, Volume 189, Issue 4, pp 1121–1131 | Cite as

Seasonal timing in honey bee colonies: phenology shifts affect honey stores and varroa infestation levels

  • Fabian NürnbergerEmail author
  • Stephan Härtel
  • Ingolf Steffan-Dewenter
Global change ecology – original research


Increasingly frequent warm periods during winter, which are associated with climate change, may cause mismatches between the colony phenology of the western honey bee, Apis mellifera L., and their floral resources. Warmer winter periods can also affect colony brood rearing activity and consequently the reproduction of the invasive brood parasite Varroa destructor Anderson and Trueman. Until now little is known about the effects of climate change on biotic interactions in such a multitrophic system comprising flowering plants, a pollinator, and its parasite. We performed a reciprocal translocation experiment with honey bee colonies to simulate climate change-induced phenology shifts. Honey bee brood phenology was highly sensitive to environmental conditions in late winter. Colonies in which phenology was experimentally delayed had smaller worker populations in early spring and reduced amounts of stored honey during the following months. During summer, the varroa load in colonies with non-shifted phenology was three times higher than in colonies with delayed phenology. High varroa loads during summer were negatively correlated with worker population growth. Despite a remarkable resilience of colony development to phenology shifts, our results show that mismatches between the phenology of honey bee colonies and flowering plants can affect the build-up of resource stores. Further, an advanced onset of brood rearing activity after hibernation can reinforce the negative impact of the brood parasite V. destructor. We conclude that trade-offs between synchronisation with earlier flower phenology and prolonged brood phases with build-up of varroa populations might constrain the honey bees’ capability to adapt to climate warming.


Climate change Phenological mismatch Tri-trophic interactions Apis mellifera Varroa destructor 



We would like to thank Stefan Berg from the Bayerische Landesanstalt für Weinbau und Gartenbau, Veitshöchheim, for his expert support and provision of honey bee colonies for the experiment and Susanne Schiele for her excellent technical support and assistance during the fieldwork. We thank the Bayreuth Centre of Ecology and Environmental Research BayCEER for access to the experimental site in the Fichtelgebirge. The Bundesamt für Kartographie und Geodäsie kindly provided access to land use data. We thank Riccardo Bommarco and two anonymous reviewers for helpful comments on an earlier version of the manuscript.

Author contribution statement

FN, SH and ISD conceived and designed the study. FN performed the study and analysed the data. FN, SH and ISD wrote the paper. All authors read and approved the final manuscript.


Funding was provided by the German Research Foundation (DFG) to the Collaborative Research Center 1047—insect timing: mechanisms, plasticity and interactions, Project C2, to ISD and SH.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable institutional and/or national guidelines for the care and use of animals were followed.

Supplementary material

442_2019_4377_MOESM1_ESM.xlsx (34 kb)
Supplementary material 1 (XLSX 33 kb)


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Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Department of Animal Ecology and Tropical Biology, BiocenterUniversity of WürzburgWürzburgGermany

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