Abstract
Climate change is directly and indirectly affecting species. The degree of these effect types differs by species and context, with indirect effects likely to be stronger for consumers of pulsed resources. Here, we investigated how higher mean air temperature related to climate change affects masting, and in parallel, how this change affects life-history traits in edible dormice (Glis glis). We analysed 17 years of capture-recapture data from 2,530 individuals. We collected air temperature, and, as a measure of seed production, pollen data from European beech (Fagus sylvatica). Our results show that increasing mean air temperature was associated with a shift in beech pollen production, leading to a biannual mast cycle in recent years, with alteration of years with very high and very low seed availability. The changed cycle in mast events resulted in a significant reduction in overall yearling survival in dormice, while overall adult survival remained stable. In parallel, both age classes significantly increased their litter size in this timeframe. Furthermore, survival probabilities in the two age classes also differed depending on the beech mast status (mast, mast-failure). We show that the observed dramatic changes in seed production had complex effects on life-history traits in a pulsed resource consumer.
Data availability
The datasets analysed during the current study are available at Dryad Digital Repository (after acceptance of the manuscript).
References
Ockendon, N. et al. Mechanisms underpinning Climatic impacts on natural populations: altered species interactions are more important than direct effects. Glob Chang. Biol. 20 (7), 2221–2229. https://doi.org/10.1111/gcb.12559 (2014).
Paniw, M. et al. The myriad of complex demographic responses of terrestrial mammals to climate change and gaps of knowledge: A global analysis. J. Anim. Ecol. 90 (6), 1398–1407. https://doi.org/10.1111/1365-2656.13467 (2021).
Pearson, R. G. et al. Life history and Spatial traits predict extinction risk due to climate change. Nat. Clim. Chang. 4 (3), 217–221. https://doi.org/10.1038/nclimate2113 (2014).
Wiehn, J. J. & Zelinka, J. How many species will Earth lose to climate change? Glob Chang. Biol. 30 (1), e17125. https://doi.org/10.1111/gcb.17125 (2024).
Bradley, B. A. et al. Observed and potential range shifts of native and nonnative species with climate change. Annu. Rev. Ecol. Evol. Syst. 55, 23–40. https://doi.org/10.1146/annurev-ecolsys-102722-013135 (2024).
McClelland, G. T. W. et al. Climate change leads to increasing population density and impacts of a key Island invader. Ecol. Appl. 28 (1), 212–224. https://doi.org/10.1002/eap.1642 (2017).
Millon, A. et al. Dampening prey cycle overrides the impact of climate change on predator population dynamics: a long-term demographic study on tawny owls. Glob. Chang. Biol. 20(6), 1770–1781. https://doi.org/10.1111/gcb.12546 (2014).
Quéroué, M. et al. Multispecies integrated population model reveals bottom-up dynamics in a seabird predator-prey system. Ecol. Monogr. 91 (3), e01459. https://doi.org/10.1002/ecm.1459 (2021).
Peers, M. J. L. et al. Climate change increases predation risk for a keystone species of the boreal forest. Nat. Clim. Chang. 10 (12), 1149–1153. https://doi.org/10.1038/s41558-020-00908-4 (2020).
Kausrud, K. L. et al. Linking climate change to lemming cycles. Nature 456 (7218), 93–97. https://doi.org/10.1038/nature07442 (2008).
Mangeon, S., Spessa, A., Deveson, E., Darnell, R. & Kriticos, D. J. Daily mapping of Australian plague locust abundance. Sci. Rep. 10 (1), e16915. https://doi.org/10.1038/s41598-020-73897-1 (2020).
Bogdziewicz, M. How will global change affect plant reproduction? A framework for mast seeding trends. New. Phytol. 234 (1), 14–20. https://doi.org/10.1111/nph.17682 (2022).
Koerner, S. E. et al. Invasibility of a mesic grassland depends on the time-scale of fluctuating resources. J. Ecol. 103 (6), 1538–1546. https://doi.org/10.1111/1365-2745.12479 (2015).
Matthews, J. D. The influence of weather on the frequency of Beech mast years in England. Forestry 28 (2), 107–116. https://doi.org/10.1093/forestry/28.2.107 (1995).
