Noradrenalin induces thermogenesis in a phylogenetically ancient eutherian mammal, the rock elephant shrew, Elephantulus myurus

Journal of Comparative Physiology B: Biochemical, Systemic, and Environmental Physiology

Volumn 176, Issue 1, 2006, Pages 75-84

  Mzilikazi, Nomakwezi ^a,b   Lovegrove, Barry G ^b  

^a NELSON MANDELA METROPOLITAN UNIVERSITY   (South Africa)

^b UNIVERSITY OF KWAZULU NATAL   (South Africa)

Author keywords

Afrotheria; Brown adipose tissue; Elephantulus; Exogenous passive heating; Nonshivering thermogenesis; Uncoupling proteins

Indexed keywords

NORADRENALIN;

ANIMAL; ARTICLE; DRUG EFFECT; GENETICS; OXYGEN CONSUMPTION; PHYLOGENY; PHYSIOLOGY; SHREW; THERMOGENESIS;

ANIMALS; NOREPINEPHRINE; OXYGEN CONSUMPTION; PHYLOGENY; SHREWS; THERMOGENESIS;

ELEPHANTULUS; ELEPHANTULUS MYURUS; EUTHERIA; MAMMALIA; METATHERIA; SORICIDAE;

EID: 28844439374     PISSN: 01741578     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00360-005-0035-x     Document Type: Article

References (86)

