Abstract
Rodents colonising subterranean environments have developed several morphological, physiological and behaviour traits that promote the success of individuals in such demanding conditions. Resting metabolic rate, thermoregulation capacity and daily energy expenditure were analysed in two semi-fossorial pine-vole species Microtus lusitanicus and Microtus duodecimcostatus inhabiting distinct areas of the Iberian Peninsula. Individuals capture location varied in habitat and soil features, allowing the comparison of energetic parameters with ecological characteristics, that can help explain the use of the subterranean environment and dependence of the burrow system. Results showed that M. duodecimcostatus has lower mass independent resting metabolic rate when compared with M. lusitanicus, which may be a response to environmental features of their habitat, such as dryer soils and lower water availability. Thermal conductance increased with body mass and was dependent on the ambient temperature. No significant differences were observed in the daily energy expenditure, but water economy data demonstrated the influence of the water available in the habitat on the energetics of voles. These species may rely on behavioural adaptations and seasonal use of burrows to cope with thermal challenges of subterranean activity and soil constraints. We found strong evidence that M. lusitanicus is able to use torpor as a response to low ambient temperatures which is a new observation among Arvicolines.
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Abu-Hamdeh NH (2003) Thermal properties of soils as affected by density and water content. Biosyst Eng 86:97–102. https://doi.org/10.1016/S1537-5110(03)00112-0
Abu-Hamdeh NH, Reeder RC (2000) Soil thermal conductivity: effects of density, moisture, salt concentration, and organic matter. Soil Sci Soc Am J 64:1285–1290. https://doi.org/10.2136/sssaj2000.6441285x doi
Aulagnier S (2016a) Microtus duodecimcostatus. The IUCN Red List of Threatened Species 2016: e.T13493A513875. http://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T13493A513875.en
Aulagnier S (2016b) Microtus lusitanicus. The IUCN Red List of Threatened Species 2016: e.T13494A513980. http://dx.doi.org/10.2305/IUCN.UK.2016-3.RLTS.T13494A513980.en
Bennett NC, Aguilar GH, Jarvis JUM, Faulkes CG (1994) Thermoregulation in three species of Afrotropical subterranean mole-rats (Rodentia: Bathyergidae) from Zambia and Angola and scaling within the genus Cryptomys. Oecologia 97:222–227. https://doi.org/10.1007/BF00323153
Bertolino S, Asteggiano L, Saladini MA et al (2015) Environmental factors and agronomic practices associated with Savi’s pine vole abundance in Italian apple orchards. J Pest Sci (2004) 88:135–142. https://doi.org/10.1007/s10340-014-0581-7
Borghi CE, Giannoni SM, Martínez-Rica JP (1994) Habitat segregation of three sympatric fossorial rodents in the Spanish Pyrenees. Z Fur Saugetierkd 59:52–57
Bozinovic F, Carter MJ, Ebensperger LA (2005) A test of the thermal-stress and the cost-of-burrowing hypotheses among populations of the subterranean rodent Spalacopus cyanus. Comp Biochem Physiol 140:329–336. https://doi.org/10.1016/j.cbpb.2005.01.015
Bozinovic F, Muñoz JLP, Cruz-Neto AP (2007) Intraspecific variability in the basal metabolic rate: testing the food habits hypothesis. Physiol Biochem Zool 80:452–460. https://doi.org/10.1086/518376
