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Heat dissipation in subterranean rodents: the role of body region and social organisation

. 2021 Jan 21 ; 11 (1) : 2029. [epub] 20210121

Language English Country Great Britain, England Media electronic

Document type Journal Article, Research Support, Non-U.S. Gov't

Grant support
GAJU n. 048/2019/P to F.V. Jihočeská Univerzita v Českých Budějovicích
GUN number 64756 South African Research Chair
GACR 17-19896S Grantová Agentura České Republiky

Links

PubMed 33479351
PubMed Central PMC7820455
DOI 10.1038/s41598-021-81404-3
PII: 10.1038/s41598-021-81404-3
Knihovny.cz E-resources

The relatively warm and very humid environment of burrows presents a challenge for thermoregulation of its mammalian inhabitants. It was found that African mole-rats dissipate body heat mainly through their venter, and social mole-rats dissipate more body heat compared to solitary species at lower temperatures. In addition, the pattern of the ventral surface temperature was suggested to be homogeneous in social mole-rats compared to a heterogeneous pattern in solitary mole-rats. To investigate this for subterranean rodents generally, we measured the surface temperatures of seven species with different degrees of sociality, phylogeny, and climate using infrared thermography. In all species, heat dissipation occurred mainly through the venter and the feet. Whereas the feet dissipated body heat at higher ambient temperatures and conserved it at lower ambient temperatures, the ventral surface temperature was relatively high in all temperatures indicating that heat dissipation to the environment through this body region is regulated mainly by behavioural means. Solitary species dissipated less heat through their dorsum than social species, and a tendency for this pattern was observed for the venter. The pattern of heterogeneity of surface temperature through the venter was not related to sociality of the various species. Our results demonstrate a general pattern of body heat exchange through the three studied body regions in subterranean rodents. Besides, isolated individuals of social species are less able to defend themselves against low ambient temperatures, which may handicap them if staying alone for a longer period, such as during and after dispersal events.

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da Silva RG, Maia ASC. Principles of Animal Biometeorology. Dordrecht: Springer; 2012.

Mohler FS, Heath JE. Comparison of IR thermography and thermocouple measurement of heat-loss from rabbit pinna. Am. J. Physiol. 1988;254:389–395. PubMed

Phillips PK, Heath JE. An infrared thermographic study of surface temperature in the euthermic woodchuck (Marmota monax) Comp. Biochem. Physiol. A. 2001;129:557–562. doi: 10.1016/S1095-6433(01)00294-X. PubMed DOI

Klir JJ, Heath JE. An infrared thermographic study of surface temperature in relation to external thermal stress in three species of foxes: the red fox (Vulpes vulpes), arctic fox (Alopex lagopus), and kit fox (Vulpes macrotis) Physiol. Zool. 1992;65:1011–1021. doi: 10.1086/physzool.65.5.30158555. DOI

Kuhn R, Meyer W. Infrared thermography of the body surface in the Eurasian otter Lutra lutra and the giant otter Pteronura brasiliensis. Aquat. Biol. 2009;6:143–152. doi: 10.3354/ab00176. DOI

Khamas WA, Smodlaka H, Leach-Robinson J, Palmer L. Skin histology and its role in heat dissipation in three pinniped species. Acta Vet. Scand. 2012;54:46. doi: 10.1186/1751-0147-54-46. PubMed DOI PMC

Johansen K. Heat exchange through the muskrat tail. Evidence for vasodilator nerves to the skin. Acta Physiol. Scand. 1962;55:160–169. doi: 10.1111/j.1748-1716.1962.tb02428.x. PubMed DOI

Mauck B, Bilgmann K, Jones DD, Eysel U, Dehnhardt G. Thermal windows on the trunk of hauled-out seals: hot spots for thermoregulatory evaporation? J. Exp. Biol. 2003;206:1727–1738. doi: 10.1242/jeb.00348. PubMed DOI

Underwood LS, Reynolds P. Photoperiod and fur lengths in the Arctic fox (Alopex lagopus L.) Int. J. Biometeorol. 1980;24:39–48. doi: 10.1007/BF02245540. DOI

Korhonen H, Harri M. Heat loss of farmed raccoon dogs and blue foxes as evaluated by infrared thermography and body cooling. Comp. Biochem. Physiol. A. 1986;84:361–364. doi: 10.1016/0300-9629(86)90630-4. PubMed DOI