1. Böckler H, Steinlechner S, Heldmaier G (1982) Complete cold substitution of noradrenaline-induced thermogenesis in the Djungarian hamster, Phodopus sungorus. Experiment 38:261-262
2. Cannon B, Nedergaard J (2004) Brown adipose tissue: function and physiological significance. Physiol Rev 84:277-359
3. Cannon B, Nedergaard J (1985) The biochemistry of an inefficient tissue: brown adipose tissue. Essays Biochem 20:110-164
4. Cannon B, Golozoubova V, Matthias A, Ohlson K, Jacobsson A, Nedergaard J (2000) Is there life in the cold without UCP1? Uncoupling proteins and thermoregulatory thermogenesis. In: Heldmaier G, Klingenspor M (eds) Life in the cold: 11th international hibernation symposium. Springer, Berlin, pp 387-400
5. Catzeflis FM, Hänni C, Sourrouille P, Douzery E (1995) Molecular systematics of hystricognath rodents: the contribution of sciurognath mitochondrial 12S rRNA sequences. Mol Phylogenet Evol 4:357-360
6. Corbet GB, Hill JE (1991) A world list of mammalian species. Oxford University Press, Oxford
7. Dausmann K, Glos J, Ganzhorn JU, Heldmaier G (2004) Hibernation in a tropical primate. Nature 429:825-826
8. Dew EM, Carson KA, Rose RK (1998). Seasonal changes in brown fat and pelage in southern short-tailed shrews. J Mammal 79:271-278
9. Downs CT, Perrin MR (1991) Physiological adjustments to low temperatures of for Gerbillurus species. J therm Biol 16:25-29
10. Feist DD, Feist CF (1986) Effects of cold, short day and melatonin on thermogenesis, body weight and reproductive organs in Alaskan red-backed voles. J Comp Physiol B 156:741-746
11. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1-15
12. Filippucci M, Macholán M, Michaux J (2002) Genetic variation and evolution in the genus Apodemus (Muridae: Rodentia). Biol J Linn Soc 75:395-419
13. Garland T, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18-32
14. Geiser F, Goodship N, Pavey CR (2002) Was basking important in the evolution of mammalian endothermy? Naturwiss 89:412-414
15. Geiser F, Drury RL (2003) Radient heat affects thermoregulation and energy expenditure during rewarming from torpor. J Comp Physiol B 173:55-60
16. Geiser F, Drury RL, Körtner G, Turbill C, Pavey C R, Brigham M (2004) Passive rewarming from torpor in mammals and birds: energetic, ecological and evolutionary implications. In: Barnes BM, Carey H (eds) Life in the cold: evolution, mechanisms, adaptation and application. Twelfth international hibernation symposium. Institute of Arctic Biology, University of Alaska, Fairbanks, Alaska, pp 51-62
17. Gettinger R, Ralph C (1985) Thermoregulatory responses to photoperiod by kangaroo rats (Dipodomys ordii): influence of night lighting on non-shivering thermogenesis and resting metabolism. J Exp Zool 234:335-340
18. Grafen A (1989) The phylogenetic regression. Philos Trans R Soc Lond 326B:119-157
19. Haim A, Fourie le R (1980) Heat production in cold and long scotophase acclimated and winter acclimatized rodents. Int J Biometeorol 24:231-236
20. Haim A, Borut A (1981) Heat production and dissipation in Golden spiny Mice, Acomys russatus from two extreme habitats. J Comp Physiol 142:445-450
21. Haim A, Yahav S (1982) Non-shivering thermogenesis in winter-acclimatized and in long-scotophase and cold acclimated Apodemus mystacinus (Rodentia). J therm Biol 7:193-195
22. Haim A (1984) Adaptive variations in heat production within gerbils (genus Gerbillus) from different habitats. Oecologia 61:49-52
23. Haim A, Heth G, Avnon Z, Nevo E (1984) Adaptive physiological variation in non-shivering thermogenesis and its significance in speciation. J Comp Physiol B 154:145-147
24. Haim A, Fairall N (1986) Physiological adaptations to the subterranean environment by the mole rat Cryptomys hottentotus. Cimbebasia 8:49-53
25. Haim A, Levi G (1990) Role of body temperature in seasonal acclimatization: photoperiod-induced rhythms and heat production in Meriones crassus. J Exp Zool 256:237-241
26. Haim A, Izhaki I (1993) The ecological significance of resting metabolic rate and non-shivering thermogenesis for rodents. J therm Biol 18:71-81
27. Haim A, Racey PA, Speakman JR, Ellison GTH, Skinner JD (1991) Seasonal acclimation and thermoregulation in the pouched mouse Saccostomus camprestris. J therm Biol 16:13-17
28. Haim A, Izhaki I (1995) Comparative physiology of thermoregulation in rodents: Adaptations to arid and mesic environments. J Arid Environ 31:431-440
29. Haim A, McDevitt RM, Speakman JR (1995) Daily Variations in the response of wood mice Apodemus sylvaticus to noradrenaline. J Exp Biol 198:561-565
30. Haim A (1996) Food and energy intake, non-shivering thermogenesis and daily rhythm of body temperature in the bushy-tailed gerbil Sekeetamys calurus: the role of photoperiod manipulations. J Therm Biol 21:37-42
31. Haim A, Shabtay A, Arad Z (1998) Thermoregulatory responses of mesic and xeric rodent species to photoperiod manipulations. Comp Biochem Physiol A 120:187-191
