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Energetics and thermal adaptation in semifossorial pine-voles Microtus lusitanicus and Microtus duodecimcostatus

  • Rita I. MonarcaEmail author
  • John R. Speakman
  • Maria da Luz Mathias
Original Paper
  • 13 Downloads

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.

Keywords

Doubly labelled water Resting metabolic rate Water turnover Digging energetics 

Notes

Acknowledgements

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.

Supplementary material

360_2019_1205_MOESM1_ESM.pdf (111 kb)
Supplementary material 1 (PDF 111 KB)

References

  1. 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 CrossRefGoogle Scholar
  2. 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 doiCrossRefGoogle Scholar
  3. 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
  4. 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
  5. 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 CrossRefGoogle Scholar
  6. 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 CrossRefGoogle Scholar
  7. Borghi CE, Giannoni SM, Martínez-Rica JP (1994) Habitat segregation of three sympatric fossorial rodents in the Spanish Pyrenees. Z Fur Saugetierkd 59:52–57Google Scholar
  8. 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 CrossRefGoogle Scholar
  9. 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 CrossRefGoogle Scholar
  10. 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 62–110Google Scholar
  11. 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 21–33CrossRefGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. 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 CrossRefGoogle Scholar
  14. 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 423–425Google Scholar
  15. 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 CrossRefGoogle Scholar
  16. 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 CrossRefGoogle Scholar
  17. 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 CrossRefGoogle Scholar
  18. 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 CrossRefGoogle Scholar
  19. Garland T, Adolph SC (1994) Why not to do 2-species comparative-studies—limitations on inferring adaptation. Physiol Zool 67:797–828CrossRefGoogle Scholar
  20. 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 Google Scholar
  21. 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 57:364–372Google Scholar
  22. 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 CrossRefGoogle Scholar
  23. Hammond KA, Diamond J (1997) Maximal sustained energy budgets in humans and animals. Nature 386:457–462.  https://doi.org/10.1038/386457a0 CrossRefGoogle Scholar
  24. Hayes JP, Speakman JR, Racey PA (1992) Sampling bias in respirometry. Physiol Zool 65:604–619.  https://doi.org/10.2307/30157972 CrossRefGoogle Scholar
  25. 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 CrossRefGoogle Scholar
  26. 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 CrossRefGoogle Scholar
  27. 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 CrossRefGoogle Scholar
  28. 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 CrossRefGoogle Scholar
  29. Koteja P (1996) Measuring energy metabolism with open-flow metric systems: which design to choose? Funct Ecol 10:675–677CrossRefGoogle Scholar
  30. Król E, Speakman JR (1999) Isotope dilution spaces of mice injected simultaneously with deuterium, tritium and oxygen-18. J Exp Biol 202:2839–2849Google Scholar
  31. 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 CrossRefGoogle Scholar
  32. Lovegrove BG (1986) The metabolism of social subterranean rodents: adaptation to aridity. Oecologia 69:551–555.  https://doi.org/10.1007/BF00410361 CrossRefGoogle Scholar
  33. 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 CrossRefGoogle Scholar
  34. 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 Google Scholar
  35. 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 CrossRefGoogle Scholar
  36. Mathias ML (1990) Morphology of the incisors and the burrowing activity of Mediterranean and Lusitanian pine voles (Mammalia, Rodentia). Mammalia 54:302–306CrossRefGoogle Scholar
  37. 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 271–286Google Scholar
  38. 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 CrossRefGoogle Scholar
  39. McNab BK (1970) Body weight and the energetics of temperature regulation. J Exp Biol 53:329–348Google Scholar
  40. 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 CrossRefGoogle Scholar
  41. 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 CrossRefGoogle Scholar
  42. 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 CrossRefGoogle Scholar
  43. Mira A, Mathias ML (1994) Conditions controlling the colonization of an orange orchard by Microtus duodecimcostatus (Rodentia, Arvicolidae). Pol Ecol Stud 20:249–255Google Scholar
  44. 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 418–421Google Scholar
  45. 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 Google Scholar
  46. 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 CrossRefGoogle Scholar
  47. 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 CrossRefGoogle Scholar
  48. 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 CrossRefGoogle Scholar
  49. Nagy KA (1983) The doubly labeled water (3HH18O) method: a guide to its use. UCLA Publi. University of California, Los AngelesGoogle Scholar
  50. 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 CrossRefGoogle Scholar
  51. 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 CrossRefGoogle Scholar
  52. 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 CrossRefGoogle Scholar
  53. Refinetti R, Menaker M (1992) The circadian rhythm of body temperature. Physiol Behav 51:613–637.  https://doi.org/10.2741/3634 CrossRefGoogle Scholar
  54. 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 CrossRefGoogle Scholar
  55. Rezende EL, Bozinovic F, Garland TJ (2004) Climatic adaptation and the evolution of basal and maximum rates of metabolism in rodents. Evolution 58:1361–1374CrossRefGoogle Scholar
  56. Richards LA (1947) Pressure-membrane apparatus, construction and use. Agron Eng 28:451–454Google Scholar
  57. 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 CrossRefGoogle Scholar
  58. 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 CrossRefGoogle Scholar
  59. 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 CrossRefGoogle Scholar
  60. 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 CrossRefGoogle Scholar
  61. 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 CrossRefGoogle Scholar
  62. 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 CrossRefGoogle Scholar
  63. 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 CrossRefGoogle Scholar
  64. Soil Survey Division Staff (1993) Soil Survey Manual, Revised Edition. Agriculture Handbook, vol 18. United States Department of Agriculture, Washington DCGoogle Scholar
  65. Speakman JR (1997) Doubly labelled water: theory and practice. Kluwer Academic Publishers, New YorkGoogle Scholar
  66. 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 CrossRefGoogle Scholar
  67. 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 CrossRefGoogle Scholar
  68. 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 Google Scholar
  69. Speakman JR, Racey PA (1988) The doubly-labelled water techinique for measurement of energy expenditure in free-living animals. Sci Prog 72:227–237Google Scholar
  70. 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 CrossRefGoogle Scholar
  71. 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 CrossRefGoogle Scholar
  72. 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 19–61Google Scholar
  73. 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 CrossRefGoogle Scholar
  74. 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 CrossRefGoogle Scholar
  75. 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 CrossRefGoogle Scholar
  76. 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 CrossRefGoogle Scholar
  77. Vinhas A (1993) Microtus lusitanicus (rato cego) e Microtus duodecimcostatus (rato toupeira) roedores pragas das culturas. Rev Ciências Agrárias XVI:375–382Google Scholar
  78. Vleck D (1979) The energy cost of burrowing by the pocket gopher Thomomys bottae. Physiol Zool 52:122–136CrossRefGoogle Scholar
  79. 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 CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Departamento de Biologia Animal, Faculdade de Ciências da Universidade de LisboaCESAM-Center for Environmental and Marine StudiesLisbonPortugal
  2. 2.Institute of Biological and Environmental SciencesUniversity of AberdeenAberdeenUK
  3. 3.Institute of Genetics and Developmental BiologyChinese Academy of SciencesBeijingChina

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