Reichard JD, Prajapati SI, Austad SN, Keller C, Kunz TH. Thermal windows on Brazilian free-tailed bats facilitate thermoregulation during prolonged flight. Integr. Comp. Biol. 2010;50:358–370. doi: 10.1093/icb/icq033. PubMed DOI PMC

Gerken M. Relationships between integumental characteristics and thermoregulation in South American camelids. Animal. 2010;4:1451–1459. doi: 10.1017/S1751731109991443. PubMed DOI

Abdoun KA, Samara EM, Okab AB, Al-Haidary AA. Regional and circadian variations of sweating rate and body surface temperature in camels (Camelus dromedarius) Anim. Sci. J. 2012;83:556–561. doi: 10.1111/j.1740-0929.2011.00993.x. PubMed DOI

Phillips PK, Heath JE. Dependency of surface temperature regulation on body size in terrestrial mammals. J. Therm. Biol. 1995;20:281–289. doi: 10.1016/0306-4565(94)00061-M. DOI

Contreras LC. Bioenergetics and distribution of fossorial Spalacopus cyanus (Rodentia): thermal stress, or cost of burrowing. Physiol. Zool. 1986;59:20–28. doi: 10.1086/physzool.59.1.30156085. DOI

Oufara S, Barre H, Rouanet JL, Chatonnet J. Adaptation to extreme ambient temperatures in cold-acclimated gerbils and mice. Am. J. Physiol. 1987;253:R39–R45. PubMed

Hankenson FC, Marx JO, Gordon CJ, David JM. Effects of rodent thermoregulation on animal models in the research environment. Comp. Med. 2018;68:425–438. doi: 10.30802/AALAS-CM-18-000049. PubMed DOI PMC

Hayes JP, Speakman JR, Racey PA. The contributions of local heating and reducing exposed surface area to the energetic benefits of huddling by short-tailed field voles (Microtus agrestis) Physiol. Zool. 1992;65:742–762. doi: 10.1086/physzool.65.4.30158537. DOI

Bustamante DM, Nespolo RF, Rezende EL, Bozinovic F. Dynamic thermal balance in the leaf-eared mouse: the interplay among ambient temperature, body size, and behavior. Physiol. Biochem. Zool. 2002;75:396–404. doi: 10.1086/342253. PubMed DOI

Gilbert C, McCafferty D, Le Maho Y, Martrette JM, Giroud S, Blanc S, Ancel A. One for all and all for one: the energetic benefits of huddling in endotherms. Biol. Rev. 2010;85:545–569. PubMed

Atlee BA, Stannard AA, Fowler ME, Willemse T, Ihrke PJ, Olivry T. The histology of normal llama skin. Vet. Dermatol. 1997;8:165–176. doi: 10.1046/j.1365-3164.1997.d01-13.x. PubMed DOI

McNab BK. The metabolism of fossorial rodents: a study of convergence. Ecology. 1966;47:712–733. doi: 10.2307/1934259. DOI

Contreras LC, McNab BK. Thermoregulation and energetics in subterranean mammals. Prog. Clin. Biol. Res. 1990;335:231–250. PubMed

Burda H, Šumbera R, Begall S. Microclimate in burrows of subterranean rodents: revisited. In: Begall S, Burda H, Schleich CE, editors. Subterranean Rodents. Berlin: Springer; 2007. pp. 21–33.

Šumbera R. Thermal biology of a strictly subterranean mammalian family, the African mole-rats (Bathyergidae, Rodentia) J. Therm. Biol. 2019;79:166–189. doi: 10.1016/j.jtherbio.2018.11.003. PubMed DOI

Vleck D. The energy cost of burrowing by the pocket gopher Thomomys bottae. Physiol. Zool. 1979;52:122–136. doi: 10.1086/physzool.52.2.30152558. DOI

Lovegrove BG. The cost of burrowing by the social mole rats (Bathyergidae) Cryptomys damarensis and Heterocephalus glaber: the role of soil moisture. Physiol. Zool. 1989;62:449–469. doi: 10.1086/physzool.62.2.30156179. DOI

Zelová J, Šumbera R, Okrouhlík J, Burda H. Cost of digging is determined by intrinsic factors rather than by substrate quality in two subterranean rodent species. Physiol. Behav. 2010;99:54–58. doi: 10.1016/j.physbeh.2009.10.007. PubMed DOI

Luna F, Antinuchi CD. Energetics and thermoregulation during digging in the rodent tuco-tuco (Ctenomys talarum) Comp. Biochem. Physiol. A. 2007;146:559–564. doi: 10.1016/j.cbpa.2005.12.025. PubMed DOI

Sokolov VE. Mammal Skin. Berkeley: University of California Press; 1982.

