Abstract
Body temperature, oxygen consumption, respiratory and cardiac activity and body mass loss were measured in six females and four males of the subterranean Zambian mole rat Cryptomys sp. (karyotype 2 n=68), at ambient temperatures between 10 and 35°C. Mean body temperature ranged between 36.1 and 33.2°C at ambient temperatures of 32.5–10°C and was lower in females (32.7°C) than in males (33.9°C) at ambient temperatures of 10°C but dit not differ at thermoneutrality (32.5°C). Except for body temperature, mean values of all other parameters were lowest at thermoneutrality. Mean basal oxygen consumption of 0.76 ml O2·g-1· h-1 was significantly lower than expected according to allometric equations and was different in the two sexes (females: 0.82 ml O2·g-1·h-1, males: 0.68 ml O2·g1·h-1) but was not correlated with body mass within the sexes. Basal respiratory rate of 74·min-1 (females: 66·min1, males: 87·min-1) and basal heart rate of 200·min-1 (females: 190·min-1, males: 216·min-1) were almost 30% lower than predicted, and the calculated thermal conductance of 0.144 ml O2·g-1·h1·°C-1 (females; 0.153 ml O2·g-1·h-1·°C-1, males: 0.131 ml O2·g-1·h-1·°C-1) was significantly higher than expected. The body mass loss in resting mole rats of 8.6–14.1%·day-1 was high and in percentages higher in females than in males. Oxygen consumption and body mass loss as well as respiratory and cardiac activity increased at higher and lower than thermoneutral temperatures. The regulatory increase in O2 demand below thermoneutrality was mainly saturated by increasing tidal volume but at ambient temperatures <15°C, the additional oxygen consumption was regulated by increasing frequency with slightly decreasing tidal volume. Likewise, the additional blood transport capacity was mainly effected by an increasing stroke volume while there was only a slight increase of heart frequency. In an additional field study, temperatures and humidity in different burrow systems have been determined and compared to environmental conditions above ground. Constant temperatures in the nest area 70 cm below ground between 26 and 28°C facilitate low resting metabolic rates, and high relative humidity minimizes evaporative water loss but both cause thermoregulatory problems such as overheating while digging. In 13–16 cm deep foraging tunnels, temperature fluctuations were higher following the above ground fluctuations with a time lag. Dominant breeding females had remarkably low body temperatures of 31.5–32.3°C at ambient temperatures of 20°C and appeared to be torpid. This reversible hypothermy and particular social structure involving division of labour are discussed as a strategy reducing energy expenditure in these eusocial subterranean animals with high foraging costs.
Similar content being viewed by others
Abbreviations
- BMR:
-
basal metabolic rate
- br:
-
breath
- C :
-
thermal conductance
- HR:
-
neart rate
- LD:
-
light/dark
- M b :
-
body mass
- MR:
-
metabolic rate
- OP:
-
oxygen pulse
- PCO2 :
-
partial pressure of carbon dioxide
- PO2 :
-
partial pressure of oxygen
- RMR:
-
resting metabolic rate
- RR:
-
respiratory rate
- T a :
-
ambient temperature
- T b :
-
body temperature
- TNZ:
-
thermal neural zone
- \(\dot V\)O2 :
-
oxygen consumption
References
Arieli R (1979) The atmospheric environment of the fossorial mole rat (Spalax ehrenbergi): effects of season, soil texture, rain, temperature and activity. Comp Biochem Physiol 63A:569–575
Arieli R, Ar A (1979) Ventilation of a fossorial mammal, (Spalax ehrenbergi) in hypoxic and hypercapnic conditions. J Appl Physiol 47:1011–1017
Arieli R, Ar A (1981) Heart rate responses of the mole rat (Spalax ehrenbergi) in hypercapnic, hypoxic and cold conditions. Physiol Zool 54:14–21
Aschoff J (1981) Der Tagesgang der Körpertemperatur und der Sauerstoffaufnahme bei Säugetieren als Funktion des Körpergewichts. Z Säugetierkunde 46:201–216
