Seasonal and diurnal variability of the body temperature in the northern white-breasted hedgehog (Erinaceus roumanicus) in normothermia

Rutovskaya M.V., Diatroptov M.E.

P. 103-114

Both during hibernation at normothermia and while the animals are active in summer the body temperature of hedgehogs fluctuates significantly in the range from 26 to 38°C. Seasonal variability in body temperature is related to reproduction and ambient temperature. During the breeding season in May and June, the body temperature of hedgehogs is significantly higher in both males and females comparing to other seasons. This is probably due to the period of active reproduction and seasonal variability in the hormones’ content in blood. The average daily body temperature in hedgehogs correlates with the ambient temperature in the summer months — May and June, when the night air temperatures do not differ much from those during daytime one and are of the optimal range for hedgehogs. In spring, at the end of summer, and in autumn, the ambient temperature may drop significantly, being out of the optimal range, and the animal body temperature does not always follow the ambient temperature changes, so no reliable correlation between them are observed. The body temperature of hedgehogs during the day is not constant: during the daytime rest in summer period, most hedgehogs have a lower body temperature, which probably saves energy. During the non-hibernation period, females usually have a higher body temperature comparing to males, which may be associated with physiological features and, in particular, with a higher metabolism. The photoperiod affects the duration of activity of hedgehogs and, accordingly, the time during which the body temperature of hedgehogs is elevated at night. During normothermia at the hibernation period, ultradian rhythms are observed for the animal body temperature with periods of 4.0–4.3 h; apparently, they are masked by the influence of other factors during the period of activity of hedgehogs.DOI: 10.15298/rusjtheriol.21.2.01

• Andreychev A.V., Kuznetsov V.A. & Lapshin A.S. 2010. [Northern white-breasted hedgehog in the mammalian fauna of Mordovia] // Ilyinskich N.N. (ed.). [Proceedings of the 2nd International Teleconference “Fundamental Sciences and Practice”, Tomsk]. Vol.1. No.3. P.55 [in Russian].
• Bannikova A.A., Kramerov D.A., Vasilenko V.N., Dzuev R.I. & Dolgov V.A. 2003. DNA polymorphism of Erinaceus hedgehogs and E. concolor taxon (Insectivora, Erinaceidae) // Zoologicheskii Zhurnal. Vol.82. No.1. P.70‒80 [in Russian, with English summary].
• Bannikova A.A., Lebedev V.S., Rutovskaya M.V., Khlyap L.A. & Rozhnov V.V. 2010. [Genetic identification and hybridization of common hedgehogs in Central Russia] // Rozhnov V.V. (ed.). [Proceedings of Conference “Integrity of the Species in Mammals: Isolating Barriers and Hybridization”]. Moscow: KMK Scientific Press. P.9 [in Russian].
• Blessing W. & Ootsuka Y. 2016. Timing of activities of daily life is jaggy: how episodic ultradian changes in body and brain temperature are integrated into this process // Temperature (Austin). Vol.3. No3. P.371‒383.
• Blum I.D., Zhu L., Moquin L., Kokoeva M.V., Gratton A., Giros B. & Storch K.F. 2014. A highly tunable dopaminergic oscillator generates ultradian rhythms of behavioral arousal // Elife. Vol.3. DOI:10.7554/eLife.05105
• Bogdanova A.S., Bannikova A.A., Pirusskii Yu.M. & Formozov N.A. 2009. The first genetic evidence of hybridization between West European and Northern white-breasted hedgehogs (Erinaceus europaeus and E. roumanicus) in Moscow Region // Biology Bulletin. Vol.36. No.6. P.647‒651.
• Bolfıkova B. & Hulva P. 2012. Microevolution of sympatry: landscape genetics of hedgehogs Erinaceus europaeus and E. roumanicus in Central Europe // Heredity. Vol.108. P.248–255.
• Bourguignon C. & Storch K.F. 2017. Control of rest: activity by a dopaminergic ultradian oscillator and the circadian clock // Frontiers in Neurology. Vol.8. P.614.
• Diatroptov M.E. 2011. Infradian fuctuations in serum testosterone levels in male laboratory rats // Bulletin of Experimental Biology and Medicine. Vol.151. P.638–641.
• Diatroptov M.E., Diatroptova M.A., Kosyreva A.M., Dzhalilova D.Sh., Mkhitarov V.A., Mikhailova L.P. & Makarova O.V. 2019a. [Ultradian rhythms of body temperatures of Wistar rats under conditions of permanent lightning] // Bulletin of Experimental Biology and Medicine. Vol.167. No.6. P.690‒694 [in Russian, with English summary].