32. Hayes JP, Garland T (1995) The evolution of endothermy: testing the aerobic capacity model. Evol 49:836-847
33. Heldmaier G, Steinlechner S (1981) Seasonal control of energy requirements for thermoregulation in the Djungarian Hamster (Phodopus sungorus), living in natural photoperiod. J Comp Physiol B 142:429-437
34. Heldmaier G, Steinlechner S, Rafael J, Vsiansky P (1981) Photoperiodic control and effects of melatonin on non-shivering thermogenesis and brown adipose tissue. Science 212:917-919
35. Heldmaier G, Steinlechner S, Rafael J (1982) Non-shivering thermogenesis and cold resistance during seasonal acclimitization in the Djungarian Hamster. J Comp Physiol B 149:1-9
36. Heldmaier G, Böckler H, Buchberger A, Lynch GR, Puchalski W, Steinlechner S, Wiesinger H (1985) Seasonal acclimation and thermogenesis. In: Gilles R (eds) Circulation, respiration and metabolism. Springer-Verlag, Berlin, pp 490-501
37. Heldmaier G, Klaus S, Wiesinger H (1990) Seasonal adaptation of thermoregulatory heat production in small mammals. In: Bligh J, Voigt K (eds) Thermoreception and temperature regulation. Springer-Verlag, Berlin, pp 235-243
38. Hislop M, Buffenstein R (1994) Noradrenalin induces non-shivering thermogenesis in both the naked mole-rat (Heterocephalus glaber) and the damara mole-rat (Cryptomys damarensis) despite very different modes of thermoregulation. J Therm Biol 19:25-32
39. Holloway JC, Geiser F (2001) Seasonal changes in the thermoenergetics of the marsupial sugar glider, Petaurus breviceps. J Comp Physiol B 171:643-650
40. Hope PJ, Pyle D, Daniels C, Chapman I, Horowitz M, Morley J, Trayhurn P, Kumaratilake J, Wittert G (1997) Identification of brown fat and mechanisms for energy balance in the marsupial, Sminthopsis crassicaudata. Am J Physiol Regul Integr Comp Physiol 273:R161-R167
41. Huchon D, Douzery E (2001) From the old world to the new world: a molecular chronicle of the phylogeny and biogeography of hystricognath rodents. Mol Phylogenet Evol 20:238-251
42. Jansky L (1973) Non-shivering thermogenesis and its thermoregulatory significance. Biol Rev 48:85-132
43. Klaus S, Heldmaier G, Ricquier D (1988) Seasonal acclimation of bank voles and wood mice: non-shivering thermogenesis and thermogenic properties of brown adipose tissue mitochondria. J Comp Physiol B 158:157-164
44. Kronfeld-Schor N, Haim A, Dayan T, Zisapel N, Klingenspor M, Heldmaier G (2000) Seasonal thermogenic acclimation of diurnally and nocturnally active desert spiny mice. Physiol Biochem Zool 73:37-44
45. Lovegrove BG, Heldmaier G, Knight M (1991) Seasonal and circadian energetic patterns in an arboreal rodent, Thallomys paedulcus, and burrow-dwelling rodent, Aethomys namaquensis, from the Kalahari desert. J therm Biol 16:199-209
46. Lovegrove BG, Körtner G, Geiser F (1999a) The energetic cost of arousal from torpor in the marsupial Sminthopsis macroura: benefits of summer ambient temperature cycles. J Comp Physiol B 169:11-18
47. Lovegrove BG, Lawes MJ, Roxburgh L (1999b) Confirmation of pleisiomorphic daily torpor in mammals: the round-eared elephant shrew Maroscelides proboscideus (Macroscelidea). J Comp Physiol B 169:453-460
48. Lovegrove BG, Raman J, Perrin MR (2001a) Daily torpor in elephant shrews (Macroscelidea: Elephantulus sp.) in response to food deprivation. J Comp Physiol B 171:11-21
49. Lovegrove BG, Raman J, Perrin MR (2001b) Heterothermy in elephant shrews (Elephantulus spp.): hibernation or daily torpor? J Comp Physiol B 171:1-10
50. Lyman CP, Willis JS, Malan A, Wang LCH (1982) Hibernation and torpor in mammals and birds. Academic Press, New York
51. Lyman CP, O'Brien RC (1986) Is brown fat necessary? In: Heller HC, Mussachia XJ, Wang LCH (eds) Living in the cold. Elsevier, New York, pp 109-116
52. Lynch GR, White S, Grundel R, Berger M (1978) Effects of photoperiod, melatonin administration and thyroid block on spontaneous daily torpor and temperature regulation in the white-footed mouse, Peromyscus leucopus. J Comp Physiol B 125:157-163
53. Maier H, Feist D (1991) Thermoregulation, growth and reproduction in Alaskan collared lemmings: role of short day and cold. Am J Physiol 261:R522-R530
54. Malan A (1996) The origins of hibernation: a reappraisal. In: Geiser F, Hulbert AJ, Nicol SC (eds) Adaptations to the cold: tenth international hibernation symposium. University of New England Press, Armidale, pp 1-6
55. Martin Y, Gerlach G, Schlötterer C, Meyer A (2000) Molecular phylogeny of European muriod rodents based on complete cytochrome b sequences. Mol Phylogenet Evol 16:37-47
56. McDevitt R, Speakman J (1996) Summer acclimatization in the short-tailed field vole, Microtus agrestis. J Comp Physiol B 166:286-293
57. McNab BK (1978) The evolution of endothermy in the phylogeny of mammals. Am Nat 112(983):1-21
58. Merritt JF (1986) Winter survival adaptations of the short-tailed shrew, Blarina brevicauda in an apalachian montane forest. J Mammal 67:450-464
