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Daily torpor in Campbell’s hamster (Phodopus campbelli Thomas, 1905): proximate factors and ultimate fitness consequences
Khrushchova A.M., Vasilieva N.Yu., Shekarova O.N., Vasilieva N.A., Rogovin K.A.
P. 32-43
In 68 pairs of Campbell’s hamster (Phodopus campbelli Thomas, 1905) caged outdoors, under natural day length and temperature, we considered ambient temperatures, body mass and its change as proximate factors of torpor bouts. The ultimate effects of daily torpor were assessed by the mortality of animals and the number of litters born. Both sexes showed daily torpor irregularly from November 2010 to January 2011 with a maximum in December; 37% of males and 39% of females did not show any torpor at all. There was no link between torpor episodes and low ambient temperatures during the whole winter, when considering the total winter period, however, we did find a significant link between ambient temperature and torpor use in December. Daily torpor in Campbell’s hamsters we studied seems not to be an obligate, strictly deterministic physiological response to critical body condition when the body reserves are close to exhaustion. Among males, we observed a tendency towards a positive correlation of the number of torpor bouts on the initial body mass in September. The body mass loss from September to December was positively correlated to September’s body mass. Torpor pattern did not affect the hamsters’ survival and the number of litters born. We conclude that our results do not indicate daily torpor in Campbell’s hamster as an obligate life history adaptation, which should unconditionally enhance ultimate fitness consequences.

DOI: 10.15298/rusjtheriol.22.1.04

References

  • Barnes B.M. 1986. Annual cycles of gonadotropins and androgens in the hibernating golden mantled ground squirrel // General and Comparative Endocrinology. Vol.62. No.1. P.13–22.

  • Barton K. 2019. Package ‘MuMIn’. R package version, 1.43.6. Retrieved 01 Dec 2019 from https://CRAN.R-project.org/package=MuMIn.

  • Bates D., Mächler M., Bolker B.M. & Walker S. 2015. Linear mixed-effects models using “Eigen” and S4. R package version 1.1-8 (2015); http://cran. r-project.org/package=lme4.

  • Batsaikhan N., Shar S., Lkhagvasuren D., King S.R.B. & Samiya R. 2022. A Field Guide to the Mammals of Mongolia. Third edition. Mongolian Society of Mammalogy. National University of Mongolia. 321 p.

  • Buchanan K., Perera T., Carere C., Carter T., Hailey A., Hubrecht R., Jennings D., Metcalfe N., Pitcher T., Péron F., Sneddon L., Sherwin C., Talling J.,Thomas R. & Thompson M. 2012. Guidelines for the treatment of animals in behavioural research and teaching // Animal Behaviour. Vol.83. P.301–309.

  • Burnham K.P., Anderson D.R. & Huyvaert K.P. 2011. AIC model selection and multimodel inference in behavioral ecology: some background, observations, and comparisons // Behavioral Ecology and Sociobiology. Vol.65. P.23–35.

  • Cubuk C., Bank J.H.H. & Herwig A. 2016. The chemistry of cold: mechanisms of torpor regulation in the Siberian hamster // Physiology. Vol.31. P.51–59.

  • Diedrich V., Kumstel S. & Steinlechner S. 2015. Spontaneous daily torpor and fasting-induced torpor in Djungarian hamsters are characterized by distinct patterns of metabolic rate // Journal of Comparative Physiology, B, Biochemical, Systemic, and Environmental Physiology. Vol.185. P.355–366.

  • Diedrich V., Haugg E., Dreier C. & Herwig A. 2020. What can seasonal models teach us about energy balance? // Journal of Endocrinology. Vol.244. No.2. P.R17–R32.

  • Ellis L.C., Palmer R.A. & Balph D.F. 1983. The reproductive cycle of male Uinta ground squirrels: some anatomical and biochemical correlates // Comparative Biochemistry and Physiology. A, Comparative Physiology. Vol.74. No.2. P.239–245.

  • Feoktistova N.Y., Naidenko S.V., Surov A.V. & Menchinskii K.M. 2013. Ecological and physiological characteristics of seasonal biology of the Mongolian hamster, Allocricetulus curtatus Allan, 1940 (Cricetinae, Rodentia) // Russian Journal of Ecology. Vol.44. No.1. P.56–59.

  • Flint V.E. & Golovkin A.N. 1961. [Essay on the comparative ecology of Tuva hamsters] // Byulleten’ Moskovskogo Obshchestva Ispytatelei Prirody, Otdel Biologicheskii. Vol.66. P.57–75 [in Russian].

  • Geiser F. 2004. Metabolic rate and body temperature reduction during hibernation and daily torpor // Annual Review of Physiology. Vol.66. No.1. P.239–274.

  • Geiser F. 2021. Patterns and expression of torpor // Geiser F. (ed.). Ecological Physiology of Daily Torpor and Hibernation. Cham, Switzerland: Springer. P.93–107.

  • Geiser F. & Brigham R.M. 2012. The other functions of torpor // Ruf T., Bieber C., Arnold W. & Millesi E. (eds.). Living in a Seasonal World. Berlin, Heidelberg: Springer-Verlag. P.109–121.