Šumbera R, Zelová J, Kunc P, Knížková I, Burda H. Patterns of surface temperatures in two mole-rats (Bathyergidae) with different social systems as revealed by IR-thermography. Physiol. Behav. 2007;92:526–532. doi: 10.1016/j.physbeh.2007.04.029. PubMed DOI

Boyles JG, Verburgt L, McKechnie AE, Bennett NC. Heterothermy in two mole-rat species subjected to interacting thermoregulatory challenges. J. Exp. Zool. A Ecol. Genet. Physiol. 2012;317:73–82. doi: 10.1002/jez.723. PubMed DOI

Vejmělka, F. Charakteristiky srsti podzemních hlodavců ve vztahu k jejich termální biologii. [Fur characteristics of burrowing rodents in relation to their thermal biology. Bc. Thesis, in Czech]. Faculty of Science, University of South Bohemia, České Budějovice, Czech Republic (2016).

Cutrera AP, Antinuchi CD. Fur changes in the subterranean rodent Ctenomys talarum: possible thermal compensatory mechanism. Rev. Chil. Hist. Nat. 2004;77:235–242. doi: 10.4067/S0716-078X2004000200003. DOI

McGowan NE, Scantlebury DM, Bennett NC, Maule AG, Marks NJ. Thermoregulatory differences in African mole-rat species from disparate habitats: responses and limitations. J. Therm. Biol. 2020;88:102495. doi: 10.1016/j.jtherbio.2019.102495. PubMed DOI

Okrouhlík J, Burda H, Kunc P, Knížková I, Šumbera R. Surprisingly low risk of overheating during digging in two subterranean rodents. Physiol. Behav. 2015;138:236–241. doi: 10.1016/j.physbeh.2014.10.029. PubMed DOI

Kotze J, Bennett NC, Scantlebury M. The energetics of huddling in two species of mole-rat (Rodentia: Bathyergidae) Physiol. Behav. 2008;93:215–221. doi: 10.1016/j.physbeh.2007.08.016. PubMed DOI

Wiedenová P, Šumbera R, Okrouhlík J. Social thermoregulation and socio-physiological effect in the subterranean Mashona mole-rat (Fukomys darlingi) J. Therm. Biol. 2018;78:367–373. doi: 10.1016/j.jtherbio.2018.10.020. PubMed DOI

Liwanag HE, Berta A, Costa DP, Abney M, Williams TM. Morphological and thermal properties of mammalian insulation: the evolution of fur for aquatic living. Biol. J. Linn. Soc. 2012;106:926–939. doi: 10.1111/j.1095-8312.2012.01900.x. DOI

Kasza I, Hernando D, Roldán-Alzate A, Alexander CM, Reeder SB. Thermogenic profiling using magnetic resonance imaging of dermal and other adipose tissues. JCI Insight. 2016;1:e87146. doi: 10.1172/jci.insight.87146. PubMed DOI PMC

Thigpen LW. Histology of the skin of a normally hairless rodent. J. Mammal. 1940;21:449–456. doi: 10.2307/1374885. DOI

Burda H. Constraints of pregnancy and evolution of sociality in mole-rats with special reference to reproductive and social patterns in Cryptomys hottentotus (Bathyergidae, Rodentia) J. Zool. Syst. Evol. Res. 1990;28:26–39. doi: 10.1111/j.1439-0469.1990.tb00362.x. DOI

Pleštilová L, Okrouhlík J, Burda H, Sehadová H, Valesky EM, Šumbera R. Functional histology of the skin in the subterranean African giant mole-rat: thermal windows are determined solely by pelage characteristics. PeerJ. 2020;8:e8883. doi: 10.7717/peerj.8883. PubMed DOI PMC

Lövy M, Šklíba J, Burda H, Chitaukali WN, Šumbera R. Ecological characteristics in habitats of two African mole-rat species with different social systems in an area of sympatry: implications for the mole-rat social evolution. J. Zool. 2012;286:145–153. doi: 10.1111/j.1469-7998.2011.00860.x. DOI

