[en] Winter activity of hibernating mammals is likely to be influenced by climate change. Our study focuses on Nyctalus noctula, a non-cavernous hibernator using artificial roosts in a recently colonized winter region. Using continuous acoustic monitoring and temperature measurements inside and outside the roosts, we found that bats exhibit a circadian cycle (active at night, resting during the day) even during hibernation season. Activity duration and intensity changed in response to ambient temperature, photoperiod, and hibernation progression. Warm ambient temperatures led to increased nighttime activity, extending the duration of the active phase. As photoperiod increased, the rest phase lengthened, while the overall magnitude of activity decreased from the beginning to the end of the hibernation period. Below 0 °C vocal activity was nearly zero indicating a minimal probability of bat activity during both day and night. The species recent success in extending its hibernation range northward may be attributed to its flexible adjustment to prevailing environmental conditions. Nevertheless, it remains uncertain whether engaging in daily activity at temperatures above 0 °C confers any advantages at northern latitudes to prevent premature energy depletion. The persistence of circadian activity during winter could be a relic behavior, adapted from historical patterns of wintering in insect-rich and warm southern latitudes.
Disciplines :
Sciences de l’environnement & écologie
Auteur, co-auteur :
KRAVCHENKO, Kseniia ; University of Luxembourg > Faculty of Science, Technology and Medicine (FSTM) > Department of Engineering (DoE)
Furmankiewicz, Joanna; Department of Behavioral Ecology, University of Wrocław, Wrocław, Poland
Co-auteurs externes :
yes
Langue du document :
Anglais
Titre :
The interplay of temperature and circadian periodicity in winter activity of non-cavernous hibernator, Nyctalusnoctula.
Kseniia Kravchenko was supported by the Teraz Wroclaw program (http://study-in-wroclaw.pl/) for full tuition coverage for the Master's program at Wroclaw University.
Avery, M.I., Winter activity of pipistrelle bats. J. Anim. Ecol. 54 (1985), 721–738, 10.2307/4374.
Avery, M.I., The winter activity of noctule bats (Nyctalus noctula). J. Zool. 209 (1986), 296–299, 10.1111/j.1469-7998.1986.tb03590.x.
Ben-Hamo, M., Munoz-Garcia, A., Williams, J.B., Korine, C., Pinshow, B., Waking to drink: rates of evaporative water loss determine arousal frequency in hibernating bats. J. Exp. Biol. 216 (2013), 573–577, 10.1242/jeb.078790.
Bernard, R.F., Willcox, E.V., Jackson, R.T., Brown, V.A., McCracken, G.F., Feasting, not fasting: winter diets of cave hibernating bats in the United States. Front. Zool. 18 (2021), 1–13, 10.1186/s12983-021-00434-9.
Bihari, Z., The roost preference of Nyctalus noctula (Chiroptera, Vespertilionidae) in summer and the ecological background of their urbanization. Mammalia mamm 68 (2004), 329–336, 10.1515/mamm.2004.032.
Boyles, J.G., McKechnie, A.E., Energy conservation in hibernating endotherms: why “suboptimal” temperatures are optimal. Ecol. Model. 221:12 (2010), 1644–1647, 10.1016/j.ecolmodel.2010.03.018.
Boyles, J.G., Robbins, L.W., Characteristics of summer and winter roost trees used by evening bats (Nycticeius humeralis) in Missouri. Am. Midl. Nat. 155 (2006), 210–220, 10.1674/0003-0031(2006)155[0210:COSAWR]2.0 CO;2.
Boyles, J.G., Dunbar, M.B., Whitaker, J.O., Activity following arousal in winter in North American vespertilionid bats. Mamm Rev. 36 (2006), 267–280, 10.1111/j.1365-2907.2006.00095.x.
Celuch, M., Kanuch, P., Winter activity and roosts of the noctule (Nyctalus noctula) in an urban area (Central Slovakia). Lynx 36 (2005), 39–45.
Cohen, J., Screen, J.A., Furtado, J.C., Barlow, M., Whittleston, D., Coumou, D., et al. Recent Arctic amplification and extreme mid-latitude weather. Nat. Geosci., 7(9), 2014, 627, 10.1038/ngeo2234.
Cryan, P.M., Veilleux, J.P., Migration and use of autumn, winter, and spring roosts by tree bats. Lacki, M., Hayes, J., Kurta, A., (eds.) Conservation and Management of Bats in Forests, 2007, John Hopkins University Press, Baltimore, MD, 153–175.
Currie, S.E., Noy, K., Geiser, F., Passive rewarming from torpor in hibernating bats: minimizing metabolic costs and cardiac demands. Am. J. Physiol. Regul. Integr. Comp. Physiol. 308:1 (2014), R34–R41, 10.1152/ajpregu.00341.2014.