Schauber, E. M. et al. Masting by eighteen new Zealand plant species: the role of temperature as a synchronizing cue. Ecology 83 (5), 1214–1225. https://doi.org/10.1890/0012-9658(2002)083 (2002). [1214:MBENZP]2.0.CO;2.
Clotfelter, E. D. et al. Acorn mast drives long-term dynamics of rodent and Songbird populations. Oecologia 154, 493–503. https://doi.org/10.1007/s00442-007-0859-z (2007).
McShea, W. J. The influence of acorn crops on annual variation in rodent and bird populations. Ecology 81 (1), 228–238. https://doi.org/10.1890/0012-9658(2000)081[ (2000). 0228:TIOACO]2.0.CO;2.
Yang, L. H., Bastow, J. L., Spence, K. O. & Wright, A. N. What can we learn from resource pulses? Ecology 89 (3), 621–634. https://doi.org/10.1890/07-0175.1 (2008).
Vetter, S. G., Ruf, T., Bieber, C. & Arnold, W. What is a mild winter? Regional differences in Within-Species responses to climate change. PLoS ONE. 10 (7), e0132178. https://doi.org/10.1371/journal.pone.0132178 (2015).
Zwolak, R., Celebias, P. & Bogdziewicz, M. Global patterns in the predator satiation effect of masting: A meta-analysis. PNAS 119 (11), e2105655119. https://doi.org/10.1073/pnas.2105655119 (2022).
Bogdziewicz, M. et al. Mechanisms, and consequences of mast seeding. Annu. Rev. Ecol. Evol. Syst. 56, 119–144. https://doi.org/10.1146/annurev-ecolsys-102723-052948 (2025).
Boutin, S. et al. Anticipatory reproduction and population growth in seed predators. Science 314 (5807), 1928–1930. https://doi.org/10.1126/science.1135520 (2006).
Tissier, M. L., Réale, D., Garant, D. & Bergeron, P. Consumption of red maple in anticipation of Beech mast-seeding drives reproduction in Eastern chipmunks. J. Anim. Ecol. 89 (5), 1190–1201. https://doi.org/10.1111/1365-2656.13183 (2020).
Bieber, C. Population dynamics, sexual activity, and reproduction failure in the fat dormouse (Myoxus glis). J. Zool. 244 (2), 223–229. https://doi.org/10.1111/j.1469-7998.1998.tb00027.x (1998).
Stearns, S. G. The Evolution of Life Histories (Oxford University Press, 1998).
Williams, G. C. Natural selection, the costs of reproduction, and a refinement of lack’s principle. Am. Nat. 100 (916), 687–690. https://doi.org/10.1086/282461 (1966).
Rubach, K. et al. Testing the reproductive and somatic trade-off in female Columbian ground squirrels. Ecol. Evol. 6 (21), 7586–7595. https://doi.org/10.1002/ece3.2215 (2016).
Speakman, J. R. The physiological costs of reproduction in small mammals. Philos. Trans. R Soc. Lond. B Biol. Sci. 363 (1490), 375–398. https://doi.org/10.1098/rstb.2007.2145 (2008).
Turbill, C., Bieber, C. & Ruf, T. Hibernation is associated with increased survival and the evolution of slow life histories among mammals. Proc. R Soc. Lond. B Biol. Sci. 278 (1723), 3355–3363. https://doi.org/10.1098/rspb.2011.0190 (2011).
Shattuck, M. R. & Williams, S. A. Arboreality has allowed for the evolution of increased longevity in mammals. PNAS 107 (10), 4635–4639. https://doi.org/10.1073/pnas.0911439107 (2010).
Allison, A. Z. T., Conway, C. J. & Morris, A. E. Why hibernate? Tests of four hypotheses to explain intraspecific variation in hibernation phenology. Funct. Ecol. 37, 1580–1593. https://doi.org/10.1111/1365-2435.14322 (2023).
Lebl, K. et al. Survival rates in a small hibernator, the edible dormouse: a comparison across Europe. Ecography 34 (4), 683–692. https://doi.org/10.1111/j.1600-0587.2010.06691.x (2011).
Hoelzl, F. et al. How to spend the summer? Free-living dormice (Glis glis) can hibernate for 11 months in non-reproductive years. J. Comp. Physiol. B. 185 (8), 931–939. https://doi.org/10.1007/s00360-015-0929-1 (2015).
