[en] Predicting species range shifts in response to environmental change requires the determination of regions where individuals maintain a positive energy budget. For hibernating animals, this budget depends on two physiological states (normothermy and torpor) that alternate in response to ambient temperature. To study range shifts of hibernators like the common noctule (Nyctalus noctula), we developed an ecophysiological approach that integrates metabolic rates, physiological states, and environmental conditions. Our model accurately hindcasted the northward range shift of this migratory bat over the past 50 years. Under climate change forecasts SSP1-2.6, SSP2-4.5, SSP3-7.0, and SSP5-8.5, for which winters will shorten by 1.4-41 days and warm by 0.11°C-2.3°C, the hibernation area is predicted to shift by 78-732 km and expand north-eastward by 5.8%-14% by 2100. Mean ambient temperature and winter duration prove sufficient to approximate the hibernation niche and may be used to predict changes in hibernation areas where collecting physiological measurements is difficult.
Disciplines :
Environmental sciences & ecology
Author, co-author :
KRAVCHENKO, Kseniia ; University of Luxembourg ; Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany ; Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland ; Ukrainian Bat Rehabilitation Center of NGO "Ukrainian Independent Ecology Institute", Kharkiv, Ukraine
Voigt, Christian C ; Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany ; Institute of Biochemistry and Biology, University of Potsdam, Potsdam, Germany
Volkholz, Jan ; Department of Transformation Pathways, Potsdam Institute for Climate Impact Research, Potsdam, Germany
Courtiol, Alexandre ; Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany
Currie, Shannon E ; Leibniz Institute for Zoo and Wildlife Research, Berlin, Germany ; School of BioSciences, University of Melbourne, Parkville, Australia
External co-authors :
yes
Language :
English
Title :
Shorter and Warmer Winters Expand the Hibernation Area of Bats in Europe.
Alexander von Humboldt-Stiftung Deutscher Akademischer Austauschdienst
Funding text :
Funding: Deutscher Akademischer Austauschdienst, grant 57214224 (K.K.); Alexander von Humboldt-Stiftung, grant AUS-1164625-HFST-P (S.E.C.). We thank Dr. Stefan Lange for having provided us with guidance on which climate projection models to use. We thank Dr. Jochen Klar for assisting us with the access and preparation of climate data. We thank the staff of the Field Research Station Niederfinow, and especially Irina Kasprzak, Ervin Havic, and Jerzy Kasprzak for continuous support and assistance during the experimental phase of the research. We also thank Lea Gajewski and Sofia Hayden Bofill for their help in the maintenance/care of animals. We thank Dr. Nicolas Fasel for cheerfully supporting K.K. during the manuscript preparation and guidance through the \u2018torpor\u2019 package. K.K. also expresses gratitude to Prof. Philippe Christe and Prof. Antoine Guisan for fostering an excellent working environment during her time at UNIL, while working on the manuscript. Additionally, special thanks to Dr. Olivier Broennimann for providing valuable advice on the hibernation niche. K.K. also thanks Prof. Christian Vincenot for his support and for allowing her to work on this project during her time at the University of Luxembourg. We thank Dr. Olivia Judson for commenting on our manuscript. We thank Leonie F Walter for help during the editing process. We thank editor Dr. Jonathan Lenoir, reviewer Dr. Mari A Fjelldal, and two anonymous reviewers for providing helpful criticisms and suggestions. We thank Prof. Anders Hedenstr\u00F6m for his guidance with aerodynamic modeling and the \u2018afpt\u2019 package. We thank all the members of the Ukrainian Bat Rehabilitation Center and salute their courage and dedication to continue monitoring and rescuing bats despite the hardship of warfare in Kharkiv, Ukraine. Open Access funding enabled and organized by Projekt DEAL.Deutscher Akademischer Austauschdienst, grant 57214224 (K.K.); Alexander von Humboldt\u2010Stiftung, grant AUS\u20101164625\u2010HFST\u2010P (S.E.C.). Funding:
Allison, A. Z. T., C. J. Conway, and A. E. Morris. 2023. “Why Hibernate? Tests of Four Hypotheses to Explain Intraspecific Variation in Hibernation Phenology.” Functional Ecology 37, no. 6: 1580–1593. https://doi.org/10.1111/1365-2435.14322.
