory ability" displayed by these animals (Withers and Jarvis, 1980; Tucker, 1981). Several factors limit the maintenance of a controlled body temperature, viz. (a) the size of the animal (Pearson, 1948), (b) the thermal environment (e.g. in reptiles and insects (Tracy, 1977), (c) the development of mechanisms for producing endogenous heat e.g. in newborn birds and mammals (Chew and Spencer, 1967) and (d) the degree of insulation (Scholander et aL, 1950). Employment of endothermy becomes more costly the smaller the 227
animal. Many small birds and mammals, therefore, are compelled to employ facultative hypothermia, albeit for short periods of time (Hainsworth and Wolf, 1970; Hudson, 1978; Heldmaier and Steinlechner, 1981) when temperatures fall below certain critical values (Buffenstein, 1984). Whilst the "poor thermoregulatory ability" of naked mole-rats is often referred to (McNab, 1966; Withers and Jarvis, 1980; Tucker, 1981), this has not been thoroughly investigated under steady-state conditions. We question whether naked mole-rats are indeed "poorly thermoregulating" homeotherms or rather poikilotherms, using the precise definitions of these terms given in the IUPS glossary (Anon, 1987). This paper therefore re-examines body temperature, metabolism and heat exchange mechanisms in naked mole-rats. MATERIAL AND METHODS
Seventeen adult naked mole-rats, weighing 42.8 + 4.5 g were used in determining the effect of ambient temperature (Ta, over a range of 12-37°C), on body temperature (Tb), rate of oxygen consumption (I702) and evaporative water loss (EWL). All measurements were determined during daylight hours (08:00 h - I 7: 00 h). Animal maintenance Naked mole-rats used in this study were born in captivity. Their progenitors were collected in northern Kenya during 1980. These animals were housed in a climatically controlled room, simulating natural conditions, with an ambient temperature of 30 + I°C and relative humidity between 70 and 80% (Jarvis, 1990). The mole-rats were fed an ad libitum
228
R O ( ' H E L L E BUFFENSTEIN a n d
diet of mixed fresh fruit and vegetables. During this period body mass was regularly monitored to the nearest 0.1 g. The average mass of mole-rats used in this study was 32.1 _+ 5.4g (n = 14). Thermoregulatory measurements
Naked mole-rats do not display a circadian rhythm (Jarvis and Bennett, 1990a, b). However, all measurements of T~, 1202 and EWL were made between 08:00h and 17:00h. Body temperatures
The effect of Ta on Tb was determined by measuring Tb after exposure to a wide range of Ta. Body temperature was measured by inserting a copperconstantan thermocouple approximately 2 cm into the rectum. The thermocouple was connected to a calibrated digital display (Bailey Bat). At each Ta the mole-rats were given 4 h to become thermally equilibrated. At 72~sbelow 20°C and above 34°C, this equilibration period was reduced to 2.5 h. All measurements were taken immediatedly after monitoring 1202 and EWL. In addition core temperature (Tb), skin temperature (T~k) and T~ were measured in 14 animals housed individually in a temperature controlled room at 30-32=C. Oxygen consumption
Oxygen consumption and EWL were measured simultaneously over the Ta range (12-37°C), using an open flow system (Depocas and Hart, 1957), in which inlet air was not dried. As the animals have a very permeable skin (Tucker, 1981), we did not wish to subject them to unnatural addition stresses by drying the inlet air. Air flowed through the respiratory chamber at 150-200ml/min and was measured by a Hastings mass flowmeter (Teledyne HastingsRaydist). The air passed over a sensor for relative humidity (Hygrodynamics, API Instruments). Thereafter the air was dried over silica gel and passed into an oxygen analyser (S-3A/ii Ametek, Sensor model N37-M). The oxygen analyser, thermocouples and relative humidity probe were connected to a data logger (PD 2064 Esterline Angus) which was programmed to record at 5-rain intervals. Monitoring of 1202 and T, within the chamber began immediately on placing the animal in a chamber. However minimal rates of oxygen were determined only after the Zd within the chamber and the rate of I~O2 had reached a steady state. Time taken to reach a steady state was dependent on the T~, and took approximately 2-3 h. Thereafter I202 was monitored for 1 h. At each T, the lowest six consecutive readings for each animal, corrected to STP, were used in calculating the resting minimal metabolic rate.
SHLOMO YAHAV
imental chamber and the control was used in the determination of EWL, using the equation: EWL = (X~ * R H * I-" • 60)/(1000 * 100 • M) where EWL is a water loss rate (rag H:O/g/h), X~ is a mass of water in saturated air at the Td, (g/ml), R H is the change in relative humidity caused by the animal (%), F is the flow rate (ml/min) and M is the mass of the animal (g). All data in the text are presented as means and standard deviations. Linear and exponential regression equations were calculated as described by Zar (1974). Pair Student t-tests were used in comparing skin, core and ambient temperature. Data were considered significantly different at P ~<0.05. RESULTS
Body temperature
Over the entire T~ range monitored (12-37 C). it"b was dependent on T, (Fig. 1). This relationship was linear and can be described by the equation: Tb = 0 . 5 6 8 + l . 0 1 6 T ~ ;
Skin temperature at 7~, of 31.9_+ 1.2C was 30.8 _+ 0.9°C (n = 14). This was significantly lower (P ~<0.01) than both Th (32.6 _ 0.7) and T~,. Oxygen consumption
Below T~ 20°C, 1202 was markedly elevated (Fig. 2) for only the first 45 min. This was attributed to increased activity, as the animals attempted to escape and to non-steady state conditions caused by opening the metabolic chamber. Thereafter VO, decreased dramatically at a rate of 0.21 ml/g/min interval, reaching a steady state with minimal values (0.17 ml/g/h) after 90rain (Fig. 2) at the lowest T,. All animals demonstrate apnea at these low rates of 1202 and do not move. After an equilibration period at each T,, 120, increased with increasing T,, exhibiting a typical poikilothermic response (Fig. 3) reaching a maximum at Td 29°C. This relationship can be described by the exponential equation: l?Oz=0.0615e°USr";
r=0.86, n=40.
When Tds increased above 29°C, PO2 followed the typical endothermic pattern decreasing with increasing T,, reaching a minimum rate at 31°C.
40 "
T==0,568+1.016To r,-0.997
30-
20-
Evaporative water loss Air flowing into the chamber was not dried. The vapour pressure in the system without an animal at 15°C was 0.9 kPa and at the highest measured temperature (36°C) was 3.7kPa. The change in relative humidity between the air leaving the exper-
r=0.977, n = 5 4
10 10
n=54
P" :6"
/" "/•
~.~I"
~"
, 20 Ambient
, 30 temperoture
, 40 (*C)
Fig. l. Effect of ambient temperature on body temperature.