Braude S. Dispersal and new colony formation in wild naked mole-rats: evidence against inbreeding as the system of mating. Behav. Ecol. 2000;11:7–12. doi: 10.1093/beheco/11.1.7. DOI

Lacey EA, Wieczorek JR. Kinship in colonial tuco-tucos: evidence from group composition and population structure. Behav. Ecol. 2004;15:988–996. doi: 10.1093/beheco/arh104. DOI

Lövy M, Šklíba J, Šumbera R. Spatial and temporal activity patterns of the free-living giant mole-rat (Fukomys mechowii), the largest social bathyergid. PLoS ONE. 2013;8:e55357. doi: 10.1371/journal.pone.0055357. PubMed DOI PMC

Finn, K. T. Density-dependent effects on body size, philopatry, and dispersal in the damaraland mole-rat (Fukomys damarensis) Master thesis. (Rhodes University, Faculty of Science, Grahamstown, Republic of South Africa. 2017).

Zemanová M, Šumbera R, Okrouhlík J. Poikilothermic traits in Mashona mole-rat (Fukomys darlingi). Reality or myth? J. Therm. Biol. 2012;37:485–489. doi: 10.1016/j.jtherbio.2012.04.001. DOI

Honeycutt R. Family Bathyergidae (African mole-rats) In: Wilson DE, Lacher TE, Mittermeier RA, editors. Handbook of the Mammals of the World. Lagomorphs and Rodents I. Barcelona: Lynx Edicions; 2016. pp. 352–370.

Ojeda A. Family Octodontidae. In: Wilson DE, Lacher TE, Mittermeier RA, editors. Handbook of the Mammals of the World. Lagomorphs and Rodents I. Barcelona: Lynx Edicions; 2016. pp. 536–551.

Nevo E, Ivanitskaya E, Beiles A. Adaptive Radiation of Blind Subterranean Mole Rats. Kerkwerve: Backhuys Publishers; 2001.

Hart JS, Heroux O. Exercise and temperature regulation in lemmings and rabbits. Can. J. Biochem. Physiol. 1955;33:428–435. doi: 10.1139/y55-056. PubMed DOI

Cortes A, Miranda E, Rosenmann M, Rau JR. Thermal biology of the fossorial rodent Ctenomys fulvus from the Atacama desert, northern Chile. J. Therm. Biol. 2000;25:425–430. doi: 10.1016/S0306-4565(00)00005-X. PubMed DOI

Cortes A, Tirado C, Rosenmann M. Energy metabolism and thermoregulation in Chinchilla brevicaudata. J. Therm. Biol. 2003;28:489–495. doi: 10.1016/S0306-4565(03)00049-4. DOI

Shido O, Romanovsky A, Ungar A, Blatteis C. Role of intrapreoptic norepinephrine in endotoxin-induced fever in guinea-pigs. Am. J. Physiol. 1993;265:R1369–R1375. PubMed

Chen PH, White CE. Comparison of rectal, microchip transponder, and infrared thermometry techniques for obtaining body temperature in the laboratory rabbit (Oryctolagus cuniculus) J. Am. Assoc. Lab. Anim. Sci. 2006;45:57–63. PubMed

Chapon P, Bulla J, Gauthier A, Moussay S. On the importance of telemetric temperature sensor location during intraperitoneal implantation in rats. Lab. Anim. 2014;48:114–123. doi: 10.1177/0023677214522035. PubMed DOI

Vandewint AL, Zhu-Pawlowsky AJ, Kirby A, Tattersall GJ, Pamenter ME. Evaporative cooling and vasodilation mediate thermoregulation in naked mole-rats during normoxia but not hypoxia. J. Therm. Biol. 2019;84:228–235. doi: 10.1016/j.jtherbio.2019.07.011. PubMed DOI

Harrap MJM, de Hempel Ibarra N, Whitney HM, Rands SA. Reporting of thermography parameters in biology: a systematic review of thermal imaging literature. R. Soc. Open Sci. 2018;5:181281. doi: 10.1098/rsos.181281. PubMed DOI PMC

R Core Team. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/ (2016).

Muggeo VMR. Segmented: an R package to fit regression models with broken-line relationships. R News. 2008;8:20–25.

Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D. & R Core Team. nlme: linear and nonlinear mixed effects models. R package version 3.1–128. CRAN http://CRAN.R-project.org/package=nlme (2016).