Arlettaz, R., C. Ruchet, J. Aeschimann, E. Brun, M. Genoud, and P. Vogel. 2000. “Physiological Traits Affecting the Distribution and Wintering Strategy of the Bat Tadarida teniotis.” Ecology 81, no. 4: 1004–1014. https://doi.org/10.1890/0012-9658(2000)081[1004:PTATDA]2.0.CO;2.
Bestion, E., A. Teyssier, M. Richard, J. Clobert, and J. Cote. 2015. “Live Fast, Die Young: Experimental Evidence of Population Extinction Risk due to Climate Change.” PLoS Biology 13, no. 10: e1002281. https://doi.org/10.1371/journal.pbio.1002281.
Boyles, J. G., V. Brack Jr., K. E. Marshall, and D. Brack. 2024. “Shifts in Population Density Centers of a Hibernating Mammal Driven by Conflicting Effects of Climate Change and Disease.” Global Change Biology 30, no. 1: e17035. https://doi.org/10.1111/gcb.17035.
Boyles, J. G., F. Seebacher, B. Smit, and A. E. McKechnie. 2011. “Adaptive Thermoregulation in Endotherms May Alter Responses to Climate Change.” Integrative and Comparative Biology 51, no. 5: 676–690. https://doi.org/10.1093/icb/icr053.
Briscoe, N. J., S. D. Morris, P. D. Mathewson, et al. 2023. “Mechanistic Forecasts of Species Responses to Climate Change: The Promise of Biophysical Ecology.” Global Change Biology 29, no. 6: 1451–1470. https://doi.org/10.1111/gcb.16557.
Buck, C. L., and B. M. Barnes. 2000. “Effects of Ambient Temperature on Metabolic Rate, Respiratory Quotient, and Torpor in an Arctic Hibernator.” American Journal of Physiology-Regulatory, Integrative and Comparative Physiology 279, no. 1: R255–R262. https://doi.org/10.1152/ajpregu.2000.279.1.R255.
Buckley, L. B., B. Briones Ortiz, I. Caruso, et al. 2022. “TrenchR: Tools for Microclimate and Biophysical Ecology [Computer software].” https://trenchproject.github.io/TrenchR/.
Buckley, L. B., I. Khaliq, D. L. Swanson, and C. Hof. 2018. “Does Metabolism Constrain Bird and Mammal Ranges and Predict Shifts in Response to Climate Change?” Ecology and Evolution 8, no. 24: 12375–12385. https://doi.org/10.1002/ece3.4537.
Caro, S. P., S. V. Schaper, R. A. Hut, G. F. Ball, and M. E. Visser. 2013. “The Case of the Missing Mechanism: How Does Temperature Influence Seasonal Timing in Endotherms?” PLoS Biology 11, no. 4: e1001517. https://doi.org/10.1371/journal.pbio.1001517.
Chmura, H. E., C. Duncan, G. Burrell, B. M. Barnes, C. L. Buck, and C. T. Williams. 2023. “Climate Change is Altering the Physiology and Phenology of an Arctic Hibernator.” Science 380, no. 6647: 846–849. https://doi.org/10.1126/science.adf5341.
Currie, S. E., C. Stawski, and F. Geiser. 2018. “Cold-Hearted Bats: Uncoupling of Heart Rate and Metabolism During Torpor at Subzero Temperatures.” Journal of Experimental Biology 221: jeb.170894. https://doi.org/10.1242/jeb.170894.
Dunbar, M. B., and T. E. Tomasi. 2006. “Arousal Patterns, Metabolic Rate, and an Energy Budget of Eastern Red Bats (Lasiurus borealis) in Winter.” Journal of Mammalogy 87, no. 6: 1096–1102. https://doi.org/10.1644/05-MAMM-A-254R3.1.