The poikilothermic mammal
the rate of biomass production. This is especially true in a chthonic ecosystem which is characterized by a poor and periodic food supply and by an atmosphere saturated with moisture (Nevo, 1979). Consequently, there are many physiological adaptations to a subterranean existence (Arieli et al., 1977; Contreras and McNab, 1990; Jarvis and Bennett, 1990a, b). These include low basal metabolic rates and low resting body temperatures (McNab, 1979). H. glaber conforms with some of these trends in that resting metabolic rate is reduced. Body temperature is however directly dependent on the Ta of the environs.
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Fig. 2. Changes in oxygen consumption in an individual mole-rat housed at 15°C over a 2 h period.
Minimal (endothermic) I202 values (1.00 + 0.09 ml/ g/h, n = 19) were obtained between 7", 31-34°C. Thereafter VO2 increased once again with increasing 7+. (Fig. 3). Evaporative water loss Evaporative water loss increased exponentially with increasing T, [Fig. 4(a)] where: EWL = 0.0015 e°289:q; r = 0.93, n = 54. Within the "thermoneutral zone" (31-34°C), EWL amounted to 16.59 _+ 3.44 mg H20/g/h and accounted for 173+ 51% of the heat produced [Fig. 4(b)]. DISCUSSION Measurements of energy metabolism, vis-~-vis heat production and loss, are extremely relevant in an ecological context, in that they are related to the amount of food taken from the ecotope and also to .E
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+
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Fig. 3. Effects of ambient temperature on oxygen consumption.
Body temperature The naked mole-rat showed a complete lack of control of Tb over the entire range of ambient temperatures measured. Indeed Tb was essentially proportional to 7', (Fig. 1), indicating that these animals are poikilotherms and are, therefore, unique amongst mammals. At the lowest T,s measured, mole-rats were incapable of moving and could not raise their TbS in the absence of exogenous heat sources. These animals, most likely would have died if exposed to low T,s for long periods. It is well known that the range of thermal environments in which a mammal can maintain body temperature is reduced the smaller the animal, culminating in the smallest mammals (e.g. 2.5g shrews) only maintaining Tb when kept in a perfectly constant thermal environment (Tracey, 1977). This inability to maintain Tb outside a very narrow 7", range is attributed to their high surface area/volume ratios, limited insulative covering (e.g. fur, fat and/or feathers) and prohibitively high metabolic rates. Naked mole-rats weigh on average 35 g and as such their body mass is no where near the expected lower limit of endothermy (Tracy, 1977; McNab, 1983). The insulation of these mammals is however very poor. They lack fur, but rather, possess a thin layer of subcutaneous fat. Lack of insulation, might therefore be a contributing factor to the observed poikilothermic response to ambient temperature. An alternate suggestion as to why these atypical mammals exhibit poikiothermy is that they have lost the ability to produce endogenously sufficient heat (Buffenstein et al., in preparation) to control Tb, having exploited a thermally stable but resource limiting milieu for millenia (Lavocat, 1978). In addition, their social lifestyle (i.e. resting in groups) assists in maintaining a relatively constant Tb (+I°C), albeit over the very narrow range of Tas (30-34°C) normally encountered in their equatorial habitat (Yahav and Buffenstein, 1991). Oxygen consumption In their natural habitat, naked mole-rats would seldom, if ever, be exposed to temperatures below 28~C. For the first 45 min in the metabolic chamber, I702 increased (Fig. 2). We attribute this increase in I702 to firstly, non-steady state conditions within the chamber as a result of opening the system and introducing warmer air, and secondly to increased initial activity when the animals are confined in the cold metabolic chambers. Naked mole-rats, normally, seek out warmer areas of the burrow system (Jarvis, 1990). It is therefore thought that their initial
230
ROCHELLE
BUFFENSTEIN
response to the cold was to attempt to leave the area. This hypothesis is borne out by the observations of high activity and digging behaviour when exposed to cold. Although we did not measure Tb during the period of 1202 monitoring (but only on completion of V 0 2 monitoring), we assume that with time, the animals became hypothermic and 1202 correspondingly dropped in a poikilothermic manner reaching an equilibrated steady hypothermic state after 90 min (Fig. 2). It is highly unlikely that this hypothermia is reversible by endogenous means. These animals do not employ non-shivering thermogenesis (NST) when subjected to noradrenaline stimulation, both under normal and cold simulated conditions (Buffenstein et al., in preparation). Lack of a NST response after noradrenaline stimulation supports our suggestion that these animals are indeed poikilotherms rather than "poorly thermoregulating homeotherms'" (McNab, 1966; Withers and Jarvis, 1980) in torpor. It is, therefore, speculated that these animals, unlike most small mammals do not employ torpor (Lyman, 1982) in response to cold. Rather, given their thermally stable habitat, the level of autonomic control and/or the mechanisms for thermoregulation are insufficient to enable homeothermy in both individuals isolated from the colony and within the colony at TdS below 28°C. Animals huddling in groups show the same trends in 1202 with T,, to those housed individually (Yahav and Buffenstein, 1991). The energetic cost of maintaining Tb in animals with poor insulation becomes prohibitive at low T,s. Whilst this holds true for the naked mole-rat, energetic demands in this animal are further exaccerbated by the high energetic costs associated with the location of underground food resources (Vleck, 1981; Lovegrove, 1989). Living in the semi-arid zone, food resources are limiting and the cost of seeking food, might not always be met. The reduction of energy requirements albeit at the expense of maintaining endothermy, could therefore, contribute to their successful colonization of their chosen habitat. Above 29~C IkOz followed the typical endothermic pattern, suggesting that those animals are partially thermoregulating. They do not, however, employ NST, and heat generation by increasing 1202 is insufficient to maintain a constant Th. Instead Tb is governed entirely by 7", (Fig. 1) and the animals could be described as endothermic poikilotherms (i.e. animals that produce endogenous heat but cannot regulate Tb, resulting in a Tb that conforms with 7~,; Anon, 1987). Whilst endothermic homeotherms (e.g. most mammals) and ectothermic poikilotherms (most insects) are the expected norms in thermoregulatory biology (Bligh, 1973; Schmidt-Nielsen, 1983). ectothermic homeotherms have been previously reported (e.g. varanids and crocodiles, Louw et al., 1976; Lang, 1986). This, however, is the first report to date of an apparent endothermic poikilotherm. The apparent "thermoneutral zone" (Fig. 3) lies at temperatures normally encountered in their natural mileu with a minimal resting metabolic rate of 1.0ml/g/h. These results are higher than those reported by McNab (1966) and Withers and Jarvis (1980) but are still 66% of that expected allometrically for burrowing mammals (McNab, 1979).