Lenth, R. Emmeans: estimated marginal means, aka Least-Squares Means. R package version 1.3.4. CRANhttps://CRAN.Rproject.org/package=emmeans (2019).

Hadfield JD. MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J. Stat. Softw. 2010;33:1–22. doi: 10.18637/jss.v033.i02. PubMed DOI

Upham NS, Esselstyn JA, Jetz W. Inferring the mammal tree: Species-level sets of phylogenies for questions in ecology, evolution, and conservation. PLoS Biol. 2019;17:e3000494. doi: 10.1371/journal.pbio.3000494. PubMed DOI PMC

Schliep KP. phangorn: phylogenetic analysis in R. Bioinformatics. 2011;27:592–593. doi: 10.1093/bioinformatics/btq706. PubMed DOI PMC

Revell LJ. phytools: an R package for phylogenetic comparative biology (and other things) Methods Ecol. Evol. 2012;3:217–223. doi: 10.1111/j.2041-210X.2011.00169.x. DOI

de Lamo DA, Sanborn AF, Carrasco CD, Scott DJ. Daily activity and behavioral thermoregulation of the guanaco (Lama guanicoe) in winter. Can. J. Zool. 1998;76:1388–1393. doi: 10.1139/z98-070. DOI

Terrien J, Perret M, Aujard F. Behavioral thermoregulation in mammals: a review. Front. Biosci. 2011;16:1428–1444. doi: 10.2741/3797. PubMed DOI

Lyman CP. Hibernation and Torpor in Mammals and Birds. Cambridge: Academic Press; 1982.

Gordon CJ. Temperature Regulation in Laboratory Rodents. Cambridge: Cambridge University Press; 1993.

Shimer HW. Adaptations to aquatic, arboreal, fossorial and cursorial habits in mammals III. Fossorial adaptations. Am. Nat. 1903;37:819–825. doi: 10.1086/278368. DOI

Stein BR. Morphology of subterranean rodents. In: Lacey EA, Patton JL, Cameron GN, editors. Life Underground: The Biology of Subterranean Rodents. Chicago: University of Chicago Press; 2000. pp. 19–61.

Thomas JR, Shurtleff D, Schrot J, Ahlers ST. Cold-induced perturbation of cutaneous blood flow in the rat tail: a model of nonfreezing cold injury. Microvasc. Res. 1994;47:166–176. doi: 10.1006/mvre.1994.1013. PubMed DOI

Daanen HAM. Finger cold-induced vasodilation: a review. Eur. J. Appl. Physiol. 2003;89:411–426. doi: 10.1007/s00421-003-0818-2. PubMed DOI

Klir JJ, Heath JE, Bennani N. An infrared thermographic study of surface temperature in relation to external thermal stress in the Mongolian gerbil, Meriones unguiculatus. Comp. Biochem. Physiol. A. 1990;96:141–146. doi: 10.1016/0300-9629(90)90055-W. PubMed DOI

Wunder BA. A model for estimating metabolic rate of active or resting mammals. J. Theor. Biol. 1975;49:345–354. doi: 10.1016/0022-5193(75)90177-0. PubMed DOI

Šklíba J, Šumbera R, Chitaukali WN, Burda H. Determinants of daily activity patterns in a free-living Afrotropical solitary subterranean rodent. J. Mammal. 2007;88:1009–1016. doi: 10.1644/06-MAMM-A-235R1.1. DOI

Šklíba J, Lövy M, Koeppen SC, Pleštilová L, Vitámvás M, Nevo E, Šumbera R. Activity of free-living subterranean blind mole rats Spalax galili (Rodentia: Spalacidae) in an area of supposed sympatric speciation. Biol. J. Linn. Soc. 2016;118:280–291. doi: 10.1111/bij.12741. DOI

Vlasatá T, Šklíba J, Lövy M, Meheretu Y, Sillero-Zubiri C, Šumbera R. Daily activity patterns in the giant root rat (Tachyoryctes macrocephalus), a fossorial rodent from the Afro-alpine zone of the Bale Mountains Ethiopia. J. Zool. 2017;302:157–163. doi: 10.1111/jzo.12441. DOI

McNab BK. The influence of body size on the energetics and distribution of fossorial and burrowing mammals. Ecology. 1979;60:1010–1021. doi: 10.2307/1936869. DOI

Nevo E, Shkolnik A. Adaptive metabolic variation of chromosome forms in mole rats. Spalax. Exp. 1974;30:724–726. PubMed

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