Abstract
Anatolian ground squirrels, Spermophilus xanthoprymnus (Bennett, 1835), are nearly endemic to Turkey. Various aspects of the biology of Anatolian ground squirrels have been studied. However, a detailed description of hibernation, with special attention to age and sex differences, has not previously been reported. Thus, in this study, we aimed to present a detailed description of hibernation in a population of free-living Anatolian ground squirrels, with special attention to age and sex differences, in relation to soil temperature (Tsoil) at the expected depth of the hibernacula. This study is the first such study for Old World ground squirrels (the genus Spermophilus sensu stricto) and incorporates an additional species from a different environment (e.g. warmer than those of others) into comparative studies of hibernation patterns in Holarctic ground squirrels (the tribe Marmotini) under natural conditions. Body temperature (Tb) was continuously recorded from late summer to spring by intraperitoneally implanted temperature loggers and Tsoil by a temperature logger at a depth of 1 m in the field. Anatolian ground squirrels spent about half of the year in hibernation. However, differences in timing of the beginning and end of hibernation resulted in differences in the duration of hibernation among age-sex classes. The duration of torpor bouts was short at the beginning of hibernation, increased as Tsoil decreased, reached its maximum toward the end of hibernation, and decreased thereafter. Adult males exhibited hibernation characteristics rather different from those of other age-sex classes, spending less time in hibernation, exhibiting shorter torpor bouts and longer interbout arousals, especially toward the end of hibernation, and spending proportionally less time in torpor. In conclusion, we observed that hibernation patterns in free-living Anatolian ground squirrels were influenced by age-sex classes, as well as environmental conditions.
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References
Animal Care and Use Committee, 1998. Guidelines forthe capture, handling, and care of mammals as approved by the American Society of Mammalogists. J. Mammal. 79, 1416–1431.
Aschoff, J., 1981. Thermal conductance in mammals and birds: its dependence on body size and circadian phase. Comp. Biochem. Physiol. A: Comp. Physiol. 69, 611–619.
Atalay, I., Mortan, K., 2006. Türkiye bölgesel cografyası. I˙nkılap Kitabevi, Istanbul.
Barnes, B.M., 1989. Freeze avoidance in a mammal: body temperatures below 0 degree C in an Arctic hibernator. Science 244, 1593–1595.
Barnes, B.M., 1996. Relationships between hibernation and reproduction in male ground squirrels. In: Geiser, F., Hulbert, A.J., Nicol, S.C. (Eds.), Adaptations to the Cold: Tenth International Hibernation Symposium. University of New England Press, Australia, pp. 71–80.
Barnes, B.M., Ritter, D., 1993. Patterns of body temperature change in hibernating arctic ground squirrels. In: Carey, C, Florant, G.L., Wunder, B.A., Horwitz, B. (Eds.), Life in the Cold: Ecological Physiological and Molecular Mechanisms. Westview Press, Colorado, pp. 119–130.
Bartholomew, G.A., 1982. Body temperature and energy metabolism. In: Gordon, M.S., Bartholomew, G.A., Grinnell, A.D., Jørgensen, C.B., White, F.N. (Eds.), Animal Physiology: Principles and Adaptations. Macmillan, New York, pp. 333–406.
Benjamini, Y., Hochberg, Y., 1995. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc. B 57, 289–300.
Buck, C.L., Breton, A., Kohl, F., Tøien, Ø., Barnes, B.M., 2008. Overwinter body temperature patterns in free-living arctic squirrels (Spermophilus parryii). In: Lovegrove, B.G., McKechnie, A.E. (Eds.), Hypometabolism in Animals: Hibernation, Torpor and Cryobiology. University of KwaZulu-Natal Press, South Africa, pp. 317–326.
Fagerstone, K.A., 1988. The annual cycle of Wyoming ground squirrels in Colorado. J. Mammal. 69, 678–687.
Florant, G.L., Hill, V., Ogilvie, M.D., 2000. Circadian rhythms of body temperature in laboratory and field marmots (Marmota flaviventris). In: Heldmaier, G., Klingen-spor, M. (Eds.), Life in the Cold. Springer-Verlag, Heidelberg, pp. 223–231.
Geiser, F., 1988. Reduction of metabolism during hibernation and daily torpor in mammals and birds: temperature effect or physiological inhibition? J. Comp. Physiol. B 158, 25–37.
Geiser, F., Ruf, T., 1995. Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol. Zool. 68, 935–966.
Gür, H., 2010. Why do Anatolian ground squirrels exhibit a Bergmannian size pattern? A phylogenetic comparative analysis of geographic variation in body size. Biol. J. Linn. Soc. 100, 695–710.
Gür, H., 2013. The effects of Late Quaternary glacial-interglacial cycles on Anatolian ground squirrels: range expansion during the glacial periods? Biol. J. Linn. Soc. 109, 19–32.