Czenze, Z.J., Park, A.D., Willis, C.K., Staying cold through dinner: cold-climate bats rewarm with conspecifics but not sunset during hibernation. J. Comp. Physiol. B 183 (2013), 859–866, 10.1007/s00360-013-0753-4.
Dietz, C., Nill, D., von Helversen, O., Bats of Britain, Europe and Northwest Africa. 2009, A & C Black.
Dubicki, A., Dubicka, M., Szymanowski, M., Klimat wrocławia. Smolnicki, K., Szykasiuk, M., (eds.) Środowisko Wrocławia—Informator, 2002, Dolnośląska Fundacja Ekorozwoju, Wrocław, 9–20 (In Polish.).
Fleming, T.H., Eby, P., Ecology of bat migration. Kunz, T.H., Fenton, M.B., (eds.) Bat Ecology, 2003, University of Chicago Press, Chicago, Illinois, 156–208.
Furmankiewicz, J., Kucharska, M., Migration of bats along a large river valley in southwestern Poland. J. Mammal. 90 (2009), 1310–1317, 10.1644/09-MAMM-S-099R1.1.
Furmankiewicz, J., Ruczynski, I., Urban, R., Jones, G., Social calls provide tree-dwelling bats with information about the location of conspecifics at roosts. Ethology 117 (2011), 480–489, 10.1111/j.1439-0310.2011.01897.x.
Gazarian, Наблюдения за зимовкой рыжих вечерни⃛ в дуплах деревьев в предкавказье. Plecotus 5 (2002), 28–34.
Gebhard, J., Nyctalus noctula – Beobachtungen an einem traditionellen Winterquartier in Fels. Myotis 21–22 (1984), 163–170.
Gebhard, J., Observations on the mating behaviour of Nyctalus noctula (Schreber, 1774) in the hibernaculum. Myotis 32–33 (1995), 123–129.
Geiser, F., Metabolic rate and body temperature reduction during hibernation and daily torpor. Annu. Rev. Physiol. 66 (2004), 239–274, 10.1146/annurev.physiol.66.032102.115105.
Geiser, F., Drury, R.L., Kortner, G., Turbill, C., Pavey, C.R., Brigham, R.M., Passive rewarming from torpor in mammals and birds: energetic, ecological and evolutionary implications. Barnes, B.M., Carey, H.V., (eds.) Life in the Cold: Evolution, Mechanisms, Adaptation, and Application, 2004, Inkworks, Fairbanks, AK, 51–62.
Georgiev, D.G., Stoycheva, S.B., Flight activity of Nyctalus noctula bats (SCHREBER, 1774) (Mammalia: chiroptera) close to their winter colonies in the town area of Stara Zagora, Southern Bulgaria. Animalia 42 (2006), 161–166.
Godlevska, L.V., Northward expansion of the winter range of Nyctalus noctula (chiroptera: vespertilionidae) in eastern Europe. Mammalia 79 (2015), 315–324, 10.1515/mammalia-2013-0178.
Halle, S., Stenseth, N.C., (eds.) Activity Patterns in Small Mammals: an Ecological Approach, vol. 141, 2012, Springer.
Hayman, D.T., Cryan, P.M., Fricker, P.D., Dannemiller, N.G., Long‐term video surveillance and automated analyses reveal arousal patterns in groups of hibernating bats. Methods Ecol. Evol. 8:12 (2017), 1813–1821, 10.1111/2041-210x.12823.
Hope, P.R., Jones, G., Warming up for dinner: torpor and arousal in hibernating Natterer's bats (Myotis nattereri) studied by radiotelemetry. J. Comp. Physiol. B 182 (2012), 569–578, 10.1007/s00360-011-0631-x.
Hope, P.R., Jones, G., An entrained circadian cycle of peak activity in a population of hibernating bats. J. Mammal. 94 (2013), 497–505, 10.1644/12-MAMM-A-095.1.
Horn, J., Temperaturuntersuchung in winterquartierkasten. Mitteilungen des LFA. Saugetierkunde Branderburg-Berlin 23 (2015), 2–3.
Hutterer, R., Ivanova, T., Meyer-Cordes, C., Rodrigues, L., Bat migrations in Europe—a review of banding data and literature. Naturschutz, Biologie und Vielfalt, 28, 2005.
Jonasson, K.A., Willis, C.K.R., Hibernation energetics of little brown bats. J. Exp. Biol. 215 (2012), 2141–2149, 10.1242/jeb.066514.
Jones, G., Duverge, P.L., Ransome, R.D., Conservation biology of an endangered species: field studies of greater horseshoe bats. Symp. Zool. Soc. Lond. 67 (1995), 309–324, 10.1093/oso/9780198549451.003.0020.