59. Merritt JF (1995) Seasonal thermogenesis and changes in body mass of masked shrews, Sorex cinereus. J Mammal 76:1020-1035
60. Michaux J, Catzeflis F (2000) The bushlike radiation of muroid rodents is exemplified by the molecular phylogeny of the LCAT nuclear gene. Mol Phylogenet Evol 17:280-293
61. Moshkin M, Novikov E, Petrovski D (2001) Seasonal changes of thermoregulation in the mole vole Ellobius talpinus. Physiol Biochem Zool 74:869-875
62. Murphy WJ, Elzirik E, Johnson WE, Ryder OA, O'Brien JO (2001) Molecular phylogenetics and the origins of placental mammals. Nature 409:614-618
63. Mzilikazi N, Lovegrove BG, Ribble D (2002) Exogenous passive heating during torpor arousal in free-ranging rock elephant shrews, Elephantulus myurus. Oecologia 133:307-314
64. Mzilikazi N, Lovegrove BG (2004) Daily torpor in free-ranging rock elephant shrews, Elephantulus myurus: a year-long study. Physiol Biochem Zool 77:285-296
65. Mzilikazi N, Lovegrove BG (in press) Daily torpor during the active phase in free-ranging rock elephant shrews, Elephantulus myurus. J Zool (Lond)
66. Nedergaard J, Cannon B (1984) Preferential utilization of brown adipose tissue lipids during arousal from hibernation in hamsters. Am J Physiol Regul Integr Comp Physiol 247:R506-R512
67. Nespolo RF, Opazo J, Rosenmann M, Bozinovic F (1999) Thermal acclimation, amximum metabolic rate and non-shivering thermogenesis of Phylottis xanthopygus (Rodentia) in the Andes mountains. J Mammal 80:742-748
68. Nespolo R, Bacigalupe L, Rezende E, Bozinovic F (2001) When non-shivering thermogenesis equals maximum metabolic rate: thermal acclimation and phenotypic plasticity of fossorial Spalacopus cyanus (Rodentia). Physiol Biochem Zool 74:325-332
69. Nicol S, Pavlides, Andersen N (1997) Non-shivering thermogenesis in marsupials: absence of thermogenic response to β3-adrenergic agonists. Comp Biochem Physiol A 117:399-405
70. Ortmann S, Schmid J, Ganzhorn JU, Heldmaier G (1996) Body temperature and torpor in a Malagasy small primate, the mouse lemur. In: Geiser F, Hulbert AJ, Nicol SC (eds) Adaptations to the cold: tenth international hibernation symposium. University of New England Press, Armidale, pp 55-61
71. Pagel M (1992) A method for the analysis of comparative data. J Theor Biol 156:431-442
72. Rose RW, West AK, Ye J, McCormack GH, Colquhoun EQ (1999) Non-shivering thermogenesis in a marsupial (the Tasmanian bettong Bettongia gaimardi) is not attributable to brown adipose tissue. Physiol Biochem Zool 72:699-705
73. Ruedi M (1998) Protein evolution in shrews. In: Wójcik J, Wolsan M (eds) Evolution of shrews. Mammal Research Institute, Polish Academy of Sciences, Bialowieza, pp 269-294
74. Ruf T, Klingenspor M, Preis H, Heldmaier G (1991) Daily torpor in the Djungarian hamster (Phodopus sungorus): interactions with food intake, activity and social behaviour. J Comp Physiol B 160:609-615
75. Ruf T, Heldmaier G (1992) The impact of daily torpor on energy requirements in the Djungarian hamster, Phodopus sungorus. Physiol Zool 65:994-1010
76. Saarela S, Hissa R (1993) Metabolism, thermogenesis and daily rhythm of body temperature in the wood lemming, Myopus schisticolor. J Comp Physiol 163B:546-555
77. Schmid J (2000) Daily torpor in the gray mouse lemur (Microcebus murinus) in Madagascar: energetic consequences and biological significance. Oecologia 123:175-183
78. Sparti A (1992) Thermogenic capacity of shrews (Mammalia, Soricidae) and its relationship with basal rate of metabolism. Physiol Zool 65:77-96
79. Springer MS, Cleven GC, Madsen O, de Jong WW, Waddell VG, Amrine HM, Stanhope MJ (1997) Endemic African mammals shake the phylogenetic tree. Nature 388:61-64
80. Steinlechner S, Heldmaier G (1982) The role of photoperiod and melatonin in seasonal acclimatization of the Djungarian hamster, Phodopus sungorus. Int J Biometeor 26:329-337
81. Turbill C, Law BS, Geiser F (2003) Summer torpor in a free-ranging bat from subtropical Australia. J Therm Biol 28:223-226
82. Wang D, Sun R, Wang Z, Liu J (1999) Effects of temperature and photoperiod on the thermogenesis in plateau pikas (Ochotona curzoniae) and root voles (Microtus oeconomus). J Comp Physiol B 169:77-83
83. Watts C, Baverstock P (1995) Evolution in some African murinae (Rodentia) assessed by microcomplement fixation of albumin. J Afr Zool 109:423-433
84. Wilson DE, Reeder DM (1993) Mammal species of the world. Smithsonian Institution Press, WA
85. Wunder BA, Gettinger RD (1996) Effects of body mass and temperature acclimation on the non-shivering thermogenic response of small mammals. In: Geiser F, Hulbert AJ, Nicol SC (eds) Adaptations to the cold: tenth international hibernation symposium. University of New England Press, Armidale, pp 131-139
86. Zegers D, Merrit J (1988) Effect of photoperiod and ambient temperature on non-shivering thermogenesis of Peromyscus maniculatus. Acta Theriol 33:273-281