Fasel, N. J., C. Vullioud, and M. Genoud. 2022. “Assigning Metabolic Rate Measurements to Torpor and Euthermy in Heterothermic Endotherms: ‘Torpor’, a New Package for R.” Biology Open 11, no. 4: bio059064. https://doi.org/10.1242/bio.059064.
Fjelldal, M. A., A. S. Muller, I. I. Ratikainen, C. Stawski, and J. Wright. 2023. “The Small-Bat-in-Summer Paradigm: Energetics and Adaptive Behavioural Routines of Bats Investigated Through a Stochastic Dynamic Model.” Journal of Animal Ecology 92: 2078–2093. https://doi.org/10.1111/1365-2656.13999.
Frieler, K., J. Volkholz, S. Lange, et al. 2023. “Scenario Setup and Forcing Data for Impact Model Evaluation and Impact Attribution Within the Third Round of the Inter-Sectoral Impact Model Intercomparison Project (ISIMIP3a).” Geoscientific Model Development 17, no. 1: 1–51. https://doi.org/10.5194/egusphere-2023-281.
Gebhard, J. 1984. “Nyctalus noctula – Beobachtungen an Einem Traditionellen Winterquartier im Fels.” Myotis 21, no. 22: 163–170.
Geiser, F. 2021. Ecological Physiology of Daily Torpor and Hibernation. Springer. https://rune.une.edu.au/web/handle/1959.11/31648.
Godlevska, L. V. 2015. “Northward Expansion of the Winter Range of Nyctalus noctula (Chiroptera: Vespertilionidae) in Eastern Europe.” Mammalia 79, no. 3: 315–324. https://doi.org/10.1515/mammalia-2013-0178.
Hranac, C. R., C. G. Haase, N. W. Fuller, et al. 2021. “What is Winter? Modeling Spatial Variation in Bat Host Traits and Hibernation and Their Implications for Overwintering Energetics.” Ecology and Evolution 11, no. 17: 11604–11614. https://doi.org/10.1002/ece3.7641.
Humphries, M. M., D. W. Thomas, and J. R. Speakman. 2002. “Climate-Mediated Energetic Constraints on the Distribution of Hibernating Mammals.” Nature 418, no. 6895: 313–316. https://doi.org/10.1038/nature00828.
Kearney, M. R., and W. P. Porter. 2017. “NicheMapR – an R Package for Biophysical Modelling: The Microclimate Model.” Ecography 40, no. 5: 664–674. https://doi.org/10.1111/ecog.02360.
Kooijman, S. A. L. M. 2010. Dynamic Energy Budget Theory for Metabolic Organisation. Cambridge University Press.
Kravchenko, K. A., A. S. Vlaschenko, L. S. Lehnert, A. Courtiol, and C. c. Voigt. 2020. “Generational Shift in the Migratory Common Noctule Bat: First-Year Males Lead the Way to Hibernacula at Higher Latitudes.” Biology Letters 16, no. 9: 20200351. https://doi.org/10.1098/rsbl.2020.0351.
Kravchenko, K. A., A. S. Vlaschenko, A. Prylutska, O. Rodenko, V. Hukov, and V. Shuvaev. 2017. “Year-Round Monitoring of Bat Records in an Urban Area: Kharkiv (NE Ukraine), 2013, as a Case Study.” Turkish Journal of Zoology 41, no. 3: 530–548. https://doi.org/10.3906/zoo-1602-51.
Lange, S., and M. Büchner. 2021. ISIMIP3b Bias-Adjusted Atmospheric Climate Input Data (Version 1.1) [Dataset]. ISIMIP Repository. https://doi.org/10.48364/ISIMIP.842396.1.
Lange, S., M. Mengel, S. Treu, and M. Büchner. 2023. ISIMIP3a Atmospheric Climate Input Data (v1.2). ISIMIP Repository. https://doi.org/10.48364/ISIMIP.982724.2.