Buffenstein R (2000) Ecophysiological responses of subterranean rodents to underground habitats. In: Lacey EA, Patton JL, Cameron GN (eds) Life Undergr. Biol. Subterr. rodents. University of Chicago Press, Chicago, pp 62–110
Burda H, Sumbera R, Begall S (2007) Microclimate in burrows of subterranean rodents—revisited. In: Begall S, Burda H, Schleich CE (eds) Subterr. Rodents News from Undergr. Springer-Verlag, Berlin, pp 21–33
Butler PJ, Green J, Boyd IL, Speakman JR (2004) Measuring metabolic rate in the field: the pros and cons of the doubly labelled water and heart rate methods. Funct Ecol 18:168–183. https://doi.org/10.1111/j.0269-8463.2004.00821.x
Castellanos-Frías E, García-Perea R, Gisbert J et al (2015) Intraspecific variation in the energetics of the Cabrera vole. Comp Biochem Physiol Physiol Part A Mol Integr 190:32–38. https://doi.org/10.1016/j.cbpa.2015.08.011
Cotilla I, Palomo LJ (2007) Microtus duodecimcostatus (de Sélys-Longchamps, 1839). In: Palomo LJ, Gisbert J, Blanco JC (eds) Atlas y Libr. rojo los Mamíferos Terr. España. Dirección General para la Biodiversidad-SECEM-SECEM, Madrid, pp 423–425
Depocas F, Hart JS (1957) Use of the paulling oxygen analyzer for measurement of oxygen consumption of animals in open-circuit systems and in a short-lag, closed circuit apparatus. J Appl Physiol 10:388–392. https://doi.org/10.1152/jappl.1957.10.3.388
Duarte LC, Vaanholt LM, Sinclair RE et al (2010) Limits to sustained energy intake XII: is the poor relation between resting metabolic rate and reproductive performance because resting metabolism is not a repeatable trait? J Exp Biol 213:278–287. https://doi.org/10.1242/jeb.037069
Ebensperger LA, Bozinovic F (2000) Energetics and burrowing behaviour in the semifossorial degu Octodon degus (Rodentia: Octodontidae). J Zool 252:179–186. https://doi.org/10.1017/S0952836900009912
Farley KA, Kelly EF, Hofstede RGM (2004) Soil organic carbon and water retention after conversion of grasslands to pine plantations in Ecuadorian Andes. Ecosystems 7:729–739. https://doi.org/10.1007/s10021-004-0047-5
Garland T, Adolph SC (1994) Why not to do 2-species comparative-studies—limitations on inferring adaptation. Physiol Zool 67:797–828
Giannoni SM, Borghi CE, Martínez-Rica JP (1993) Comparing the burrowing behaviour of the Iberian mole voles (Microtus (Terricola) lusitanicus, M. (T.) pyrenaicus and M. (T.) duodecimcostatus). Mammalia 57:483–490. https://doi.org/10.1515/mamm.1993.57.4.483
Guedon G, Paradis E, Croset H (1992) Capture-recapture study of a population of the Mediterranean Pine vole (Microtus duodecimcostatus) in Southern France. Z Fur Saugetierkd 57:364–372
Halle S, Stenseth NCHR (1994) Microtine ultradian rhythm of activity: an evaluation of different hypotheses on the triggering mechanism. Mamm Rev 24:17–39. https://doi.org/10.1111/j.1365-2907.1994.tb00132.x
Hammond KA, Diamond J (1997) Maximal sustained energy budgets in humans and animals. Nature 386:457–462. https://doi.org/10.1038/386457a0
Hayes JP, Speakman JR, Racey PA (1992) Sampling bias in respirometry. Physiol Zool 65:604–619. https://doi.org/10.2307/30157972
Ishii K, Kuwahara M, Tsubone H, Sugano S (1996) The telemetric monitoring of heart rate, locomotor activity, and body temperature in mice and voles (Microtus arvalis) during ambient temperature changes. Lab Anim 30:7–12. https://doi.org/10.1258/002367796780744992
Jaarola M, Martínková N, Gündüz I et al (2004) Molecular phylogeny of the speciose vole genus Microtus (Arvicolinae, Rodentia) inferred from mitochondrial DNA sequences. Mol Phylogenet Evol 33:647–663. https://doi.org/10.1016/j.ympev.2004.07.015