Gür, H., Barlas, N., 2006. Sex ratio of a population of Anatolian ground squirrels Spermophilus xanthoprymnus in Central Anatolia, Turkey. Acta Theriol. 51, 61–67.
Gür, H., Kart Gür, M., 2005. Annual cycle of activity, reproduction, and body mass of Anatolian ground squirrels (Spermophilus xanthoprymnus) in Turkey. J. Mammal. 86, 7–14.
Gür, H., Kart Gür, M., 2012. Is spatial variation in food availability an explanation for a Bergmannian size pattern in a North American hibernating, burrowing mammal? An information-theoretic approach. J. Zool. 287, 104–114.
Healy, J.E., Burdett, K.A., Buck, C.L., Florant, G.L., 2012. Sex differences in torpor patterns during natural hibernation in golden-mantled ground squirrels (Cal-lospermophilus lateralis).J. Mammal. 93, 751–758.
Heldmaier, G., Ruf, T., 1992. Body temperature and metabolic rate during natural hypothermia in endotherms. J. Comp. Physiol. B 162, 696–706.
Helgen, K.M., Cole, R.F., Helgen, L.E., Wilson, D.E., 2009. Generic revision in the Holarctic ground squirrel genus Spermophilus. J. Mammal. 90, 270–305.
Humphries, M.M., Kramer, D.L., Thomas, D.W., 2003. The role of energy availability in mammalian hibernation: an experimental test in free-ranging eastern chipmunks. Physiol. Biochem. Zool. 76, 180–186.
Hut, R.A., Barnes, B.M., Daan, S., 2002. Body temperature patterns before, during and aftersemi-natural hibernation intheEuropeanground squirrel. J. Comp. Physiol. B 172, 47–58.
Institute for Laboratory Animal Research-ILAR, 1996. Guide for the Care and Use of Laboratory Animals. The National Academy Press, Washington.
Karabag, T., 1953. Ankara dolaylarındaki tarla sincaplarının (Citellus’ların) biyolojisi vebunlarlasavas¸usulleri. Ankara ÜniversitesiZiraat FakültesiYayınları, Ankara.
Kart Gür, M., Gür, H., 2010. Spermophilus xanthoprymnus (Rodentia: Sciuridae). Mamm. Species 42, 183–194.
Kart Gür, M., Refınetti, R., Gür, H., 2009. Daily rhythmicity and hibernation in the Anatolian ground squirrel under natural and laboratory conditions. J. Comp. Physiol. B 179, 155–164.
Kisser, B., Goodwin, T., 2012. Hibernation and overwinter body temperatures in free-ranging thirteen-lined ground squirrels, Ictidomys tridecemlineatus. Am. Midl. Nat. 167, 396–409.
Knopf, F.L., Balph, D.F., 1977. Annual periodicity of Uinta ground squirrels. Southwest. Nat. 22, 213–224.
Krystufek, B., Vohralík, V., 2005. Mammals of Turkey and Cyprus. Rodentia I: Sciuridae, Dipodidae, Gliridae, Arvicolinae, Založba Annales, Koper, Slovenia.
Kryštufek, B., Vohralík, V., 2012. Taxonomic revision of the Palaearctic rodents (Rodentia). Sciuridae: Xerinae 1 (Eutamias and Spermophilus). Lynx 43, 17–111.
Lee, T.E., Barnes, B.M., Buck, C.L., 2009. Body temperature patterns during hibernation in a free-living Alaska marmot (Marmota broweri). Ethol. Ecol. Evol. 21, 403–413.
Lehmer, E.M., Biggins, D.E., 2005. Variation in torpor patterns of free-ranging black-tailed and Utah prairie dogs across gradients of elevation. J. Mammal. 86, 15–21.
Lyman, C.P., 1982. Who is who among hibernators. In: Lyman, C.P., Willis, J.S., Malan, A., Wang, L.C.H. (Eds.), Hibernation and Torpor in Mammals and Birds. Academic Press, California, pp. 12–31.
Malan, A., 2010. Is the torpor-arousal cycle of hibernation controlled by a non-temperature-compensated circadian clock? J. Biol. Rhythms 25, 166–175.
Malan, A., 2012. The torpor-arousal cycle is controlled by an endogenous clock. In: Ruf, T., Bieber, C, Arnold, W., Millesi, E. (Eds.), Living in a Seasonal World. Springer Verlag, Heidelberg, pp. 211–218.
Mcnab, B.K., 1974. The energetics of endotherms. Ohio J. Sci. 74, 370–380.
Michener, G.R., 1984. Age, sex, and species differences in the annual cycle of ground-dwelling sciurids: implications forsociality. In: Murie,J.O., Michener, G.R.(Eds.), The Biology of Ground Dwelling Squirrels: Annual Cycles, Behavioral Ecology, and Sociality. University of Nebraska Press, Lincoln, pp. 81–107.
Michener, G.R., 1992. Sexual differences in over-winter torpor patterns of Richardson’s ground squirrels in natural hibernacula. Oecologia 89, 397–406.