and
SHLOMO
YAHAV
Reduced R M R is an adaptive feature in response to the limited resources and is also advantageous within the burrow context. Firstly, low R M R would reduce the chances of overheating in a closed burrow system where high relative humidities and limited air movements would preclude the use of evaporative and convective cooling. Secondly, low RMRs will reduce gaseous exchange in the hypoxic/hypercapnic conditions encountered in plugged burrows (Arieli et al., 1977). Et~aporatit,e water loss
Below 22"C, EWL is negligible, at the sensitivity level of our equipment [Fig. 4(a)]. Above this temperature, EWL increased exponentially reaching maximum rate (25 mg/g/h) at the highest T, recorded. These rates are amongst the highest recorded for homeotherms and even exceed rates measured at lethal TbS (Hart, 1971; Buffenstein and Jarvis, 1985). Pulmocutaneous water loss data obtained from daily water balance studies (Buffenstein and Yahav, in preparation) confirm that these high EWL rates are real and not experimental artifacts. These high rates of EWL are attributed to passive uncontrolled water loss by diffusion through their very fine and poorly insulated skin (Tucker, 1981). The porous skin is such that prolonged exposure to low humidities leads to cracked dry peeling skin (Jarvis, 1990) and may result in death by dehydration. The morphology of the skin is such that these animals, if isolated at normal burrow temperatures, would lose about 36% of their body weight per day and would not survive long periods above the ground at their preferred T,s. High rates of EWL are reduced when
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Fig. 4. Effects of ambient temperature on (a) evaporative water loss and (b) percentage heat loss.
The poikilothermic mammal animals huddle in groups (Yahav and Buffenstein, 1991) as huddling reduces the surface area through which uncontrolled water loss occurs. The high humidities encountered in plugged burrows prevent these high rates of passive water loss and hence impeded evaporative cooling. Burrow humidities, coupled with the social huddling behaviour exhibited by these animals enable their survival at the high burrow temperatures encountered in their habitat. Within the "thermoneutral zone", EWL accounted for 1 7 3 + 5 1 % of the metabolic heat produced [Fig. 4(b)]. One would therefore expect these animals to have body temperatures approximately 3°C lower than ambient. This was not the case, rather, Tb closely approximated Ta, whilst skin temperature was lower than both Tb and Ta. A surface temperature lower than T~ facilitates heat gain from the environment to the animal. Using Fourier's law (Seagrave, 1971), heat transfer coefficients for both convection and radiation (Heller, 1972; Seagrave, 1971) and the data for 1702 and EWL presented here, a skin temperature 0.4-2.8°C lower than Ta would enable the animal to remain in thermal equilibrium within the range of temperatures encountered within the TNZ. Measured Tsk was 1.8 + 0.6°C lower than Tb and 1.2 _+0.7°C lower than ambient (30-32°C) and thus facilitated this heat transfer from the environment to the animal. Heat gain in this manner coupled with metabolic heat production therefore counteracts the high rate of evaporative heat loss and keeps Tb at approximately T~ levels. In conclusion, the low level of metabolic heat production, coupled with the high passive rates of heat transfer are such that naked mole rats cannot regulate Tb. Even at high T~s (i.e. > 29°C) despite the endothermic pattern in 1702, Tb is still governed predominantly by T~. Infact the linear relationship describing Tb and T~ at high temperatures does not differ from that at low temperatures (Fig. 1). The naked mole-rat is therefore unique amongst mammals in that it is indeed, a poikilotherm. SUMMARY The naked mole-rat is a chthonic equatorial dwelling mammal, that did not regulate Tb over the entire Ta range (12-37°C) monitored; instead Tb was directly dependent on T,d. Below 29°C, I702 increased with increasing Ta in a poikilothermic manner. Thereafter the response of 1702 to Ta followed a typical endothermic pattern, with minimal metabolic rate of 1.00 ml/g h at Tas ranging between 31 and 34°C. Over this Ta range, EWL accounted for 173% of the metabolic heat produced. As a direct consequence of this high rate of evaporative cooling, skin temperature was 1.8 + 0.6°C lower than Tb and 1.2 _+0.7"C lower than Z,. This facilitated heat transfer to the animal by convection and radiation from the environment. The summed effect of environmental heat gain and the low levels of metabolic heat production counteract the evaporative heat loss and maintain thermal equilibrium with Tb approximating Ta. Despite the apparent employment of endothermy at high Tas (>29°C), these animlas exhibit a complete dependence of Tb on 77, (as indicated by the same linear relationship at high and low temperatures).
231
These animals are therefore unique amongst mammals in that they appear to be poikilotherms. Acknowledgements--We sincerely thank Professor Jenny Jarvis for supplying the animals, and for her comments on this manuscript. We gratefully acknowledge CSIR funding for this project. This experimentwas approved by the Animal Ethics Committee of the University of the Witwaterstrand (AEC 89/6/2).
