Solar radiation during rewarming from torpor in elephant shrews: Supplementation or substitution of endogenous heat production?

PLoS ONE

Volumn 10, Issue 4, 2015, Pages

  Thompson, Michelle L ^a   Mzilikazi, Nomakwezi ^a   Bennett, Nigel C ^a   McKechnie, Andrew E ^a  

^a UNIVERSITY OF PRETORIA   (South Africa)

Author keywords

[No Author keywords available]

Indexed keywords

AIR TEMPERATURE; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ARTICLE; BASAL METABOLIC RATE; BODY TEMPERATURE; CONTROLLED STUDY; ELEPHANT SHREW; ELEPHANTULUS MYURUS; FEMALE; FOOD AVAILABILITY; HEAT ACCLIMATIZATION; MALE; METABOLIC PARAMETERS; NONHUMAN; PHENOTYPE; PREDATION RISK; PREDICTION; SOLAR RADIATION; SPECIES HABITAT; SUMMIT METABOLISM; THERMOGENESIS; TORPOR; WARMING; ANIMAL; METABOLISM; PHYSIOLOGY; RADIATION RESPONSE; SHREW; SOLAR ENERGY;

ELEPHANTULUS MYURUS; MAMMALIA; SORICIDAE;

ANIMALS; BASAL METABOLISM; FEMALE; MALE; PHENOTYPE; SHREWS; SOLAR ENERGY; THERMOGENESIS; TORPOR;

EID: 84929493029     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0120442     Document Type: Article

References (48)