Pengelley, E.T., Fisher, K.C., 1961. Rhythmical arousal from hibernation in the golden-mantled ground squirrel, Citellus lateralis tescorum. Can. J. Zool. 39, 105–120.
Pohl, H., 1961. Temperaturregulation und Tagesperiodik des Stoffwechsels bei Win-terschläfern. Z. Vergl. Physiol. 45, 109–153.
Ruf, T., Arnold, W., 2000. Mechanisms of social thermoregulation in hibernating alpine marmots (Marmota marmota). In: Heldmaier, G., Klingenspor, M. (Eds.), Life in the Cold. Springer-Verlag, Heidelberg, pp. 81–94.
Ruf, T., Geiser, F., 2014. Daily torpor and hibernation in birds and mammals. Biol. Rev., https://doi.org/10.1111/brv.1213710.1111/brv.12137
Russell, R.L., O’Neill, P.H., Epperson, L.E., Martin, S.L., 2010. Extensive use of torpor in 13-lined ground squirrels in the fall prior to cold exposure. J. Comp. Physiol. B 180, 1165–1172.
Sheriff, M.J., Kenagy, G.J., Richter, M., Lee, T., Tøien, O., Kohl, F., Buck, C.L., Barnes, B.M., 2011. Phenological variation in annual timing of hibernation and breeding in nearby populations of Arctic ground squirrels. Proc. R. Soc. Lond. B: Biol. Sci. 278, 2369–2375.
Sheriff, M.J., Williams, C.T., Kenagy, G.J., Buck, L., Barnes, B.M., 2012. Thermoregulatory changes anticipate hibernation onset by 45 days: data from free-living arctic ground squirrels. J. Comp. Physiol. B 182, 841–847.
Sokal, R.R., Rohlf, F.J., 1995. Biometry: The Principles and Practice of Statistics in Biological Research. W. H. Freeman and Company, New York.
Speakman, J.R., 2000. The Cost of Living: Field Metabolic Rates of Small Mammals. Adv. Ecol. Res. 30, 177–297.
Stawski, C, 2012. Comparison of variables of torpor between populations of a hibernating subtropical/tropical bat at different latitudes. In: Ruf, T., Bieber, C, Arnold, W., Millesi, E. (Eds.), Living in a Seasonal World. Springer Verlag, Heidelberg, pp. 99–108.
Strumwasser, F., 1959. Factors in the pattern, timing and predictability of hibernation in the squirrel, Citellus beecheyi. Am. J. Physiol. 196, 8–14.
Strumwasser, F., 1960. Some physiological principles governing hibernation inCitel-lus beecheyi. Bull. Mus. Comp. Zool. 124, 285–320.
Thorington, R.W., Koprowski, J.L., Steele, M.A., Whatton, J.F., 2012. Squirrels of the World. The Johns Hopkins University Press, Baltimore, Maryland.
Wang, L.C.H., 1973. Radiotelemetric study of hibernation under natural and laboratory conditions. Am. J. Physiol. 224, 673–677.
Wang, L.C.H., 1979. Time patterns and metabolic rates of natural torpor in the Richardson’s ground squirrel. Can. J. Zool. 57, 149–155.
Wickham, H., 2009. ggplot2: Elegant Graphics for Data Analysis. Springer, New York.
Williams, C.T., Barnes, B.M., Kenagy, G.J., Buck, C.L., 2014. Phenology of hibernation and reproduction in ground squirrels: integration of environmental cues with endogenous programming. J. Zool. 292, 112–124.
Yang, M., Xing, X., Guan, S., Zhao, Y., Wang, Z., Wang, D., 2011. Hibernation patterns and changes of body temperature in Daurian ground squirrels (Spermophilus dauricus) during hibernation. Acta Theriol. Sin. 31, 387–395.
Yigit, N., Colak, E., Sözen, M., Özkurt, S¸., 2000. A Study on the Hibernation of Spermophilus xanthoprymnus (Bennet, 1835) (Mammalia: Rodentia) in Turkey. Turk. J. Zool. 24, 87–93.
Young, P.J., 1990. Hibernating patterns of free-ranging Columbian ground squirrels. Oecologia 83, 504–511.
Zervanos, S.M., Salsbury, CM., 2003. Seasonal body temperature fluctuations and energetic strategies in free-ranging eastern woodchucks (Marmota monax). J. Mammal. 84, 299–310.
Zervanos, S.M., Maher, C.R., Waldvogel, J.A., Florant, G.A., 2010. Latitudinal differences in the hibernation characteristics of woodchucks (Marmota monax). Physiol. Biochem. Zool. 83, 135–142.
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Kart Gür, M., Gür, H. Age and sex differences in hibernation patterns in free-living Anatolian ground squirrels. Mamm Biol 80, 265–272 (2015). https://doi.org/10.1016/j.mambio.2015.02.006
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DOI: https://doi.org/10.1016/j.mambio.2015.02.006