REFERENCES Anon. IUPS Thermal Commission (1987) Glossary of terms for thermal physiology. Pfliigers Arch. 410, 567-587. Arieli R., Ar A. and Shkolnik A. (1977) Metabolic responses of fossorial rodent (Spalax ehrenbergi) to simulated burrow conditions. Physiol. Zool. 51, 61-75. Bennett N. B., Jarvis J. U. M. and Davis K. C. (1988) Daily and seasonal temperatures in the burrows of African rodent moles. S. Afr. J. Zool. 3, 189-195. Bligh J. (1973) Temperature Regulation in Mammals and Other Vertebrates. North-Holland, Amsterdam. Buffenstein R. (1984) The importance of microhabitat in thermoregulation and thermal conductance in two Namib rodents---a creative dweller, Aethomys namaquensis, and burrow dweller, Gerbillurus paeba. J. therm. Biol. 9, 235-241. BuffensteinR. and Jarvis J. U. M. (1985) Thermoregulation and metabolism in the smallest African gerbil, Gerbillus pusillus. J. Zool. Lond. 205, 107-121. Chew R. M. and Spencer E. (1967) Development of metabolic response to cold in young mice of four species. Comp. Biochem. Physiol. 22, 873-888. Contreras L. C. and MacNab B. K. (1990) Thermoregulation and energetics in subterranean mammals. In Evolution of Subterranean Mammals at the Organisational and Molecular Levels (Edited by Nevo E. and Reig O. A.), pp. 231-250. Wiley-Liss, New York. De Graaff G. (1981) The Rodents of Southern Africa, pp. 267. Butterworths, Pretoria. Depocas F. and Hart J. S. (1957) Use of the Pauling oxygen analyser for measurement of oxygen consumption of animals in open circuit systems and in a short-lag closedcircuit apparatus. J. appl. Physiol. 10, 388-392. Gorou P. (1970) L'Afrique. Hatchett, Paris. Hainsworth, F. R. and Wolf L. L. (1970) Regulation of oxygen consumption and body temperature during torpor in a hummingbird, Eulampis jugularis. Science 168, 368-369. Hart J. (1971) Rodents. In Comparative Physiology and Thermoregulation (Edited by Whittow G. C.), pp. 2-149. Academic Press, New York. Heldmaier G. and Steinlechner S. (1981) Seasonal pattern and the energetics of short daily torpor in the Djungarian hamster, Phodopus sangorus. Oecologia 48, 265-270. Heller H. C. (1972) Measurements of convective and radiative heat transfer in small mammals. J. Mammal. 53, 289-295. Hudson H. W. (1978) Shallow daily torpor: a thermoregulatory adaptation. In Strategies in Cold: Natural Torpidity and Thermogenesis (Edited by Wang L. C. H. and Hudson J. W.), pp. 67-108. Academic Press, New York. Jarvis J. U. M. (1981) Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212, 571-573. Jarvis J. U. M. (1990) Capture methods, maintenance in captivity and transport. In Biology of the Naked Mole Rat (Edited by Sherman P. W., Jarvis J. U. M. and Alexander R. D.), pp. 467-483. Princeton UniversityPress, Princeton. Jarvis J. U. M. and Bennett N. C. (1990a) Ecology and behaviour of the family Bathyergidae. In Biology of the Naked Mole Rat (Edited by Sherman P. W., Jarvis
232
ROCHELLE BUFFENSTEINand SHLOMOYAHAV
J. U. M. and Alexander R. D.I, pp. 66 96. Princeton University Press, Princeton. Jarvis J. U. M. and Bennett N. C. i 1990b) The evolutionary history, population biology and social structure of African mole-rats: family Bathyergidae. In Evolution ~?f
Subterranean Mammals at the Organismal and Molecular Levels (Edited by Nevo E. and Osvaldo O. A.), pp. 97 128. Wiley-Liss, New York. Lang J. W. (1986) Crocodilian thermal selection. In Wildlife Management: Crocodiles and Alligators (Edited by Webb G. J. W., Manolis S. C. and Whitehead), pp. 301 317. Surrey Beatty, Vancouver. Lavocat R. (1978) Rodentia and Lagomorpha. In Evolution of African Mammals (Edited by Magio V. H. and Cooke H. B. S.), pp. 68 89 Harvard University Press, Cambridge, MA. Louw G. N., Young B. A. and Bligh J. (1976) Effect of thyroxine and noradrenaline on thermoregulation, cardiac rate and oxygen consumption in the Monitor lizard, Varanus Albigularis. J. therm. Biol. 1, 189-193. Lovegrove B. G. (1989) The cost of burrowing by the social mole rat (Bathyergidea) Cryptomys demarensis and Heterocephalus glaber: the role of soil moisture. Physiol. Zool. 62, 449-469, Lyman C. P. (1981) Who and who among the hibernators. In Hibernation and Torpor in Mammals and Birds (Edited by Lyman C. P., Willis J. S., Malan A. and Wang L. C. H.), pp. 12-36. Academic Press, New York. McNab B. K. (1986) The metabolism of fossorial rodents: A study of convergence. Ecology 47, 712-733. McNab B. K. (1979) On estimating thermal conductance in endotherms. Physiol. Zool. 53, 145-156. McNab B. K. (1983) Energetics, body size and the limits to endothermy. J. Zool. Lond. 199, 1 29.
Nevo E. (1979) Adaptive convergence and divergence of subterranean mammals. A. Rev. ecol. Svst. 10, 269-308. Pearson O. (1948) Metabolism of small mammals, with remarks on the lower limit of mammalian size. Science 108, 44. Schmidt-Nielsen K. (1983) Temperature regulation. In Animal Physiology: Adaptation and Environment (Edited by Schmidt-Nielsen K.), pp. 249 308. Cambridge University Press, Cambridge. Scholander P. F., Hock R., Walters, V., Johnson F. and Irving L. (1950) Heat regulation in some arctic tropical mammals birds. Biol. Bull. 9, 237 258. Seagrave R. C. (1971) Heat transfer in living systems. In Biomedical Applications (~1"Heat and Mass Transfer (Edited by Seagrave R. C.), pp. 93 113. Iowa State University Press, Iowa. Tracy C. R. (1977) Minimum size of mammalian homeotherms: role of the thermal environment. Science 198, 1034 1035. Tucker R. (1981) The digging behavior and skin differentiations in Heterocephalus glaber. J. Morphol. 168, 51 71, Withers P. C. and Jarvis J. U. M. (1980) The effect of huddling on thermoregulation and oxygen consumption for the naked mole-rat. Comp. Biochem. Physiol. ¢~A, 215-219. Vleck D. (1981) Burrow structure and foraging costs in the fossorial rodent, Thomomys bottae. Oecologia 49, 391-396. Yahav S. and Buffenstein R. (1991) Huddling behaviour facilitates homeotherapy in Heterocephalus glaber. Physiol. Zool. In press. Zar J. H. (1974) Biostatistical Analysis. Prentice-Hall, Englewood Cliffs, N.J.