Lange, S., D. Quesada-Chacón, and M. Büchner. 2023. Secondary ISIMIP3b Bias-Adjusted Atmospheric Climate Input Data (Version 1.3) [Dataset]. ISIMIP Repository. https://doi.org/10.48364/ISIMIP.581124.3.
Lehnert, L. S., S. Kramer-Schadt, T. Teige, et al. 2018. “Variability and Repeatability of Noctule Bat Migration in Central Europe: Evidence for Partial and Differential Migration.” Proceedings of the Royal Society B: Biological Sciences 285, no. 1893: 20182174. https://doi.org/10.1098/rspb.2018.2174.
Lighton, J. R. B. 2008. Measuring Metabolic Rates: A Manual for Scientists. Oxford University Press.
Lindecke, O., S. E. Currie, N. J. Fasel, et al. 2023. “Common Noctule Nyctalus noctula (Schreber, 1774).” In Handbook of the Mammals of Europe, edited by K. Hackländer and F. E. Zachos, 1–25. Springer International Publishing. https://doi.org/10.1007/978-3-319-65038-8_63-3.
Łupicki, D., R. Szkudlarek, J. Cichocki, and M. Ciechanowski. 2007. “The Wintering of Noctule Bat Nyctalus noctula (Schreber, 1774) in Poland.” Nietoperze 8, no. 1–2: 13–24.
McCracken, G. F., R. F. Bernard, M. Gamba-Rios, et al. 2018. “Rapid Range Expansion of the Brazilian Free-Tailed Bat in the Southeastern United States, 2008–2016.” Journal of Mammalogy 99, no. 2: 312–320. https://doi.org/10.1093/jmammal/gyx188.
Nunez, S., E. Arets, R. Alkemade, C. Verwer, and R. Leemans. 2019. “Assessing the Impacts of Climate Change on Biodiversity: Is Below 2°C Enough?” Climatic Change 154, no. 3: 351–365. https://doi.org/10.1007/s10584-019-02420-x.
Parmesan, C. 2006. “Ecological and Evolutionary Responses to Recent Climate Change.” Annual Review of Ecology, Evolution, and Systematics 37, no. 1: 637–669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100.
Perez-Navarro, M. A., O. Broennimann, M. A. Esteve, G. Bagaria, A. Guisan, and F. Lloret. 2022. “Comparing Climatic Suitability and Niche Distances to Explain Populations Responses to Extreme Climatic Events.” Ecography 2022, no. 11: e06263. https://doi.org/10.1111/ecog.06263.
Perry, R. W. 2018. “Migration and Recent Range Expansion of Seminole Bats (Lasiurus seminolus) in the United States.” Journal of Mammalogy 99, no. 6: 1478–1485. https://doi.org/10.1093/jmammal/gyy135.
Pohl, H. 1961. “Temperaturregulation und Tagesperiodik des Stoffwechsels bei Winterschläfern.” Zeitschrift für Vergleichende Physiologie 45, no. 2: 109–153. https://doi.org/10.1007/BF00297762.
R Core Team. 2023. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing. https://www.R-project.org/.
Radchuk, V., T. Reed, C. Teplitsky, et al. 2019. “Adaptive Responses of Animals to Climate Change are Most Likely Insufficient.” Nature Communications 10, no. 1: 3109. https://doi.org/10.1038/s41467-019-10924-4.
Reher, S., J. Ehlers, H. Rabarison, and K. H. Dausmann. 2018. “Short and Hyperthermic Torpor Responses in the Malagasy Bat Macronycteris Commersonireveal a Broader Hypometabolic Scope in Heterotherms.” Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 188, no. 6: 1015–1027. https://doi.org/10.1007/s00360-018-1171-4.
Richter, M. M., C. T. Williams, T. N. Lee, et al. 2015. “Thermogenic Capacity at Subzero Temperatures: How Low can a Hibernator Go?” Physiological and Biochemical Zoology 88, no. 1: 81–89. https://doi.org/10.1086/679591.
Rousset, F., and J.-B. Ferdy. 2014. “Testing Environmental and Genetic Effects in the Presence of Spatial Autocorrelation.” Ecography 37, no. 8: 781–790. https://doi.org/10.1111/ecog.00566.