Jareno D, Vinuela J, Luque-Larena JJ et al (2015) Factors associated with the colonization of agricultural areas by common voles Microtus arvalis in NW Spain. Biol Invasions 17:2315–2327. https://doi.org/10.1007/s10530-015-0877-4
Kinlaw A (1999) A review of burrowing by semi-fossorial vertebrates in arid environments. J Arid Environ 41:127–145. https://doi.org/10.1006/jare.1998.0476
Koteja P (1996) Measuring energy metabolism with open-flow metric systems: which design to choose? Funct Ecol 10:675–677
Król E, Speakman JR (1999) Isotope dilution spaces of mice injected simultaneously with deuterium, tritium and oxygen-18. J Exp Biol 202:2839–2849
Lessa EP, Thaeler CS Jr (1989) A reassessment of morphological specializations for digging in pocket gophers. J Mammal 70:689–700. https://doi.org/10.2307/1381704
Lovegrove BG (1986) The metabolism of social subterranean rodents: adaptation to aridity. Oecologia 69:551–555. https://doi.org/10.1007/BF00410361
Lovegrove BG (1989) The cost of burrowing by the social mole rats (Bathyergidae) Cryptomys damarensis and Heterocephalus glaber: the role of soil moisture. Physiol Zool 62:449–469. https://doi.org/10.1086/physzool.62.2.30156179
Lovegrove BG (2003) The influence of climate on the basal metabolic rate of small mammals: a slow-fast metabolic continuum. J Comp Physiol B 173:87–112. https://doi.org/10.1007/s00360-002-0309-5
Luna F, Antinuchi CD (2006) Cost of foraging in the subterranean rodent Ctenomys talarum: effect of soil hardness. Can J Zool Can Zool 84:661–667. https://doi.org/10.1139/Z06-040
Mathias ML (1990) Morphology of the incisors and the burrowing activity of Mediterranean and Lusitanian pine voles (Mammalia, Rodentia). Mammalia 54:302–306
Mathias ML (1996) Skull size variability in adaptation and speciation of the semifossorial pine voles Microtus duodecimcostatus and M. lusitanicus (Arvicolidae, Rodentia). Proc. I Eur. Congr. Mammal. Lisboa, pp 271–286
Mathias ML, Klunder M, Santos SM (2003) Metabolism and thermoregulation in the Cabrera vole (Rodentia: Microtus cabrerae). Comp Biochem Physiol Part A Mol Integr Physiol 136:441–446. https://doi.org/10.1016/S1095-6433(03)00202-2
McNab BK (1970) Body weight and the energetics of temperature regulation. J Exp Biol 53:329–348
Mcnab BK (1979) The influence of body size on the energetics and distribution of fossorial and burrowing mammals. Ecology 60:1010–1021. https://doi.org/10.2307/1936869
McNab BK (1992) The comparative energetics of rigid endothermy—the Arvicolidae. J Zool 227:585–606. https://doi.org/10.1111/j.1469-7998.1992.tb04417.x
Miñarro M, Montiel C, Dapena E (2012) Vole pests in apple orchards: use of presence signs to estimate the abundance of Arvicola terrestris cantabriae and Microtus lusitanicus. J Pest Sci (2004) 85:477–488. https://doi.org/10.1007/s10340-012-0438-x
Mira A, Mathias ML (1994) Conditions controlling the colonization of an orange orchard by Microtus duodecimcostatus (Rodentia, Arvicolidae). Pol Ecol Stud 20:249–255
Mira A, Mathias MDL (2007) Microtus lusitanicus (Gerbe, 1879). In: Palomo LJ, Gisbert J, Blanco JC (eds) Atlas y Libr. rojo los mamífers Terr. España. Dirección General para la Biodiversidad-SECEM-SECEM, Madrid, pp 418–421
Mitchell SE, Delville C, Konstantopedos P et al (2015) The effects of graded levels of calorie restriction: III. Impact of short term calorie and protein restriction on mean daily body temperature and torpor use in the C57BL/6 mouse. Oncotarget 6:22–28. https://doi.org/10.18632/oncotarget.4506