Ruf, T., Bieber, C. & Physiological Behavioral, and Life-History adaptions to environmental fluctuations in the edible dormouse. Front. Physiol. 11, e423. https://doi.org/10.3389/fphys.2020.00423 (2020).
Vekhnik, V. A., Ruf, T. & Bieber, C. A. Review on the edible dormouse reproduction (Glis Glis Linnaeus, 1766). J. Wildl. Biodivers. 6, 24–45. https://doi.org/10.5281/zenodo.7338112 (2022).
Piovesan, G. & Adams, J. M. Masting behaviour in beech: linking reproduction and Climatic variation. Can. J. Bot. 79 (9), 1039–1047. https://doi.org/10.1139/b01-089 (2001).
Oro, D., Freixas, L., Bartrina, C., Míguez, S. & Torre, I. Direct and indirect effects of climate and seed dynamics on the breeding performance of a seed predator at the distribution edge. Ecol. Evol. 14 (8), e70104. https://doi.org/10.1002/ece3.70104 (2024).
Trout, R. C., Brooks, S. & Morris, P. Nest box usage by old edible dormice (Glis glis) in breeding and non-breeding years. Folia Zool. 64 (4), 320–324. https://doi.org/10.25225/fozo.v64.i4.a5.2015 (2015).
Schau, M. & Vaterlaus-Schlegel, C. Annual and seasonal variation of survival rates in the garden dormouse (Eliomys quercinus). J. Zool. 255 (1), 89–96. https://doi.org/10.1017/S0952836901001133 (2001).
Ruf, T., Fietz, J., Schlund, W. & Bieber, C. High survival in poor years: life history tactics adapted to mast seeding in the edible dormouse. Ecology 87 (2), 372–381. https://doi.org/10.1890/05-0672 (2006).
Havenstein, N., Langer, F., Weiler, U., Stefanski, V. & Fietz, J. Bridging environment, physiology and life history: stress hormones in a small hibernator. Mol. Cell. Endocrinol. 533, e111315. https://doi.org/10.1016/j.mce.2021.111315 (2021).
Hacket-Pain, A. & Bogdziewicz, M. Climate change and plant reproduction: trends and drivers of mast seeding change. Philos. Trans. R Soc. Lond. B Biol. Sci. 376 (1839), e20200379. https://doi.org/10.1098/rstb.2020.0379 (2021).
Wells, C. P., Barbier, R., Nelson, S. & Kanaziz, R. Aubry. L. M. Life history consequences of climate change in hibernating mammals: a review. Ecography 6 (6), e6056. https://doi.org/10.1111/ecog.06056 (2022).
Touzot, L. et al. How does increasing mast seeding frequency affect population dynamics of seed consumers? Wild Boar as case study. Ecol. Appl. 30 (6), e02134. https://doi.org/10.1002/eap.2134 (2020).
Rödel, H. G., Valencak, T. G., Handrek, A. & Moclús, R. Paying the energetic costs of reproduction: reliance on postpartum foraging and stored reserves. Behav. Ecol. 27 (3), 748–756. https://doi.org/10.1093/beheco/arv217 (2016).
Allison, A. Z. T. & Conway, C. J. Daily foraging activity of an imperilled ground squirrel: effects of hibernation, thermal environment, body condition, and conspecific density. Behav. Ecol. Sociobiol. 76 (2), e28. https://doi.org/10.1007/s00265-022-03142-4 (2022).
Daly, M., Behrends, P. R., Wilson, M. I. & Jacobs, L. F. Behavioural modulation of predation risk: moonlight avoidance and crepuscular compensation in a nocturnal desert rodent, Dipodomys merriami. Anim. Behav. 44 (1), 1–9. https://doi.org/10.1016/S0003-3472(05)80748-1 (1992).
Turbill, C. & Stojanovski, L. Torpor reduces predation risk by compensating for the energetic cost of antipredator foraging behaviours. Proc. Biol. Sci. B, 285, e20182370. https://doi.org/10.1098/rspb.2018.2370 (2018).
Stawski, C. & Geiser, F. Fat and fed: frequent use of summer torpor in a subtropical Bat. Naturwissenschaften 97, 29–35. https://doi.org/10.1007/s00114-009-0606-x (2010).