Kanuch, P.I., Celuch, M., Výskyt Nyctalus noctula v panelových budovách mesta Prešov v rokoch 1998–1999 (The occurrence of Nyctalus noctula in prefab houses in Prešov in 1998–1999 (E-Slovakia)). Vespertilio 4 (2000), 146–148 (in Slovak with English abstract).
Kepel, A., Ciechanowski, M., Jaros, R., Wytyczne dotyczące oceny oddziaływania elektrowni wiatrowych na nietoperze. Generalna Dyrekcja Ochrony Środowiska, Warszawa, 2011 (In Polish).
Klüg-Baerwald, B.J., Lausen, C.L., Willis, C.K., Brigham, R.M., Home is where you hang your bat: winter roost selection by prairie-living big brown bats. J. Mammal. 98:3 (2017), 752–760, 10.1093/jmammal/gyx039.
Klüg-Baerwald, B.J., Lausen, C.L., Burns, S.M., Brigham, R.M., Physiological and behavioural adaptations by big brown bats hibernating in dry rock crevices. J. Comp. Physiol. B (2024), 1–10, 10.1007/s00360-024-01546-4.
Körtner, G., Geiser, F., The temporal organization of daily torpor and hibernation: circadian and circannual rhythms. Chronobiol. Int. 17:2 (2000), 103–128, 10.1081/cbi-100101036.
Kravchenko, K., Vlaschenko, A., Prylutska, A., Rodenko, O., Hukov, V., Shuvaev, V., Year-round monitoring of bat records in an urban area: kharkiv (NE Ukraine), 2013, as a case study. Turk. J. Zool. 41 (2017), 530–548, 10.3906/zoo-1602-51.
Kravchenko, K.A., Vlaschenko, A.S., Lehnert, L.S., Courtiol, A., Voigt, C.C., Generational shift in the migratory common noctule bat: first-year males lead the way to hibernacula at higher latitudes. Biol. Lett., 16(9), 2020, 20200351, 10.1098/rsbl.2020.0351.
Kunz, T.H., Lumsden, L.F., Fenton, M.B., Ecology of cavity and foliage roosting bats. Bat ecology 1 (2003), 3–89.
Lee, K., Park, J.Y., Yoo, W., Gwag, T., Lee, J.W., Byun, M.W., Choi, I., Overcoming muscle atrophy in a hibernating mammal despite prolonged disuse in dormancy: proteomic and molecular assessment. J. Cell. Biochem. 104 (2008), 642–656, 10.1002/jcb.21653.
Lee, K., So, H., Gwag, T., Ju, H., Lee, J.W., Yamashita, M., Choi, I., Molecular mechanism underlying muscle mass retention in hibernating bats: role of periodic arousal. J. Cell. Physiol. 222 (2010), 313–319, 10.1002/jcp.21952.
Lupicki, D., Szkudlarek, R., Cichocki, J., Ciechanowski, M., Zimowanie borowca wielkiego Nyctalus noctula (Schreiber, 1774) w Polsce. Nietoperze 8 (2007), 27–38.
Lyman, C.P., Mechanisms of arousal. Lyman, C.P., Willis, J.S., Malan, A., Wang, L.C.H., (eds.) Hibernation and Torpor in Mammals and Birds, 1982, Academic Press, New York, 104–123.
McNab, B.K., The Physiological Ecology of Vertebrates: a View from Energetics. 2002, Cornell University Press.
Moiseienko, M., Vlaschenko, A., Deep torpor patterns and body mass loss of above-ground hibernating bats (Nyctalus noctula) in captivity—effects of sex, age, and grouping. Acta Chiropterol. 25:2 (2023), 299–310, 10.3161/15081109acc2023.25.2.009.
Nievergelt, Y., Fourier series for periodic functions. Wavelets Made Easy, 2013, Birkhäuser, New York, NY, 175–201, 10.1007/978-1-4614-6006-0_6.
Park, K.J., Jones, G., Ransome, R.D., Winter activity of a population of greater horseshoe bats (Rhinolophus ferrumequinum). J. Zool. 248 (1999), 419–427, 10.1111/j.1469-7998.1999.tb01041.x.
Park, K.J., Jones, G., Ransome, R.D., Torpor, arousal and activity of hibernating greater horseshoe bats (Rhinolophus ferrumequinum). Funct. Ecol. 14 (2000), 580–588, 10.1046/j.1365-2435.2000.t01-1-00460.x.
Pfalzer, G., Kusch, J., Structure and variability of bat social calls: implications for specificity and individual recognition. J. Zool. 261 (2003), 21–33, 10.1017/S0952836903003935.