  • Geiser F. & Ruf T. 1995. Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns // Physiological Zoology. Vol.68. No.6. P.935–966.

  • Goldman B.D., Darrow J.M., Duncan M.J. & Yogev L. 1986. Photoperiod, reproductive hormones, and winter torpor in three hamster species // Heller H.C., Musacchia X.J. & Wang L.C.H. (eds.). Living in the Cold. New York: Elsevier. P.341–350.

  • Hall V. & Goldman B. 1980. Effects of gonadal steroid hormones on hibernation in the Turkish hamster (Mesocricetus brandti) // Journal of Comparative Physiology. Vol.135. P.107–114.

  • Haugg E., Herwig A. & Diedrich V. 2021. Body temperature and activity adaptation of short photoperiod-exposed Djungarian hamsters (Phodopus sungorus): timing, traits, and torpor // Frontiers in Physiology. Vol.12. P.1–21.

  • Hazlerigg D. 2012.The evolutionary physiology of photoperiodism in vertebrates // Progress in Brain Research. Vol.199. P.413–422.

  • Heldmaier G. & Steinlechner S. 1981. Seasonal control of energy requirements for thermoregulation in the Djungarian hamster (Phodopus sungorus), living in natural photoperiod // Journal of Comparative Physiology. Vol.142. No.4. P.429–437.

  • Heldmaier G., Ortmann S. & Elvert R. 2004. Natural hypometabolism during hibernation and daily torpor in mammals // Respiratory Physiology & Neurobiology. Vol.141. No.3. P.317–329.

  • Jastroch M., Giroud S., Barrett P., Geiser F., Heldmaier G. & Herwig A. 2016. Seasonal control of mammalian energy balance: recent advances in the understanding of daily torpor and hibernation // Journal of Neuroendocrinology. Vol.28. No.11. P.jne.12437.

  • Kalabukhov N.I. 1936. [Mammalian Hibernation]. Moscow, Leningrad: Biomedgiz. 204 p. [in Russian].

  • Khrushchova A.M. & Vasilieva N.Yu. 2011. [Torpor in Campbell’s hamster (Phodopus campbelli Thomas, 1905). Experimental proofs] // Abstracts of IX Congress of the Theriological Society, the Russian Academy of Sciences, Moscow, Russia. P.510 [in Russian].

  • Khrushchova A.M., Vasilieva N.Yu., Shekarova O.N., Rogovin K.A. & Petrovski D.V. 2017. Torpor in Campbell’s hamster (Phodopus campbelli) and desert hamster (Phodopus roborovskii): a comparative analysis // Abstracts of the 9th International Symposium of Integrative Zoology, Xining, China. P.68.

  • Kortner G. & Geiser F. 2000. The temporal organization of daily torpor and hibernation: circadian and circannual rhythms // Chronobiology International. Vol.17. No.2. P.103–128.

  • Landau B.R. & Dawe A.R. 1960. Observations on a colony of captive ground squirrels throughout the year // Lyman C.P. & Dawe A.R. (eds.). Mammalian Hibernation. Bulletin of the Museum of Comparative Zoology. Cambridge: Harvard University. P.173–189.

  • Lee T.M., Pelz K., Licht P. & Zucker I. 1990. Testosterone influences hibernation in golden-mantled ground squirrels // American Journal of Physiology — Regulatory, Integrative and Comparative Physiology. Vol.259. No.4. P.760–767.

  • Lyman C.P., Willis J.S., Malan A. & Wang L.C.H. 1982. Hibernation and Torpor in Mammals and Birds. New York: Academic Press. 318 p.

  • Mallon D.P. 1985. The mammals of the Mongolian People’s Republic // Mammal Review. Vol.15. No.2. P.71–102.

  • McAllan B.M. & Geiser F. 2014. Torpor during reproduction in mammals and birds: dealing with an energetic conundrum // American Zoologist. Vol.54. No.3. P.516–532.

  • Murzaev E.M. 1952. [Mongolian People’s Republic. Physical and Geographical Description]. Moscow: Geografgiz. 472 p. [in Russian].

  • Müller D., Hauer J., Schöttner K., Fritzsche P. & Weinert D. 2015. Seasonal adaptation of dwarf hamsters (genus Phodopus): differences between species and their geographic origin // Journal of Comparative Physiology, B. Vol.185. No.8. P.917–930.

  • Nowack J., Stawski C. & Geiser F. 2017. More functions of torpor and their roles in a changing world // Journal of Comparative Physiology, B. Vol.187. No.5. P.889–897.

  • Nowack J., Levesque D.L., Reher S. & Dausmann K.H. 2020. Variable climates lead to varying phenotypes: “Weird” mammalian torpor and lessons from non-Holarctic species // Frontiers in Ecology and Evolution. Vol.8. P.e60.

  • Ouarour A., Kirsch R. & Pevet P. 1991. Effects of temperature, steroids and castration on daily torpor in the Djungarian hamster (Phodopus sungorus) // Journal of Comparative Physiology, A. Vol.168. No.4. P.477–481.