Schaefer, A., Piquard, F. & Haberey, P. Food self-selection during spontaneous body weight variations in the dormouse (Glis glis). Comp. Biochem. Physiol. 52, 115–118. https://doi.org/10.1016/0300-9629(76)90077-3 (1976).
Bieber, C. & Ruf, T. Summer dormancy in edible dormice (Glis glis) without energetic constraints. Naturwissenschaften 96, 165–171. https://doi.org/10.1007/s00114-008-0471-z (2009).
Turbill, C. & Prior, S. Thermal climate-linked variation in annual survival rate of hibernating rodents: shorter winter dormancy and lower survival in warmer climates. Funct. Ecol. 30 (8), 1366–1372. https://doi.org/10.1111/1365-2435.12620 (2016).
Klug, B. J. & Brigham, R. M. Changes to metabolism and cell physiology that enable mammalian hibernation. Springer Sci. Rev. 3, 39–56. https://doi.org/10.1007/s40362-015-0030-x (2015).
Broussard, D. R., Dobson, F. S. & Murie, J. O. The effects of capital on an income breeder: evidence from female Columbian ground squirrels. Can. J. Zool. 83 (4), 546–552. https://doi.org/10.1139/z05-044 (2005).
Humphries, M. M., Thomas, D. W. & Kramer, D. L. The role of energy availability in mammalian hibernation: A Cost-Benefit approach. Physiol. Biochem. Zool. 76 (2), 165–179. https://doi.org/10.1086/367950 (2003).
Lindstedt, S. L., Boyce, M. S. & Seasonality Fasting Endurance, and body size in mammals. Am. Nat. 125 (6), 873–878. https://doi.org/10.1086/284385 (1985).
Descamps, S., Boutin, S., Berteaux, D. & Gaillard, J. M. Female red squirrels fit williams’ hypothesis of increasing reproductive effort with increasing age. J. Anim. Ecol. 76, 1192–1201 (2007). https://www.jstor.org/stable/4539230
Shibata, M., Masaki, T., Yagihashi, T., Shimada, T. & Saitoh, T. Decadal changes in masting behaviour of oak trees with rising temperature. J. Ecol. 108 (3), 1088–1100. https://doi.org/10.1111/1365-2745.13337 (2020).
Zhao, Z. J. et al. Late lactation in small mammals is a critically sensitive window vulnerability to elevated ambient temperature. Proc. Natl. Acad. Sci. U S A. 117 (39), 24352–24358. https://doi.org/10.1073/pnas.2008974117 (2020).
Schwartz, T. S., Pearson, P., Dawson, J., Allison, D. B. & Gohlke, J. M. Effects of fluctuating temperature and food availability on reproduction and lifespan. Exp. Gerontol. 86, 62–72. https://doi.org/10.1016/j.exger.2016.06.010 (2016).
Bogdziewicz, M. et al. Reproductive collapse in European Beech results from declining pollination efficiency in large trees. Glob Chang. Biol. 29 (16), 4595–4604. https://doi.org/10.1111/gcb.16730 (2023).
Cornils, J. S., Hoelzl, F., Rotter, B., Bieber, C. & Ruf, T. Edible dormice (Glis glis) avoid areas with high density of their preferred food plant – the European Beech. Front. Zool. 14, e23. https://doi.org/10.1186/s12983-017-0206-0 (2017).
Morris, P. A. & Hoodless, A. Movements and hibernaculum site in the fat dormouse (Glis glis). J. Zool. 228 (4), 685–687. https://doi.org/10.1111/j.1469-7998.1992.tb04468.x (1992).
Hirst, J. M. An automatic volumetric spore trap. Ann. Appl. Biol. 39 (2), 257–265. https://doi.org/10.1111/j.1744-7348.1952.tb00904.x (1952).
Galán, C. et al. Pollen monitoring: minimum requirements and reproducibility of analysis. Aerobiologia 30, 385–395. https://doi.org/10.1007/s10453-014-9335-5 (2014).
Bogdziewicz, M. et al. Masting in wind-pollinated trees: system-specific roles of weather and pollination dynamics in driving seed production. Ecology 98 (10), 2615–2625. https://doi.org/10.1002/ecy.1951 (2017).