Racey, P.A., Speakman, J.R., The energy costs of pregnancy and lactation in heterothermic bats. Loudon, A.S.I., Racey, P.A., (eds.) Reproductive Energetics in Mammals. Symp Zool Soc Lond, vol. 57, 1987, 107–125.
Reeder, D.M., Frank, C.L., Turner, G.G., Meteyer, C.U., Kurta, A., Britzke, E.R., et al. Frequent arousal from hibernation linked to severity of infection and mortality in bats with white-nose syndrome. PLoS One, 7, 2012, e38920, 10.1371/journal.pone.0038920.
Rousset, F., Ferdy, J.B., Courtiol, A., spaMM: Mixed-Effect Models, with or without Spatial Random Effects. 2014, 10.32614/CRAN.package spaMM.
Ruf, T., Arnold, W., Mechanisms of social thermoregulation in hibernating alpine marmots (Marmota marmota). Life in the Cold: Eleventh International Hibernation Symposium, 2000, Springer Berlin Heidelberg, Berlin, Heidelberg, 81–94.
Ruf, T., Geiser, F., Daily torpor and hibernation in birds and mammals. Biol. Rev. 90:3 (2015), 891–926, 10.1111/brv.12137.
Schmidt, A., Zum Überwinterungsverhalten des Abendseglers Nyctalus noctula in Ostbrandenburg. Nyctalus 15 (2010), 223–234.
Sluiter, J.W., Van Heerdt, P.F., Distribution and abundance of bats in S. Limburg from 1958 till 1962. Natuurhist. Maandbl. 53:11/12 (1964), 164–173.
Speakman, J.R., Racey, P.A., Hibernal ecology of the pipistrelle bat: energy expenditure, water requirements and mass loss, implications for survival and the function of winter emergence flights. J. Anim. Ecol. 58 (1989), 797–813, 10.2307/5125.
Speakman, J.R., Thomas, D.W., Physiological ecology and energetics of bats. Kunz, T.H., Fenton, M.B., (eds.) Bat Ecology, 2003, University of Chicago Press, Chicago, 430–490.
Stawski, C., Willis, C.K.R., Geiser, F., The importance of temporal heterothermy in bats. J. Zool. 292:2 (2014), 86–100, 10.1111/jzo.12105.
Strelkov, P.P., Migratory and stationary bats (chiroptera) of the European part of the soviet union. Acta Zoologica Cracoviensia 14 (1969), 393–440.
Thomas, D.W., Dorais, M., Bergeron, J., Winter energy budgets and cost of arousals for hibernating little brown bats, Myotis lucifugus. J. Mammal. 71 (1990), 475–479, 10.2307/1381967.
Turbill, D.W., Winter activity of Australian tree-roosting bats: influence of temperature and climatic patterns. J. Zool. 276 (2008), 285–290, 10.1111/j.1469-7998.2008.00487.x London.
Turbill, C., Geiser, F., Hibernation by tree-roosting bats. J. Comp. Physiol. B, 178, 2008, 597, 10.1007/s00360-007-0249-1.
Voigt, C.C., Lehnert, L.S., Popa-Lisseanu, A.G., Ciechanowski, M., Estók, P., Gloza-Rausch, F., Kramer-Schadt, S., The trans-boundary importance of artificial bat hibernacula in managed European forests. Biodivers. Conserv. 23 (2014), 617–631, 10.1007/s10531-014-0620-y.
Walther, G.R., Post, E., Convey, P., Menzel, A., Parmesan, C., Beebee, T.J., et al. Ecological responses to recent climate change. Nature 416 (2002), 389–395, 10.1038/416389a.
Williams, C.B., Studies in the effect of weather conditions on the activity and abundance of insect populations. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 244 (1961), 331–378, 10.1098/rstb.1961.0011.
Willis, C.K., Brigham, R.M., Social thermoregulation exerts more influence than microclimate on forest roost preferences by a cavity-dwelling bat. Behav. Ecol. Sociobiol. 62 (2007), 97–108, 10.1007/s00265-007-0442-y.
Zahn, A., Clauss, B., Winteraktivität des Abendseglers (Nyctalus noctula) in Südbayern. Nyctalus 9 (2003), 99–104.
Zahn, A., Kriner, E., Winter foraging activity of Central European Vespertilionid bats. Mammalian Biology-Zeitschrift für Säugetierkunde 81 (2016), 40–45, 10.1016/j.mambio.2014.10.005.
Zahn, A., Christoph, C., Christoph, L., Kredler, M., Reitmeier, A., Reitmeier, F., Schachenmeier, A., Schott, T., Die Nutzung von Spaltenquartieren an Gebäuden durch Abendsegler (Nyctalus noctula) in Südostbayern. Myotis 37 (2000), 61–76.