0306-4565/91 $3.00+ 0.00 Copyright© 1991 PergamonPress plc
IS THE N A K E D MOLE-RAT H E T E R O C E P H A L U S GLABER A N E N D O T H E R M I C YET POIKILOTHERMIC M A M M A L ? ROCHELLE BUFFENSTEINand SHLOMOYAHAV Department of Physiology, Medical School, University of Witwatersrand, 7 York Road, Parktown 2193, Johannesburg, South Africa
(Received 25 August 1990; accepted in revisedform 19 January 1991)
Abstract--1. Thermoregulatory changes with ambient temperature (Ta) were monitored in Heterocephalus glaber between 12 and 37°C. 2. At all Tas monitored, body temperature (Tb) was directly proportional to T~ (Tb = 0.568 + 1.016 T~). 3. Below T~ 29°C, 1?O2 varied in a typically poikilothermic pattern, whereas above 29°C, I702 followed a typically endothermic pattern. 4. At T~s between 31 and 34°C, 1702was minimal (1.00 _+0.09 ml/g/h), skin temperature was 1.8 _+0.6°C lower than Tb and evaporative water loss accounted for 173.7 _ 51.0% of the metabolic heat produced. 5. The high rates of heat transfer are such that individual naked mole-rats cannot regulate Tb over the entire range of measured /'as and, as such, are poikilothermic mammals. Key Word Index: Poikilothermic mammal; endothermy; skin temperature; high evaporative water loss; body temperature
INTRODUCTION
The naked mole-rat, Heterocephalus glaber is a strictly subterranean (chthonic) mammal found only in the tropical semi-arid zones of north east Africa (De Graaff, 1981). Here, it lives in the extensive maze of poorly ventilated plugged burrows. Atmospheric conditions within the burrow differ from those above ground, in that the relative humidity is higher and both hypoxic and hypercapnic conditions may be encountered. Burrow conditions, nevertheless, are relatively stable throughout the year with a diel temperature range of less than 2°C (Bennett et al., 1988) and similar seasonal constancy (Gorou, 1970). The naked mole-rat is a remarkable mammal in many ways. Firstly, it is eusocial, living in colonies of up to 300 individuals with a strict division of labour culminating in a single breeding female (Jarvis, 1981). Secondly, it has the longest lifespan known of any animal under 100g in weight, living more than 16 years in captivity (Jarvis and Bennett, 1990a, b). These animals are also effectively naked, having only tactile vibrissae, and possess a skin that is loosely folded, lacks sweat glands and is very permeable to water (Tucker, 1981). These latter features are thought to contribute significantly to the "poor thermoregulatory ability" displayed by these animals (Withers and Jarvis, 1980; Tucker, 1981). Several factors limit the maintenance of a controlled body temperature, viz. (a) the size of the animal (Pearson, 1948), (b) the thermal environment (e.g. in reptiles and insects (Tracy, 1977), (c) the development of mechanisms for producing endogenous heat e.g. in newborn birds and mammals (Chew and Spencer, 1967) and (d) the degree of insulation (Scholander et aL, 1950). Employment of endothermy becomes more costly the smaller the 227
animal. Many small birds and mammals, therefore, are compelled to employ facultative hypothermia, albeit for short periods of time (Hainsworth and Wolf, 1970; Hudson, 1978; Heldmaier and Steinlechner, 1981) when temperatures fall below certain critical values (Buffenstein, 1984). Whilst the "poor thermoregulatory ability" of naked mole-rats is often referred to (McNab, 1966; Withers and Jarvis, 1980; Tucker, 1981), this has not been thoroughly investigated under steady-state conditions. We question whether naked mole-rats are indeed "poorly thermoregulating" homeotherms or rather poikilotherms, using the precise definitions of these terms given in the IUPS glossary (Anon, 1987). This paper therefore re-examines body temperature, metabolism and heat exchange mechanisms in naked mole-rats. MATERIAL AND METHODS
Seventeen adult naked mole-rats, weighing 42.8 + 4.5 g were used in determining the effect of ambient temperature (Ta, over a range of 12-37°C), on body temperature (Tb), rate of oxygen consumption (I702) and evaporative water loss (EWL). All measurements were determined during daylight hours (08:00 h - I 7: 00 h). Animal maintenance Naked mole-rats used in this study were born in captivity. Their progenitors were collected in northern Kenya during 1980. These animals were housed in a climatically controlled room, simulating natural conditions, with an ambient temperature of 30 + I°C and relative humidity between 70 and 80% (Jarvis, 1990). The mole-rats were fed an ad libitum
228
R O ( ' H E L L E BUFFENSTEIN a n d
diet of mixed fresh fruit and vegetables. During this period body mass was regularly monitored to the nearest 0.1 g. The average mass of mole-rats used in this study was 32.1 _+ 5.4g (n = 14). Thermoregulatory measurements
Naked mole-rats do not display a circadian rhythm (Jarvis and Bennett, 1990a, b). However, all measurements of T~, 1202 and EWL were made between 08:00h and 17:00h. Body temperatures
The effect of Ta on Tb was determined by measuring Tb after exposure to a wide range of Ta. Body temperature was measured by inserting a copperconstantan thermocouple approximately 2 cm into the rectum. The thermocouple was connected to a calibrated digital display (Bailey Bat). At each Ta the mole-rats were given 4 h to become thermally equilibrated. At 72~sbelow 20°C and above 34°C, this equilibration period was reduced to 2.5 h. All measurements were taken immediatedly after monitoring 1202 and EWL. In addition core temperature (Tb), skin temperature (T~k) and T~ were measured in 14 animals housed individually in a temperature controlled room at 30-32=C. Oxygen consumption
Oxygen consumption and EWL were measured simultaneously over the Ta range (12-37°C), using an open flow system (Depocas and Hart, 1957), in which inlet air was not dried. As the animals have a very permeable skin (Tucker, 1981), we did not wish to subject them to unnatural addition stresses by drying the inlet air. Air flowed through the respiratory chamber at 150-200ml/min and was measured by a Hastings mass flowmeter (Teledyne HastingsRaydist). The air passed over a sensor for relative humidity (Hygrodynamics, API Instruments). Thereafter the air was dried over silica gel and passed into an oxygen analyser (S-3A/ii Ametek, Sensor model N37-M). The oxygen analyser, thermocouples and relative humidity probe were connected to a data logger (PD 2064 Esterline Angus) which was programmed to record at 5-rain intervals. Monitoring of 1202 and T, within the chamber began immediately on placing the animal in a chamber. However minimal rates of oxygen were determined only after the Zd within the chamber and the rate of I~O2 had reached a steady state. Time taken to reach a steady state was dependent on the T~, and took approximately 2-3 h. Thereafter I202 was monitored for 1 h. At each T, the lowest six consecutive readings for each animal, corrected to STP, were used in calculating the resting minimal metabolic rate.