  • Paul M.J., Zucker I. & Schwartz W.J. 2008. Tracking the seasons: the internal calendars of vertebrates // Philosophical Transactions of the Royal Society of London. Biological Series. Vol.363. No.1490. P.341–361.

  • Place N.J., Veloso C., Visser G.H. & Kenagy G.J. 2002. Energy expenditure and testosterone in free-living male yellow-pine chipmunks // Journal of Experimental Zoology. Vol.292. No.5. P.460–467.

  • Przybylska A.S., Wojciechowski M.S. & Jefimow M. 2019. Photoresponsiveness affects life history traits but not oxidative status in a seasonal rodent // Frontiers in Zoology. Vol.16. No.1. P.1–13.

  • R Core Development Team. 2021. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna.

  • Ruby N.F., Nelson R.J., Licht P. & Zucker I. 1993. Prolactin and testosterone inhibit torpor in Siberian hamsters // American Journal of Physiology. Vol.264. No.1. P.R123–R128.

  • Ruf T., Klingenspor M., Preis H. & Heldmaier G. 1991. Daily torpor in the Djungarian hamster (Phodopus sungorus): interactions with food intake, activity, and social behavior // Journal of Comparative Physiology, B. Vol.160. P.609–615.

  • Ruf T., Stieglitz A., Steinlechner S., Blank J.L. & Heldmaier G. 1993.Cold exposure and food restriction facilitate physiological responses to short photoperiod in Djungarian hamsters (Phodopus sungorus) // Journal of Experimental Zoology. Vol.267. P.104–112.

  • Ruf T. & Geiser F. 2015. Daily torpor and hibernation in birds and mammals // Biological Reviews. Vol.90. No.3. P.891–926.

  • Scherbarth F. & Steinlechner S. 2010. Endocrine mechanisms of seasonal adaptation in small mammals: from early results to present understanding // Journal of Comparative Physiology, B. Vol.180. No.7. P.935–952.

  • Sokolov V.E. & Orlov V.N. 1980. [Guide to Mammals of the Mongolian People’s Republic]. Moscow: Nauka. 351 p. [in Russian].

  • Sokolov V.E. & Vasilieva N.Y. 1993. [Behavior of the Campbell hamster (Phodopus campbelli Thomas, 1905) in nature: confirmation of the biological signal field theory] // Doklady Rossiiskoi Akademii Nauk. Vol.332. No.5. P.667–670 [in Russian with English summary].

  • Strauss A., Hoffmann I.E., Vielgrader H. & Millesi E. 2008. Testis development and testosterone secretion in captive European ground squirrels before, during, and after hibernation // Acta Theriologica. Vol.53. P.47–56.

  • Surov A.V. 2006. [Olfactory Signals in Sexual Behavior of Mammals]. Dissertation of Doctor of Science in Zoology. Moscow: AN. Severtsov Institute of Ecology and Evolution RAS. 190 p. [in Russian].

  • Turner J.M., Körtner G., Warnecke L., & Geiser F. 2012. Summer and winter torpor use by a free-ranging marsupial // Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. Vol.162. No.3. P.274–280.

  • Ushakova M.V., Kropotkina M.V., Feoktistova N.Yu. & Surov A.V. 2012. [Daily torpor in hamsters (Rodentia, Cricetidae)] // Russian Journal of Ecology. Vol.43. No.1. P.65–69 [in Russian].

  • Vasilieva N.Y., Surov A.V. & Telitsina A.Y. 1988. [Structure of the settlement and territory use in Campbell dwarf hamsters at the south of Tuva ASSR] // Rodents: Materials of 7th All-USSR Conference, Sverdlovsk. P.61–62 [in Russian].

  • Vasilieva N.Y. & Khrushchova A.M. 2010. [Nursing father — myth or reality? The role of secretions of father-male specific skin glands in survival and development of Campbell’s hamsters juveniles (Phodopus campbelli Thomas, 1905; Cricetidae, Rodentia)] // Zhurnal Obshchei Biologii. Vol.71. No.3. P.115–130 [in Russian with English summary].

  • Vasilieva N.Y., Khrushchova A.M., Kuptsov A.V., Shekarova O.N., Sokolova O.V., Wang D. & Rogovin K.A. 2020. On the winter enhancement of adaptive humoral immunity: hypothesis testing in desert hamsters (Phodopus roborovskii: Cricetidae, Rodentia) kept under long-day and short-day photoperiod // Integrative Zoology. Vol.15. No.3. P.232–247.

  • Wynne-Edwards K.E. 1987. Evidence for obligate monogamy in the Djungarian hamster, Phodopus campbelli: pup survival under different parenting conditions // Behavioral Ecology and Sociobiology. Vol.20. No.6. P.427–437.

  • Wynne-Edwards K.E. 1995. Biparental care in Djungarian but not Siberian dwarf hamster Phodopus // Animal Behaviour. Vol.50. P.1571–1585.

  • Wynne-Edwards K.E., Surov A.V. & Telitsyna A.Y. 1992. Field studies of chemical signaling: direct observation of dwarf hamster Phodopus in Soviet Asia // Doty R.J. & Muller-Schwarze D. (eds.). Chemical Signals in Vertebrates 6. New York: Springer. P.482–492.

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