R Development Core Team. R: a Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2022).
White, G. C., Burnham, K. P. & Program, M. A. R. K. Survival Estimation from populations of marked animals. Bird. Study. 46, 120–138. https://doi.org/10.1080/00063659909477239 (1999).
Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear Mixed-Effects models using lme4. J. Stat. Softw. 67, 1–48. https://doi.org/10.18637/jss.v067.i01 (2015).
Zuur, A., Ieno, E., Walker, N., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R (Springer Science & Business Media, 2009).
Akaike, H. Information theory and extension of the maximum likelihood principle. In Proceedings of 2nd International Symposium on Information Theory, edited by. B. N. Petrov, and F. Csaki. Akademia Kaido (1973).
Barton, K. MuMIn: Multi-Model Inference. R package version 1.47.5, (2023). https://cran.rproject.org/web/packages/MuMIn.
Sutherland, C. et al. Practical advice on variable selection and reporting using Akaike information criterion. Proc. R. Soc. Lond. B. Biol. Sci. 290 e20231261, (2007). https://doi.org/10.1098/rspb.2023.1261 (2023).
Marwick, B. & Krishnamoorthy, K. Cvequality: tests for the equality of coefficients of variation from multiple groups. R Package Version 0.2.0, (2022). https://cran.r-project.org/web/packages/cvequality.
Laake, J. L. RMark: An R Interface for analysis of capture-recapture data with MARK. R package version 3.0.0, (2022). https://cran.r-project.org/web/packages/RMark.
Lebreton, J. D., Burnham, K. P., Clobert, J. & Anderson, D. R. Modeling survival and testing biological hypotheses using marked animals: A unified approach with case studies. Ecol. Monogr. 62 (1), 67–118. https://doi.org/10.2307/2937171 (1992).
Burnham, K. P. & Anderson, D. R. Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach (Springer, 2002).
Hothorn, T., Bretz, F. & Westfall, P. Simultaneous inference in general parametric models. Biom J. 50 (3), 346–363. https://doi.org/10.1002/bimj.200810425 (2008).
Acknowledgements
We thank Karin Lebl, Birgit Rotter and Jessica Cornils for their assistance with the field work. We are grateful to Österreichische Bundesforste AG for their permission to use the area for our dormouse research, and the city of Vienna as well as the “Gesellschaft zur Förderung des Forschungsinstituts für Wildtierkunde und Ökologie” for providing financial support. The authors want to thank the Geosphere Austria which provided the facilities for running the Hirst-type pollen trap on the rooftop at “Hohe Warte” in Vienna from 2003 until 2022 as well as the AZ Pollen Research GmbH (former SciCon Pharma Science-Consulting GmbH) for providing the sampler (Hirst-type pollen trap at the GeoSphere Austria) and some lab materials for the respective period. Moreover, we want to thank Uwe Berger for establishing the contact (at that time affiliated with Medical University Vienna) and Prof. Siegfried Jäger † for initiating aerobiological pollen measurements in Vienna and his data analyses from the years 1976 until 2011.
Funding
This study was financially supported by the “Gesellschaft zur Förderung des Forschungsinstituts für Wildtierkunde und Ökologie” and the City of Vienna. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Author information
Authors and Affiliations
Contributions
L. H.: *Formal analysis, Investigation, Data curation, Writing – original draft, Writing – review & editing, Visualization* ; S. M.: *Writing - review & editing* ; M. B.: *Resources, Writing - review & editing* ; T. R.: *Conceptualization, Methodology, Funding acquisition, Supervision, Writing – review & editing; * C. B.: *Conceptualization, Methodology, Investigation, Resources, Funding acquisition, Supervision, Writing - review & editing.* All authors gave final approval for publication.
Corresponding author
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Open Access This article is licensed under a Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License, which permits any non-commercial use, sharing, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if you modified the licensed material. You do not have permission under this licence to share adapted material derived from this article or parts of it. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by-nc-nd/4.0/.
About this article
Cite this article
Hochleitner, L., Morris, S., Bastl, M. et al. Indirect effects of higher mean air temperature related to climate change on major life-history traits in a pulsed-resource consumer. Sci Rep (2026). https://doi.org/10.1038/s41598-026-37071-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1038/s41598-026-37071-3