Ruf, T., and F. Geiser. 2015. “Daily Torpor and Hibernation in Birds and Mammals.” Biological Reviews 90, no. 3: 891–926. https://doi.org/10.1111/brv.12137.
Ruf, T., S. Giroud, and F. Geiser. 2022. “Hypothesis and Theory: A Two-Process Model of Torpor-Arousal Regulation in Hibernators.” Frontiers in Physiology 13: 901270. https://doi.org/10.3389/fphys.2022.901270.
Sachanowicz, K., M. Ciechanowski, P. Tryjanowski, and J. Z. Kosicki. 2019. “Wintering Range of Pipistrellus nathusii (Chiroptera) in Central Europe: Has the Species Extended to the North-East Using Urban Heat Islands?” Mammalia 83, no. 3: 260–271. https://doi.org/10.1515/mammalia-2018-0014.
Scheffers, B. R., L. De Meester, T. C. L. Bridge, et al. 2016. “The Broad Footprint of Climate Change From Genes to Biomes to People.” Science 354, no. 6313: aaf7671. https://doi.org/10.1126/science.aaf7671.
Seebacher, F., C. R. White, and C. E. Franklin. 2015. “Physiological Plasticity Increases Resilience of Ectothermic Animals to Climate Change.” Nature Climate Change 5, no. 1: 61–66. https://doi.org/10.1038/nclimate2457.
Sellar, A. A., C. G. Jones, J. P. Mulcahy, et al. 2019. “UKESM1: Description and Evaluation of the U.K. Earth System Model.” Journal of Advances in Modeling Earth Systems 11, no. 12: 4513–4558. https://doi.org/10.1029/2019MS001739.
Soberon, J., and A. T. Peterson. 2005. “Interpretation of Models of Fundamental Ecological Niches and Species' Distributional Areas.” Biodiversity Informatics 2: 1–10. https://doi.org/10.17161/bi.v2i0.4.
Taylor, L. R. 1963. “Analysis of the Effect of Temperature on Insects in Flight.” Journal of Animal Ecology 32, no. 1: 99–117. https://doi.org/10.2307/2520.
Turbill, C., G. Körtner, and F. Geiser. 2008. “Timing of the Daily Temperature Cycle Affects the Critical Arousal Temperature and Energy Expenditure of Lesser Long-Eared Bats.” Journal of Experimental Biology 211, no. 24: 3871–3878. https://doi.org/10.1242/jeb.023101.
Vlaschenko, A. S. 2011. “Research History and List of Records of Bats (Chiroptera) in the Kharkov Region in the XIX and XX Centuries.” Plecotus et al 14: 26–54.
Vlaschenko, A. S., V. Hukov, O. Timofieieva, et al. 2023. “Leaping on Urban Islands: Further Summer and Winter Range Expansion of European Bat Species.” European Journal of Ecology 9, no. 1: 70–85. https://doi.org/10.17161/eurojecol.v9i1.18664.
Vlaschenko, A. S., V. Kovalov, V. Hukov, K. A. Kravchenko, and O. Rodenko. 2019. “An Example of Ecological Traps for Bats in the Urban Environment.” European Journal of Wildlife Research 65, no. 2: 20. https://doi.org/10.1007/s10344-019-1252-z.
Vlaschenko, A. S., A. Prylutska, Bat Rehabilitation Center of Feldman Ecopark, et al. 2020. “Regional Recaptures of Bats (Chiroptera, Vespertilionidae) Ringed in Eastern Ukraine.” Zoodiversity 54, no. 1: 53–66. https://doi.org/10.15407/zoo2020.01.053.
Withers, P. C. 1992. Comparative Animal Physiology. Saunders College Pub.
Zahn, A., and E. Kriner. 2016. “Winter Foraging Activity of Central European Vespertilionid Bats.” Mammalian Biology 81, no. 1: 40–45. https://doi.org/10.1016/j.mambio.2014.10.005.