1. Geiser F. Metabolic rate and body temperature reduction during daily torpor. Ann Rev Physiol. 2004; 66: 239-74. PMID: 14977403
2. Ruf T, Heldmaier G. The impact of daily torpor on energy requirements in the djungarian hamster, Phodopus sungorus. Physiol Zool. 1992; 65:994-1010.
3. Mzilikazi N, Lovegrove BG, Ribble DO. Exogenous passive heating during torpor arousal in freeranging rock elephant shrews, Elephantulus myurus. Oecologia. 2002; 133:307-14.
4. Tucker VA. Oxygen consumption, thermal conductance, and torpor in the California pocket mouse, Perognathus californicus. J Cell Comp Physiol. 1965; 65: 393-404.
5. Wang LCH. Time patterns and metabolic rates of natural torpor in the Richardson's ground squirrel. Can J Zool. 1979; 57: 149-55.
6. Thomas DW, Dorais M, Bergeron J-M. Winter energy budgets and cost of arousals for hibernating little brown bats, Myotis lucifugus. J Mamm. 1990; 71: 475-9.
7. Lovegrove BG, Körtner G, Geiser F. The energetic cost of arousal from torpor in the marsupial Sminthopsis macroura: benefits of summer ambient temperature cycles. J Comp Physiol B. 1999; 169: 11-8. PMID: 10093903
8. Geiser F, Goodship N, Pavey CR. Was basking important in the evolution of mammalian endothermy? Naturwissenschaften. 2002; 89: 412-4. PMID: 12435094
9. Geiser F, Pavey C. Basking and torpor in a rock-dwelling desert maruspial: survival strategies in a resource-poor environment. J Comp Physiol B. 2007; 177: 885-92. PMID: 17674010
10. Warnecke L, Turner JM, Geiser F. Torpor and basking in a small arid zone marsupial. Naturwissenschaften. 2008; 95: 73-8. PMID: 17684718
11. McKechnie AE, Wolf BO. Solar radiation and the energetic cost of rewarming from torpor. In: Barnes BM, Carey HV, editors. Life in the cold: evolution, mechanisms, adaptation and application 12th International Hibernation Symposium; 2004. p. 63-70.
12. Geiser F, Drury RL. Radiant heat affects thermoregulation and energy expenditure during rewarming from torpor. J Comp Physiol B. 2003; 173: 55-60. PMID: 12592443
13. Warnecke L, Geiser F. The energetics of basking behaviour and torpor in a small marsupial exposed to simulated natural conditions. J Comp Physiol B. 2010; 180: 437-45. doi: 10.1007/s00360-009-0417-6 PMID: 19888581
14. Rezende EL, Hammond KA, Chappell MA. Cold acclimation in Peromyscus: individual variation and sex effects in maximum and daily metabolism, organ mass and body composition. J Exp Biol. 2009; 212: 2795-802. doi: 10.1242/jeb.032789 PMID: 19684213
15. Nespolo RF, Opazo JC, Bozinovic F. Thermal acclimation and non-shivering thermogenesis in three species of South American rodents: a comparison between arid and mesic habitats. J Arid Environ. 2001; 48(4): 581-90.
16. Nespolo RF, Opazo JC, Rosenmann M, Bozinovic F. Thermal acclimation, maximum metabolic rate, and nonshivering thermogenesis of Phyllotis xanthopygus (Rodentia) in the Andes Mountains. J Mamm. 1999; 80(3): 742-8.
17. Lovegrove BG. Seasonal thermoregulatory responses in mammals. J Comp Physiol B. 2005; 175: 231-47. PMID: 15900504
18. Minnaar IA, Bennett NC, Chimimba CT, McKechnie AE. Summit metabolism and metabolic expansibility in Wahlberg's epauletted fruit bats (Epomophorus wahlbergi): seasonal acclimatisation and effects of captivity. J Exp Biol. 2014; 217: 1363-9. doi: 10.1242/jeb.098400 PMID: 24363417
19. Careau V. Basal metabolic rate, maximum thermogenic capacity and aerobic scope in rodents: interaction between environmental temperature and torpor use. Biol Lett. 2013; 9: 20121104. doi: 10.1098/ rsbl.2012.1104 PMID: 23407497
20. Mzilikazi N, Lovegrove BG. Daily torpor in free-ranging rock elephant shrews, Elephantulus myurus: a year-long study. Physiol Biochem Zool. 2004; 77(2): 285-96. PMID: 15095248
21. Cooper CE, Withers PC. Effects of measurement duration on the determination of basal metabolic rate and evaporative water loss of small marsupials: how long is long enough? Physiol Biochem Zool. 2009; 82(5): 438-46. doi: 10.1086/603654 PMID: 19653857
22. Mzilikazi N, Jastroch M, Meye CW, Klingenspor M. The molecular and biochemical basis of nonshivering thermogenesis in an African endemic mammal, Elephantulus myurus. Am J Physiol. 2007; 293: R2120-R7. PMID: 17686883
23. Wunder BA, Gettinger RD. Effects of body mass and temperature acclimation on the non-shivering thermogenic response of small mammals. In: Geiser F, Hulbert AJ, Nicol SC, editors. Adaptations to the cold: Tenth International Hibernation Symposium. Armidale: University of New England Press; 1996.
24. Mzilikazi N, Lovegrove BG. Noradrenalin induces thermogenesis in a phylogenetically ancient eutherian mammal, the rock elephant shrew, Elephantulus myurus. J Comp Physiol B. 2006; 176: 75-84. PMID: 16317548