SHLOMO YAHAV
imental chamber and the control was used in the determination of EWL, using the equation: EWL = (X~ * R H * I-" • 60)/(1000 * 100 • M) where EWL is a water loss rate (rag H:O/g/h), X~ is a mass of water in saturated air at the Td, (g/ml), R H is the change in relative humidity caused by the animal (%), F is the flow rate (ml/min) and M is the mass of the animal (g). All data in the text are presented as means and standard deviations. Linear and exponential regression equations were calculated as described by Zar (1974). Pair Student t-tests were used in comparing skin, core and ambient temperature. Data were considered significantly different at P ~<0.05. RESULTS
Body temperature
Over the entire T~ range monitored (12-37 C). it"b was dependent on T, (Fig. 1). This relationship was linear and can be described by the equation: Tb = 0 . 5 6 8 + l . 0 1 6 T ~ ;
Skin temperature at 7~, of 31.9_+ 1.2C was 30.8 _+ 0.9°C (n = 14). This was significantly lower (P ~<0.01) than both Th (32.6 _ 0.7) and T~,. Oxygen consumption
Below T~ 20°C, 1202 was markedly elevated (Fig. 2) for only the first 45 min. This was attributed to increased activity, as the animals attempted to escape and to non-steady state conditions caused by opening the metabolic chamber. Thereafter VO, decreased dramatically at a rate of 0.21 ml/g/min interval, reaching a steady state with minimal values (0.17 ml/g/h) after 90rain (Fig. 2) at the lowest T,. All animals demonstrate apnea at these low rates of 1202 and do not move. After an equilibration period at each T,, 120, increased with increasing T,, exhibiting a typical poikilothermic response (Fig. 3) reaching a maximum at Td 29°C. This relationship can be described by the exponential equation: l?Oz=0.0615e°USr";
r=0.86, n=40.
When Tds increased above 29°C, PO2 followed the typical endothermic pattern decreasing with increasing T,, reaching a minimum rate at 31°C.
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Evaporative water loss Air flowing into the chamber was not dried. The vapour pressure in the system without an animal at 15°C was 0.9 kPa and at the highest measured temperature (36°C) was 3.7kPa. The change in relative humidity between the air leaving the exper-
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Fig. l. Effect of ambient temperature on body temperature.
The poikilothermic mammal
the rate of biomass production. This is especially true in a chthonic ecosystem which is characterized by a poor and periodic food supply and by an atmosphere saturated with moisture (Nevo, 1979). Consequently, there are many physiological adaptations to a subterranean existence (Arieli et al., 1977; Contreras and McNab, 1990; Jarvis and Bennett, 1990a, b). These include low basal metabolic rates and low resting body temperatures (McNab, 1979). H. glaber conforms with some of these trends in that resting metabolic rate is reduced. Body temperature is however directly dependent on the Ta of the environs.
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Minimal (endothermic) I202 values (1.00 + 0.09 ml/ g/h, n = 19) were obtained between 7", 31-34°C. Thereafter VO2 increased once again with increasing 7+. (Fig. 3). Evaporative water loss Evaporative water loss increased exponentially with increasing T, [Fig. 4(a)] where: EWL = 0.0015 e°289:q; r = 0.93, n = 54. Within the "thermoneutral zone" (31-34°C), EWL amounted to 16.59 _+ 3.44 mg H20/g/h and accounted for 173+ 51% of the heat produced [Fig. 4(b)]. DISCUSSION Measurements of energy metabolism, vis-~-vis heat production and loss, are extremely relevant in an ecological context, in that they are related to the amount of food taken from the ecotope and also to .E
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Body temperature The naked mole-rat showed a complete lack of control of Tb over the entire range of ambient temperatures measured. Indeed Tb was essentially proportional to 7', (Fig. 1), indicating that these animals are poikilotherms and are, therefore, unique amongst mammals. At the lowest T,s measured, mole-rats were incapable of moving and could not raise their TbS in the absence of exogenous heat sources. These animals, most likely would have died if exposed to low T,s for long periods. It is well known that the range of thermal environments in which a mammal can maintain body temperature is reduced the smaller the animal, culminating in the smallest mammals (e.g. 2.5g shrews) only maintaining Tb when kept in a perfectly constant thermal environment (Tracey, 1977). This inability to maintain Tb outside a very narrow 7", range is attributed to their high surface area/volume ratios, limited insulative covering (e.g. fur, fat and/or feathers) and prohibitively high metabolic rates. Naked mole-rats weigh on average 35 g and as such their body mass is no where near the expected lower limit of endothermy (Tracy, 1977; McNab, 1983). The insulation of these mammals is however very poor. They lack fur, but rather, possess a thin layer of subcutaneous fat. Lack of insulation, might therefore be a contributing factor to the observed poikilothermic response to ambient temperature. An alternate suggestion as to why these atypical mammals exhibit poikiothermy is that they have lost the ability to produce endogenously sufficient heat (Buffenstein et al., in preparation) to control Tb, having exploited a thermally stable but resource limiting milieu for millenia (Lavocat, 1978). In addition, their social lifestyle (i.e. resting in groups) assists in maintaining a relatively constant Tb (+I°C), albeit over the very narrow range of Tas (30-34°C) normally encountered in their equatorial habitat (Yahav and Buffenstein, 1991). Oxygen consumption In their natural habitat, naked mole-rats would seldom, if ever, be exposed to temperatures below 28~C. For the first 45 min in the metabolic chamber, I702 increased (Fig. 2). We attribute this increase in I702 to firstly, non-steady state conditions within the chamber as a result of opening the system and introducing warmer air, and secondly to increased initial activity when the animals are confined in the cold metabolic chambers. Naked mole-rats, normally, seek out warmer areas of the burrow system (Jarvis, 1990). It is therefore thought that their initial
230
ROCHELLE
BUFFENSTEIN
response to the cold was to attempt to leave the area. This hypothesis is borne out by the observations of high activity and digging behaviour when exposed to cold. Although we did not measure Tb during the period of 1202 monitoring (but only on completion of V 0 2 monitoring), we assume that with time, the animals became hypothermic and 1202 correspondingly dropped in a poikilothermic manner reaching an equilibrated steady hypothermic state after 90 min (Fig. 2). It is highly unlikely that this hypothermia is reversible by endogenous means. These animals do not employ non-shivering thermogenesis (NST) when subjected to noradrenaline stimulation, both under normal and cold simulated conditions (Buffenstein et al., in preparation). Lack of a NST response after noradrenaline stimulation supports our suggestion that these animals are indeed poikilotherms rather than "poorly thermoregulating homeotherms'" (McNab, 1966; Withers and Jarvis, 1980) in torpor. It is, therefore, speculated that these animals, unlike most small mammals do not employ torpor (Lyman, 1982) in response to cold. Rather, given their thermally stable habitat, the level of autonomic control and/or the mechanisms for thermoregulation are insufficient to enable homeothermy in both individuals isolated from the colony and within the colony at TdS below 28°C. Animals huddling in groups show the same trends in 1202 with T,, to those housed individually (Yahav and Buffenstein, 1991). The energetic cost of maintaining Tb in animals with poor insulation becomes prohibitive at low T,s. Whilst this holds true for the naked mole-rat, energetic demands in this animal are further exaccerbated by the high energetic costs associated with the location of underground food resources (Vleck, 1981; Lovegrove, 1989). Living in the semi-arid zone, food resources are limiting and the cost of seeking food, might not always be met. The reduction of energy requirements albeit at the expense of maintaining endothermy, could therefore, contribute to their successful colonization of their chosen habitat. Above 29~C IkOz followed the typical endothermic pattern, suggesting that those animals are partially thermoregulating. They do not, however, employ NST, and heat generation by increasing 1202 is insufficient to maintain a constant Th. Instead Tb is governed entirely by 7", (Fig. 1) and the animals could be described as endothermic poikilotherms (i.e. animals that produce endogenous heat but cannot regulate Tb, resulting in a Tb that conforms with 7~,; Anon, 1987). Whilst endothermic homeotherms (e.g. most mammals) and ectothermic poikilotherms (most insects) are the expected norms in thermoregulatory biology (Bligh, 1973; Schmidt-Nielsen, 1983). ectothermic homeotherms have been previously reported (e.g. varanids and crocodiles, Louw et al., 1976; Lang, 1986). This, however, is the first report to date of an apparent endothermic poikilotherm. The apparent "thermoneutral zone" (Fig. 3) lies at temperatures normally encountered in their natural mileu with a minimal resting metabolic rate of 1.0ml/g/h. These results are higher than those reported by McNab (1966) and Withers and Jarvis (1980) but are still 66% of that expected allometrically for burrowing mammals (McNab, 1979).