Bartholomew GA, Tucker VA (1963) Control of changes in body temperature, metabolism, and circulation by the agamid lizard, Amphibolurus barbatus. Physiol Zool 36:199–218
Bennett NC Jarvis JUM, Cotterill FPD (1993a) Poikilothermic traits and thermoregulation in the afrotropical social subterranean Mashona mole-rat (Cryptomys hottentotus darlingi) Rodentia: Bathyergidae. J Zool (London) 231:179–186
Bennett NC, Taylor PJ, Aguilar GH (1993b) Thermoregulation and metabolic acclimation in the Natal mole-rat (Cryptomys hottentotus natalensis) (Rodentia: Bathyergidae). Z Säugetierkunde 58:362–367
Blake CJ, Banchero N (1985) Effects of cold and hypoxia on ventilation and oxygen consumption in awake guinea pigs. Respir Physiol 61:357–368
Boggs DF, Kilgore DL, Birchard GF (1984) Respiratory physiology of burrowing mammals and birds. Comp Biochem Physiol 77A:1–7
Bozinovic F, Rosenmann M (1988) Comparativ energetics of South American Cricetid rodents. Comp Biochem Physiol 91A:195–202
Bradley SR, Deavers DR (1980) A re-examination of the relationship between thermal conductance and body weight in mammals. Comp Biochem Physiol 65A:465–476
Brett RA (1991) The ecology of naked mole-rat colonies: Burrowing, food, and limiting factors. In: Sherman PW et al. (eds) The biology of the naked mole-rat. Princeton University Press, New Jersey, pp 137–184
Buffenstein R (1984) The importance of microhabitat in thermoregulation and thermal conductance in two Namib rodents — a crevice dweller Aethomys namaquensis, and a burrow dweller, Gerbillurus paeba. J Therm Biol 9:235–241
Burda H (1989) Reproductive biology (behaviour, breeding, and postnatal development) in subterranean mole-rats, Cryptomys hottentotus (Bathyergidae). Z Säugetierkunde 54:360–376
Burda H, Filippucci G, Macholan M, Nevo E, Zima J (1992) Biological, allozyme, and karyotype differentiation of African mole-rats (Cryptomys, Bathyergidae) from Zambia. Z Säugetierkunde [Suppl] 57:11–12
Burda H, Kawalika M (1993) Evolution of eusociality in the Bathyergidae: the case of the giant mole-rats (Cryptomys mechowi) Naturwissenschaften 80:235–237
Chapell A (1992) Ventilatory accommodation of changing oxygen demand in sciurid rodents. J Comp Physiol B 162:722–730
Contreras LC, McNab BK (1990) Thermoregulation and energetics in subterranean mammals. In: Nevo E, Reig OA (eds) Evolution of subterranean mammals at the organismal and molecular levels. Allen R. Liss, New York, pp 231–250
Depocas F, Hart JS, Heroux O (1957) Use of the Pauling oxygen analyzer for measurement of oxygen consumption in open circuit systems and in a short-lag, closed-circuit apparatus. J Appl Physiol 10:388–392
Drorbaugh JE, Fenn WO (1955) A barometric method for measuring ventilation in newborn infants. Pediatrics 16:81–87
Du Toit JT, Javis JUM, Louw GN (1985) Nutrition and burrowing energetics of the Cape mole-rat Georychus capensis Oecologia 66:82–87
Edoute Y, Arieli R, Nevo E (1988) Evidence for improved myocardial oxygen delivery and function during hypoxia in the mole rat. J Comp Physiol B 158:575–582
Epstein MAF, Epstein RA (1978) A theoretical analysis of the barometric method for measurement of tidal volume. Respir Physiol 32:105–120
Filippucci MG, Burda H, Nevo E, Kocka J (1994) Allozyme divergence and systematics of common mole-rats (Cryptomys, Bathyergidae, Rodentia) from Zambia. Z Säugetierkunde 59:42–51
Gordon CJ, Long MD (1984) Ventilatory frequency of mouse and hamster during microwave-induced heat exposure. Respir Physiol 56:81–90
Haim A, Fairall N (1986) Physiological adaptations to the subterranean environment by the mole rat Cryptomys hottentotus. Cimbebasia 8A:49–53
Hayssen V, Lacy RC (1985) Basal metabolic rate in mammals: taxonomic differences in the allometry of BMR and body mass. Comp Biochem Physiol 81A:741–754
Heldmaier G, Ruf T (1992) Body temperature and metabolic rate during natural hypothermia in endotherms. J Comp Physiol B 162:696–706
Herreid CF, Kessel B (1967) Thermal conductance in birds and mammals. Comp Biochem Physiol 81A:741–754