Morgan KR, Price MV (1992) Foraging in Heteromyid rodents: the energy costs of scratch-digging. Ecology 73:2260–2272. https://doi.org/10.2307/1941473
Mueller P, Diamond J (2001) Metabolic rate and environmental productivity: well-provisioned animals evolved to run and idle fast. Proc Natl Acad Sci USA 98:12550–12554. https://doi.org/10.1073/pnas.221456698
Mustonen A-M, Saarela S, Nieminen P (2008) Food deprivation in the common vole (Microtus arvalis) and the tundra vole (Microtus oeconomus). J Comp Physiol B 178:199–208. https://doi.org/10.1007/s00360-007-0213-0
Nagy KA (1983) The doubly labeled water (3HH18O) method: a guide to its use. UCLA Publi. University of California, Los Angeles
Nieminen P, Hohtola E, Mustonen A-M (2013) Body temperature rhythms in Microtus voles during feeding, food deprivation, and winter acclimatization. J Mammal 94:591–600. https://doi.org/10.1644/12-MAMM-A-219.1
Overton JM, Williams TD (2004) Behavioral and physiologic responses to caloric restriction in mice. Physiol Behav 81:749–754. https://doi.org/10.1016/j.physbeh.2004.04.025
Peterson CC, Nagy KA, Diamond J (1990) Sustained metabolic scope. Proc Natl Acad Sci USA 87:2324–2328. https://doi.org/10.1073/pnas.87.6.2324
Refinetti R, Menaker M (1992) The circadian rhythm of body temperature. Physiol Behav 51:613–637. https://doi.org/10.2741/3634
Rezende EL, Cortés A, Bacigalupe LD et al (2003) Ambient temperature limits above-ground activity of the subterranean rodent Spalacopus cyanus. J Arid Environ 55:63–74. https://doi.org/10.1016/S0140-1963(02)00259-8
Rezende EL, Bozinovic F, Garland TJ (2004) Climatic adaptation and the evolution of basal and maximum rates of metabolism in rodents. Evolution 58:1361–1374
Richards LA (1947) Pressure-membrane apparatus, construction and use. Agron Eng 28:451–454
Ricklefs RE, Konarzewski M, Daan S (1996) The Relationship between basal metabolic rate and daily energy expenditure in birds and mammals. Am Nat 147:1047–1071. https://doi.org/10.1086/285892
Rikke BA, Yerg JE III et al (2003) Strain variation in the response of body temperature to dietary restriction. Mech Ageing 124:663–678. https://doi.org/10.1016/S0047-6374(03)00003-4
Rubal A, Haim A, Choshniak I (1995) Resting metabolic rates and daily energy intake in desert and non-desert murid rodents. Comp Biochem Physiol Part A Physiol 112:511–515. https://doi.org/10.1016/0300-9629(95)02020-9
Ruf T, Geiser F (2015) Daily torpor and hibernation in birds and mammals. Biol Rev 90:891–926. https://doi.org/10.1111/brv.12137
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. https://doi.org/10.1007/BF00571257
Santos SM, Mathias MDL, Mira AP (2011) The influence of local, landscape and spatial factors on the distribution of the Lusitanian and the Mediterranean pine voles in a Mediterranean landscape. Mamm Biol 76:133–142. https://doi.org/10.1016/j.mambio.2010.03.007
Scantlebury M, Shanas U, Speakman JR et al (2003) Energetics and water economy of common spiny mice Acomys cahirinus from north- and south-facing slopes of a Mediterranean valley. Funct Ecol 17:178–185. https://doi.org/10.1046/j.1365-2435.2003.00717.x
Soil Survey Division Staff (1993) Soil Survey Manual, Revised Edition. Agriculture Handbook, vol 18. United States Department of Agriculture, Washington DC
Speakman JR (1997) Doubly labelled water: theory and practice. Kluwer Academic Publishers, New York