and
SHLOMO
YAHAV
Reduced R M R is an adaptive feature in response to the limited resources and is also advantageous within the burrow context. Firstly, low R M R would reduce the chances of overheating in a closed burrow system where high relative humidities and limited air movements would preclude the use of evaporative and convective cooling. Secondly, low RMRs will reduce gaseous exchange in the hypoxic/hypercapnic conditions encountered in plugged burrows (Arieli et al., 1977). Et~aporatit,e water loss
Below 22"C, EWL is negligible, at the sensitivity level of our equipment [Fig. 4(a)]. Above this temperature, EWL increased exponentially reaching maximum rate (25 mg/g/h) at the highest T, recorded. These rates are amongst the highest recorded for homeotherms and even exceed rates measured at lethal TbS (Hart, 1971; Buffenstein and Jarvis, 1985). Pulmocutaneous water loss data obtained from daily water balance studies (Buffenstein and Yahav, in preparation) confirm that these high EWL rates are real and not experimental artifacts. These high rates of EWL are attributed to passive uncontrolled water loss by diffusion through their very fine and poorly insulated skin (Tucker, 1981). The porous skin is such that prolonged exposure to low humidities leads to cracked dry peeling skin (Jarvis, 1990) and may result in death by dehydration. The morphology of the skin is such that these animals, if isolated at normal burrow temperatures, would lose about 36% of their body weight per day and would not survive long periods above the ground at their preferred T,s. High rates of EWL are reduced when
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Fig. 4. Effects of ambient temperature on (a) evaporative water loss and (b) percentage heat loss.
The poikilothermic mammal animals huddle in groups (Yahav and Buffenstein, 1991) as huddling reduces the surface area through which uncontrolled water loss occurs. The high humidities encountered in plugged burrows prevent these high rates of passive water loss and hence impeded evaporative cooling. Burrow humidities, coupled with the social huddling behaviour exhibited by these animals enable their survival at the high burrow temperatures encountered in their habitat. Within the "thermoneutral zone", EWL accounted for 1 7 3 + 5 1 % of the metabolic heat produced [Fig. 4(b)]. One would therefore expect these animals to have body temperatures approximately 3°C lower than ambient. This was not the case, rather, Tb closely approximated Ta, whilst skin temperature was lower than both Tb and Ta. A surface temperature lower than T~ facilitates heat gain from the environment to the animal. Using Fourier's law (Seagrave, 1971), heat transfer coefficients for both convection and radiation (Heller, 1972; Seagrave, 1971) and the data for 1702 and EWL presented here, a skin temperature 0.4-2.8°C lower than Ta would enable the animal to remain in thermal equilibrium within the range of temperatures encountered within the TNZ. Measured Tsk was 1.8 + 0.6°C lower than Tb and 1.2 _+0.7°C lower than ambient (30-32°C) and thus facilitated this heat transfer from the environment to the animal. Heat gain in this manner coupled with metabolic heat production therefore counteracts the high rate of evaporative heat loss and keeps Tb at approximately T~ levels. In conclusion, the low level of metabolic heat production, coupled with the high passive rates of heat transfer are such that naked mole rats cannot regulate Tb. Even at high T~s (i.e. > 29°C) despite the endothermic pattern in 1702, Tb is still governed predominantly by T~. Infact the linear relationship describing Tb and T~ at high temperatures does not differ from that at low temperatures (Fig. 1). The naked mole-rat is therefore unique amongst mammals in that it is indeed, a poikilotherm. SUMMARY The naked mole-rat is a chthonic equatorial dwelling mammal, that did not regulate Tb over the entire Ta range (12-37°C) monitored; instead Tb was directly dependent on T,d. Below 29°C, I702 increased with increasing Ta in a poikilothermic manner. Thereafter the response of 1702 to Ta followed a typical endothermic pattern, with minimal metabolic rate of 1.00 ml/g h at Tas ranging between 31 and 34°C. Over this Ta range, EWL accounted for 173% of the metabolic heat produced. As a direct consequence of this high rate of evaporative cooling, skin temperature was 1.8 + 0.6°C lower than Tb and 1.2 _+0.7"C lower than Z,. This facilitated heat transfer to the animal by convection and radiation from the environment. The summed effect of environmental heat gain and the low levels of metabolic heat production counteract the evaporative heat loss and maintain thermal equilibrium with Tb approximating Ta. Despite the apparent employment of endothermy at high Tas (>29°C), these animlas exhibit a complete dependence of Tb on 77, (as indicated by the same linear relationship at high and low temperatures).
231
These animals are therefore unique amongst mammals in that they appear to be poikilotherms. Acknowledgements--We sincerely thank Professor Jenny Jarvis for supplying the animals, and for her comments on this manuscript. We gratefully acknowledge CSIR funding for this project. This experimentwas approved by the Animal Ethics Committee of the University of the Witwaterstrand (AEC 89/6/2).