• Diatroptov M.E., Rutovskaya M.V., Kuznetsova E.V., Diatroptova M.A., Kosyreva A.M., Dzhalilova D.Sh., Ponomarenko E.A., Panchelyuga V.A. & Stankevich A.A. 2019b. [Infradian and ultradian rhythmicity of body temperature recovery during hibernation] // Bulletin of Experimental Biology and Medicine. Vol.168. No.8. P.250‒254 [in Russian, with English summary].
• Diatroptov M.E., Slesarev S.M. & Slesareva E.V. 2017. Characteristics of 4-day infradian biorhythms in mature male Wistar rats after pinealectomy // Bulletin of Experimental Biology and Medicine. Vol.163. P.109–113.
• Filchagov A.V. 1988. [Daily activity and movement of common hedgehogs according to the materials of individual tracking] // Bulletin of Moscow Society of Naturalists. Biological Series. Vol.93. No.5. P.38–49 [in Russian].
• Fowler P.A. 1988. Thermoregulation in the female hedgehog, Erinaceus europaeus, during the breeding season // Journal of Reproduction and Fertility. Vol.82. P.285‒292.
• Fowler P.A. & Racey P.A. 1990. Daily and seasonal cycles of body temperature and aspects of heterothermy in the hedgehog Erinaceus europaeus // Journal of Comparative Physiology, B. Vol.160. P.299‒307.
• Frare C., Williams C. & Drew K.L. 2021. Thermoregulation in hibernating mammals: The role of the “thyroid hormones system” // Molecular and Cellular Endocrinology. Vol.519. No.5. P.111054.
• Gnaiger E. 1987. Optimum efficiencies of energy transformation in anoxic metabolism. The strategies of power and economy // Calow P. (ed.). Evolutionary Physiological Ecology. Cambridge: Cambridge University Press. P.7‒36.
• Gureev A.A. 1979. [Fauna of the USSR. Mammals, Vol.4. No.2. Insectivores]. Leningrad: Nauka. 502 p. [in Russian].
• Ikeno T. Williams C.T., Buck C.L., Barnes B.M. & Yan L. 2017. Clock gene expression in the suprachiasmatic nucleus of hibernating Arctic ground squirrels // Journal of Biological Rhythms. Vol.32. No.3. P.246–256.
• Jozsa R., Olah A., Cornélissen G., Csernus V., Otsuka K., Zeman M., Nagy G., Kaszaki J., Stebelova K., Csokas N., Pan W., Herold M., Bakken E.E. & Halberg F. 2005. Circadian and extracircadian exploration during day time hours of circulating corticosterone and other endocrine chronomes // Biomedicine & Pharmacotherapy. Vol.59. P.109–116.
• Kalabukhov N.I. 1985. [Hibernation of Mammals]. Moscow: Nauka. 264 p. [in Russian].
• Karaseva E.V., Gottfried A.B. & Dubinina N.V. 1979. [Lifestyle of common hedgehogs (Erinaceus europaeus) and their role in the natural focus of leptospirosis in the Yaroslavl region (according to observations of tagged individuals)] // Zoologicheskii Zhurnal. Vol.58. No.5. P.705–715 [in Russian].
• Krol E. 1994. Metabolism and thermoregulation in the eastern hedgehog Erinaceus concolor // Journal of Comparative Physiology, B. Vol.164. P.503–507.
• Kucheruk V.V. & Karaseva E.V. 1980. [Hedgehogs] // Kucheruk V.V. (ed.). [Results of Tagging Mammals]. Moscow: Nauka. P.47‒57 [in Russian].
• Li J., Nguyen V., French B.A., Parlow A.F., Su G.L., Fu P., Yuan Q.X. & French S.W. 2000. Mechanism of the alcohol cyclic pattern: role of the hypothalamic-pituitary-thyroid axis // American Journal of Physiology. Gastrointestinal and Liver Physiology. Vol.279. No.1. P.118‒125.
• Maschke C., Harder J., Cornélissen G., Hecht K., Otsuka K. & Halberg F. 2003. Chronoecoepidemiology of “strain”: chronomics of urinary cortisol and catecholamines during nightly exposure to noise // Biomedicine & Pharmacotherapy. Vol.57. P.126–135.
• Morris P.A. 1997. The Hedgehog // Shire Natural History, Vol.32. London: Bloomsbury Publishing. 24 p.