Speakman JR (2000) The cost of living: field metabolic rates of small mammals. Adv Ecol Res 30:177–297. https://doi.org/10.1016/S0065-2504(08)60019-7
Speakman JR, Król E (2005) Comparison of different approaches for the calculation of energy expenditure using doubly labeled water in a small mammal. Physiol Biochem Zool PBZ 78:650–667. https://doi.org/10.1086/430234
Speakman JR, Król E (2010) Maximal heat dissipation capacity and hyperthermia risk: neglected key factors in the ecology of endotherms. J Anim Ecol 79:726–746. https://doi.org/10.1111/j.1365-2656.2010.01689.x
Speakman JR, Racey PA (1988) The doubly-labelled water techinique for measurement of energy expenditure in free-living animals. Sci Prog 72:227–237
Speakman J, Nagy K, Masman D et al (1990) Interlaboratory comparison of different analytical techniques for the determination of oxygen-18 abundance. Anal Chem 62:703–708. https://doi.org/10.1021/ac00206a011
Speakman JR, Nair KS, Goran MI (1993) Revised equations for calculating CO2 production from doubly labeled water in humans. Am J Physiol 264:E912–E917. https://doi.org/10.1152/ajpendo.1993.264.6.E912
Stein BR (2000) Morphology of subterranean rodents. In: Lacey EA, Patton JL, Cameron GN (eds) Life Undergr. Biol. Subterr. rodents. The University of Chicago Press, Chicago, pp 19–61
Tannenbaum MG, Pivorun EB (1987) Differential effect of food restriction on the induction of daily torpor in Peromyscus maniculatus and Peromyscus leucopus. J Therm Biol 12:159–162. https://doi.org/10.1016/0306-4565(87)90057-X
Tschöp MH, Speakman JR, Arch JRS et al (2012) A guide to analysis of mouse energy metabolism. Nat Methods 9:57–63. https://doi.org/10.1038/nmeth.1806
Urrejola D, Lacey EA, Wieczorek JR, Ebensperger LA (2005) Daily activity patterns of free-living cururos (Spalacopus cyanus). J Mammal 86:302–308. https://doi.org/10.1644/BWG-222.1
Ventura J, Jiménez L, Gisbert J (2010) Breeding characteristics of the Lusitanian pine vole, Microtus lusitanicus. Anim Biol 60:1–14. https://doi.org/10.1163/157075610X12610595764011
Vinhas A (1993) Microtus lusitanicus (rato cego) e Microtus duodecimcostatus (rato toupeira) roedores pragas das culturas. Rev Ciências Agrárias XVI:375–382
Vleck D (1979) The energy cost of burrowing by the pocket gopher Thomomys bottae. Physiol Zool 52:122–136
Westerterp KR, Speakman JR (2008) Physical activity energy expenditure has not declined since the 1980s and matches energy expenditures of wild mammals. Int J Obes 32:1256–1263. https://doi.org/10.1038/ijo.2008.74
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Acknowledgments are due for the financial support to Centre for environment and marine studies (UID/AMB/50017-POCI-01-0145-FEDER-007638), to Fundação para a Ciência e Tecnologia through national funds (PIDDAC), and the co-funding by the FEDER, within the PT2020 Partnership Agreement and Compete 2020. RIM was supported by fellowship BPD/UI88/7346/2016 and JRS was supported by the 1000 talents program of the Chinese government. We thank the three anonymous referees for their valuable comments on this manuscript.
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Monarca, R.I., Speakman, J.R. & Mathias, M. Energetics and thermal adaptation in semifossorial pine-voles Microtus lusitanicus and Microtus duodecimcostatus. J Comp Physiol B 189, 309–318 (2019). https://doi.org/10.1007/s00360-019-01205-z
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DOI: https://doi.org/10.1007/s00360-019-01205-z