25. Swanson DL, Drymalski MW, Brown JR. Sliding vs static cold exposure and the measurement of summit metabolism in birds. J Therm Biol. 1996; 21(4): 221-6.
26. Smit B, Boyles JG, Brigham RM, McKechnie AE. Torpor in dark times: patterns of heterothermy are associated with the lunar cycle in a nocturnal bird. J Biol Rhythms. 2011; 26(3): 241-8. doi: 10.1177/ 0748730411402632 PMID: 21628551
27. Barclay RMR, Lausen CL, Hollis L. What's hot and what's not: defining torpor in free-ranging birds and mammals. Can J Zool. 2001; 79(10): 1885-90.
28. Schleucher E, Prinzinger R. Heterothermia and torpor in birds: highly specialized physiological ability or just deep "nocturnal hypothermia"?-The limitations of terminology. Acta Zool Sinica. 2006; 52 (suppl.): 393-6.
29. Willis CKR. An energy-based body temperature threshold between torpor and normothermia for small mammals. Physiol Biochem Zool. 2007; 80(6): 643-51. PMID: 17910000
30. Boyles JG, Smit B, McKechnie AE. A new comparative metric for estimating heterothermy in endotherms. Physiol Biochem Zool. 2011; 84(1): 115-23. doi: 10.1086/656724 PMID: 20979498
31. McKechnie AE, Ashdown RAM, Christian MB, Brigham RM. Torpor in an Afrotropical caprimulgid, the Freckled Nightjar (Caprimulgus tristigma). J Avian Biol. 2007; 38: 261-6.
32. Bates D, Maechler M, Bolker B, Walker S. lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7, http://CRAN.R-project.org/package = lme4. 2014.
33. Genz A, Bretz F, Miwa T, Mi X, Leisch F, Scheipl F, et al. mvtnorm: Multivariate normal and t distributions. R package version 0.9-9991. 2011.
34. Pinheiro J, Bates D, DebRoy S, Sarkar D, RDevelopmentCoreTeam. nlme: Linear and nonlinear mixed effects models. R package version 3.1-94. 2009.
35. Walsberg GE, Wolf BO. Effects of solar radiation and wind speed on metabolic heat production by two mammals with contrasting coat colours. J Exp Biol. 1995; 198: 1499-1507. PMID: 7658187
36. Walsberg GE, Weaver T, Wolf BO. Seasonal adjustment of solar heat gain independent of coat coloration in a desert mammal. Physiol Zool. 1997; 70(2): 150-7. PMID: 9231387
37. Dawson TJ, Webster KN, Maloney SK. The fur of mammals in exposed environments; do crypsis and thermal needs necessarily conflict? The polar bear and marsupial koala compared. J Comp Physiol B. 2014; 184: 273-84. doi: 10.1007/s00360-013-0794-8 PMID: 24366474
38. Cooper CE, Walsberg GE, Withers PC. Biophysical properties of the pelt of a diurnal marsupial, the numbat (Myrmecobius fasciatus), and its role in thermoregulation. J Exp Biol. 2003; 206: 2771-7. PMID: 12847122
39. Walsberg GE. Consequences of skin colour and fur properties for solar heat gain and ultraviolet irradiance in two mammals. J Comp Physiol B. 1988; 158: 213-21. PMID: 3170827
40. Marom S, Korine C, Wojciechowski M, Tracy CR, Pinshow B. Energy metabolism and evaporative water loss in the European free-tailed bat and Hemprich's long-eared bat (Microchiroptera): species sympatric in the Negev Desert. Physiol Biochem Zool. 2006; 79(5): 944-56. PMID: 16927241
41. Heldmaier G, Steinlechner S, Rafael J, Vsiansky P. Photoperiodic control and effects of melatonin on nonshivering thermogenesis and brown adipose tissue. Science. 1981; 212(4497): 917-9. PMID: 7233183
42. Nespolo RF, Bacigalupe LD, Rezende EL, Bozinovic F. When nonshivering thermogenesis equals maximum metabolic rate: thermal acclimation and phenotypic plasticity of fossorial Spalacopus cyanus (Rodentia). Physiol Biochem Zool. 2001; 74: 325-32. PMID: 11331504
43. Novoa FF, Rivera-Hutinel A, Rosenmann M, Sabat P. Intraspecific differences in metabolic rate of Chroeomys olivaceus (Rodentia: Muridae): the effect of thermal acclimation in arid and mesic habitats. Revista Chilena de Historia Natural. 2005; 78: 207-14.
44. Heldmaier G, Steinlechner S, Ruf T, Weisinger H, Klingenspor M. Photoperiod and thermoregulation in vertebrates: body temperature rhythms and thermogenic acclimation. J Biol Rhythms. 1989; 4.
45. Lovegrove BG, Raman J, Perrin MR. Heterothermy in elephant shrews, Elephantulus spp. (Macroscelidea): daily torpor or hibernation? J Comp Physiol B. 2001; 171: 1-10. PMID: 11263721
46. Heldmaier G, Steinlechner S. Seasonal pattern and energetics of short daily torpor in the Djungarian hamster, Phodopus sungorus. Oecologia. 1981; 48: 265-70.
47. Justo R, Frontera M, Pujol E, Rodríguez-Cuenca S, Lladó I, García-Palmer J, et al. Gender-related differences in morphology and thermogenic capacity of brown adipose tissue mitochondrial subpopulations. Life Sci. 2005; 76(10): 1147-58. PMID: 15620578
48. Hinds DS, Baudinette RV, MacMillen RE, Halpern EA. Maximum metabolism and the aerobic factorial scope of endotherms. J Exp Biol. 1993; 182: 41-56. PMID: 8228784