• Nicoll M.E. & Thompson S.D. 1987. Basal metabolic rates and energetics of reproduction in therian mammals: marsupials and placentals compared // Symposium of the Zoological Society of London. Vol.57. P.7–27.
• Ognev S.I. 1928. [Mammals of Eastern Europe and Northern Asia. Vol.1. Insectivores and Bats]. Moscow–Leningrad: Gosudarstvennoe Izdatel’stvo. 631 p. [in Russian].
• Petrovsky D.V., Novikov E.A. & Moshkin M.P. 2008. [Dynamics of body temperature of the mole vole (Ellobius talpinus, Rodentia, Cricetidae) in winter] // Zoologicheskii Zhurnal. Vol.87. No.12. P.1504–1508 [in Russian, with English summary].
• Pronina T.S. 1992. [Circadian and infradian rhythms of testosterone and aldosterone excretion in children] // Problemy Endokrinologii. Vol.38. No.5. P.38–42 [in Russian, with English summary].
• Reeve N.J. 1982. The home range of the hedgehog as revealed by a radio tracking study. Telemetric studies of vertebrates // Cheeseman C.L. & Mitson R.B. (eds.). Proceedings of a Symposium held at the Zoological Society of London. London: Academic Press. Vol.49. P.207–230.
• Reeve N.J. 1994. Hedgehogs. London: T. and A.D. Poyser. 313 p.
• Robu A.I. 1982. [Relationship of Endocrine Complexes Under Stress]. Chisinau: Shtiintsa. 208 p. [in Russian].
• Rutovskaya M.V., Diatroptov M.E., Kuznetzova E.V., Anufriev A.I., Feoktistova N. Y. & Surov A.V. 2019a. The dynamics of body temperature of the eastern European hedgehog (Erinaceus roumanicus) during winter hibernation // Biological Bulletin. Vol.46. No.9. P.1136–1145.
• Rutovskaya M.V., Diatroptov M.E., Kuznetsova E.V., Anufriev A.I., Feoktistova N.Yu. & Surov A.V. 2019b. The phenomenon of negative body temperature in hibernating hedgehogs of the genus Erinaceus // Journal of Evolutionary Biochemistry and Physiology. Vol.55. No.6. P.515–516.
• Saboureau M. & Castaing L. 1985. Hibernation and reproduction in the female hedgehog // Assenmacher I. & Biossin J. (eds.). Endocrine Regulations as Adaptive Mechanisms to the Environment. Paris: CNRS. P.191–208.
• Saboureau M., Laurent G. & Boissin J. 1979. Daily and seasonal rhythms of locomotor activity and adrenal function in male hedgehog (Erinaceus europaeus L.) // Journal of Interdisciplinary Cycle Research. Vol.10. P.245–266.
• Shkolnik A. & Schmidt-Nielsen K. 1976. Temperature regulation in hedgehogs from temperate and desert environments // Physiological Zoology. Vol.49. No.1. P.56–64.
• Tembotova F.A. 1997. [Hedgehogs of the Caucasus]. Nalchik: Publishing House KBSC RAS. 80 p. [in Russian].
• Upham N.S., Esselstyn J.A. & Jetz W. 2019. Inferring the mammal tree: species-level sets of phylogenies for questions in ecology, evolution, and conservation // PLoS Biology. Vol.17. No.12. P.e3000494.
• Williams C.T., Radonich M., Barnes B.M. & Buck C.L. 2017. Seasonal loss and resumption of circadian rhythms in hibernating arctic ground squirrels // Journal of Comparative Physiology, B. Vol.187. No.5–6. P.693–703.
• Zeman M., Józsa R., Cornélissen G., Stebelova K., Bubenik G., Olah A., Poeggeler B., Huether G., Hardeland R., Nagy G., Czernus V., Pan W., Otsuka K. & Halberg F. 2005. Chronomics: circadian lead of extrapineal vs. pineal melatonin rhythms with an infradian hypothalamic exploration // Biomedicine & Pharmacotherapy. Vol.59(1). P.213–219.
• Zolotareva K.I., Bannikova A.A., Belokon M.M., Belokon Y.S., Politov D.V., Rutovskaya M.V., Hlyap L.A., Starykov V.P. & Lebedev V.S. 2021. Genetic diversity and structure of the hedgehogs Erinaceus europaeus and Erinaceus roumanicus: evidence for ongoing hybridization in Eastern Europe // Biological Journal of the Linnaean Society. Vol.132. No.1. P.174–195.