REFERENCES Anon. IUPS Thermal Commission (1987) Glossary of terms for thermal physiology. Pfliigers Arch. 410, 567-587. Arieli R., Ar A. and Shkolnik A. (1977) Metabolic responses of fossorial rodent (Spalax ehrenbergi) to simulated burrow conditions. Physiol. Zool. 51, 61-75. Bennett N. B., Jarvis J. U. M. and Davis K. C. (1988) Daily and seasonal temperatures in the burrows of African rodent moles. S. Afr. J. Zool. 3, 189-195. Bligh J. (1973) Temperature Regulation in Mammals and Other Vertebrates. North-Holland, Amsterdam. Buffenstein R. (1984) The importance of microhabitat in thermoregulation and thermal conductance in two Namib rodents---a creative dweller, Aethomys namaquensis, and burrow dweller, Gerbillurus paeba. J. therm. Biol. 9, 235-241. BuffensteinR. and Jarvis J. U. M. (1985) Thermoregulation and metabolism in the smallest African gerbil, Gerbillus pusillus. J. Zool. Lond. 205, 107-121. Chew R. M. and Spencer E. (1967) Development of metabolic response to cold in young mice of four species. Comp. Biochem. Physiol. 22, 873-888. Contreras L. C. and MacNab B. K. (1990) Thermoregulation and energetics in subterranean mammals. In Evolution of Subterranean Mammals at the Organisational and Molecular Levels (Edited by Nevo E. and Reig O. A.), pp. 231-250. Wiley-Liss, New York. De Graaff G. (1981) The Rodents of Southern Africa, pp. 267. Butterworths, Pretoria. Depocas F. and Hart J. S. (1957) Use of the Pauling oxygen analyser for measurement of oxygen consumption of animals in open circuit systems and in a short-lag closedcircuit apparatus. J. appl. Physiol. 10, 388-392. Gorou P. (1970) L'Afrique. Hatchett, Paris. Hainsworth, F. R. and Wolf L. L. (1970) Regulation of oxygen consumption and body temperature during torpor in a hummingbird, Eulampis jugularis. Science 168, 368-369. Hart J. (1971) Rodents. In Comparative Physiology and Thermoregulation (Edited by Whittow G. C.), pp. 2-149. Academic Press, New York. Heldmaier G. and Steinlechner S. (1981) Seasonal pattern and the energetics of short daily torpor in the Djungarian hamster, Phodopus sangorus. Oecologia 48, 265-270. Heller H. C. (1972) Measurements of convective and radiative heat transfer in small mammals. J. Mammal. 53, 289-295. Hudson H. W. (1978) Shallow daily torpor: a thermoregulatory adaptation. In Strategies in Cold: Natural Torpidity and Thermogenesis (Edited by Wang L. C. H. and Hudson J. W.), pp. 67-108. Academic Press, New York. Jarvis J. U. M. (1981) Eusociality in a mammal: cooperative breeding in naked mole-rat colonies. Science 212, 571-573. Jarvis J. U. M. (1990) Capture methods, maintenance in captivity and transport. In Biology of the Naked Mole Rat (Edited by Sherman P. W., Jarvis J. U. M. and Alexander R. D.), pp. 467-483. Princeton UniversityPress, Princeton. Jarvis J. U. M. and Bennett N. C. (1990a) Ecology and behaviour of the family Bathyergidae. In Biology of the Naked Mole Rat (Edited by Sherman P. W., Jarvis
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J. U. M. and Alexander R. D.I, pp. 66 96. Princeton University Press, Princeton. Jarvis J. U. M. and Bennett N. C. i 1990b) The evolutionary history, population biology and social structure of African mole-rats: family Bathyergidae. In Evolution ~?f
Subterranean Mammals at the Organismal and Molecular Levels (Edited by Nevo E. and Osvaldo O. A.), pp. 97 128. Wiley-Liss, New York. Lang J. W. (1986) Crocodilian thermal selection. In Wildlife Management: Crocodiles and Alligators (Edited by Webb G. J. W., Manolis S. C. and Whitehead), pp. 301 317. Surrey Beatty, Vancouver. Lavocat R. (1978) Rodentia and Lagomorpha. In Evolution of African Mammals (Edited by Magio V. H. and Cooke H. B. S.), pp. 68 89 Harvard University Press, Cambridge, MA. Louw G. N., Young B. A. and Bligh J. (1976) Effect of thyroxine and noradrenaline on thermoregulation, cardiac rate and oxygen consumption in the Monitor lizard, Varanus Albigularis. J. therm. Biol. 1, 189-193. Lovegrove B. G. (1989) The cost of burrowing by the social mole rat (Bathyergidea) Cryptomys demarensis and Heterocephalus glaber: the role of soil moisture. Physiol. Zool. 62, 449-469, Lyman C. P. (1981) Who and who among the hibernators. In Hibernation and Torpor in Mammals and Birds (Edited by Lyman C. P., Willis J. S., Malan A. and Wang L. C. H.), pp. 12-36. Academic Press, New York. McNab B. K. (1986) The metabolism of fossorial rodents: A study of convergence. Ecology 47, 712-733. McNab B. K. (1979) On estimating thermal conductance in endotherms. Physiol. Zool. 53, 145-156. McNab B. K. (1983) Energetics, body size and the limits to endothermy. J. Zool. Lond. 199, 1 29.
Nevo E. (1979) Adaptive convergence and divergence of subterranean mammals. A. Rev. ecol. Svst. 10, 269-308. Pearson O. (1948) Metabolism of small mammals, with remarks on the lower limit of mammalian size. Science 108, 44. Schmidt-Nielsen K. (1983) Temperature regulation. In Animal Physiology: Adaptation and Environment (Edited by Schmidt-Nielsen K.), pp. 249 308. Cambridge University Press, Cambridge. Scholander P. F., Hock R., Walters, V., Johnson F. and Irving L. (1950) Heat regulation in some arctic tropical mammals birds. Biol. Bull. 9, 237 258. Seagrave R. C. (1971) Heat transfer in living systems. In Biomedical Applications (~1"Heat and Mass Transfer (Edited by Seagrave R. C.), pp. 93 113. Iowa State University Press, Iowa. Tracy C. R. (1977) Minimum size of mammalian homeotherms: role of the thermal environment. Science 198, 1034 1035. Tucker R. (1981) The digging behavior and skin differentiations in Heterocephalus glaber. J. Morphol. 168, 51 71, Withers P. C. and Jarvis J. U. M. (1980) The effect of huddling on thermoregulation and oxygen consumption for the naked mole-rat. Comp. Biochem. Physiol. ¢~A, 215-219. Vleck D. (1981) Burrow structure and foraging costs in the fossorial rodent, Thomomys bottae. Oecologia 49, 391-396. Yahav S. and Buffenstein R. (1991) Huddling behaviour facilitates homeotherapy in Heterocephalus glaber. Physiol. Zool. In press. Zar J. H. (1974) Biostatistical Analysis. Prentice-Hall, Englewood Cliffs, N.J.