Jarvis JUM (1978) Energetics of survival in Heterocephalus glaber (Rüppell), the naked mole-rat (Rodentia: Bathyergidae). Bull Carnegie Mus Nat Hist 6:81–87
Kennerly TE (1964) Microenvironmental conditions of the pocket gopher burrow. Texas J Sci 16:395–441
Kleiber M (1961) The fire of life. Wiley, New York
Lovegrove BG (1989) The cost of burrowing by the social mole-rat (Bathyergidae) Cryptomys damarensis and Heterocephalus glaber. The role of soil moisture. Physiol Zool 62:449–469
Lovegrove BG (1991) The evolution of eusociality in mole-rats (Bathyergidae): a question of risks, numbers, and costs. Behav Ecol Sociobiol 28:37–45
Lovegrove BG, Jarvis JUM (1986) Coevolution between mole-rats (Bathyergidae) and a geophyte, Micranthus (Iridaceae). Cimbebasia 8A:79–85
Malan A (1973) Ventilation measured by body plethysmography in hibernating mammals and in poikilotherms. Respir Physiol 17:32–44
Marhold S, Nagel A (1989) Stoffwechsel, Atem- und Herztätigkeit des afrikanischen Graumulls Cryptomys hottentotus (Lesson, 1826) (Rodentia, Bathyergidae). Z Säugetierkunde [Suppl] 54:30
McNab BK (1966) The metabolism of fossorial rodents: a study of convergence. Ecology 47:712–733
McNab BK (1970) Body weight and the energetics of temperature regulation. J Exp Biol 53:329–348
McNab BK (1979) Climatic adaptations in the energetics of heteromyid rodents. Comp Biochem Physiol 62A:813–820
McNab BK (1980) On estimating thermal conductance in endotherms. Physiol Zool 53:145–156
McNab BK (1987) Basal rate and phylogeny. Funct Ecol 1:159–167
Müller EF, Rost H (1983) Respiratory frequency, total evaporative water loss and heart rate in the Kinkajou Potos flavus [Schreiber]. Z Säugetierkunde 48:217–226
Nagel A (1986) The electrocardiogram (EKG) of European shrews. Comp Biochem Physiol 83A:791–794
Nagel A (1991) Metabolic, respiratory and cardiac activity in the shrew Crocidura russula. Respir Physiol 85:139–149
Nevo E (1979) Adaptive convergence and divergence of subterranean mammals. Annu Rev Ecol Syst 10:269–308
Nevo E (1991) Evolutionary theory and processes of active speciation and adaptive radiation in subterrancan mole rats, Spalax ehrenbergi superspecies, in Israel. Evolut Biol 25:1–125
Prinzinger R (1988) Energy metabolism, body-temperature and breathing parameters in nontorpoid blue-naped mousebirds Urocolius macrourus. J Comp Physiol B 157:801–806
Stahl WR (1967) Scaling of respiratory variables in mammals. J Appl Physiol 22:453–460
Vleck D (1979) The energy cost of burrowing by the pocket gopher Thomomys bottae. Physiol Zool 52:122–135
Vleck D (1981) Burrow structure and foraging cost in the fossorial rodent Thomomys bottae. Oecologia 49:391–396
Wang LC, Hudson JW (1971) Temperature regulation in normothermic and hibernating eastern chipmuk Tamias striatus. Comp Biochem Physiol 38A:59–90
Williams GJ (1984) The environment. Climatological summaries for Zambia, 1971. Meteorological Dept, occasional study No 12. Geographical Association, Lusaka, Zambia, pp 11–18
Wilson KJ, Kilgore DL (1978) The effects of location and disign on the diffusion of respiratory gases in mammal burrows. J Theor Biol 71:73–101
Withers PC (1978) Models of diffusion mediated gas exchange in animal burrows. Am Nat 112:1101–1112
Withers PC, Jarvis JUM (1980) The effect of huddling on thermoregulation and oxygen consumption for the naked mole-rat. Comp Biochem Physiol 66A:215–219
Withers PC, Lee AK, Martin RW (1979) Metabolism, respiration and evaporative water loss in the Australien hopping-mouse Notomys alexis (Rodentia: Muridae) Aust J Zool 27:195–204
Yahav S, Buffenstein R, Jarvis JUM, Mitchell D (1989) Thermoregulation and evaporative water loss in the naked mole-rat, Heterocephalus glaber. S Afr J Sci 85:340
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Marhold, S., Nagel, A. The energetics of the common mole rat Cryptomyś, a subterranean eusocial rodent from Zambia. J Comp Physiol B 164, 636–645 (1995). https://doi.org/10.1007/BF00389805
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00389805