Abstract
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.
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References
Alexander JM, Diez JM, Hart SP, Levine JM (2016) When climate reshuffles competitors: a call for experimental macroecology. Trends Ecol Evol 31:831–841. https://doi.org/10.1016/j.tree.2016.08.003
Amdam GV, Hartfelder K, Norberg K, Hagen A, Omholt SW (2004) Altered physiology in worker honey bees (Hymenoptera: Apidae) infested with the mite Varroa destructor (Acari: Varroidae): a factor in colony loss during overwintering? J Econ Entomol 97:741–747. https://doi.org/10.1093/jee/97.3.741
Avitabile A (1978) Brood rearing in honeybee colonies from late autumn to early spring. J Apic Res 17:69–73. https://doi.org/10.1080/00218839.1978.11099905
Bartomeus I et al (2011) Climate-associated phenological advances in bee pollinators and bee-pollinated plants. Proc Natl Acad Sci 108:20645–20649. https://doi.org/10.1073/pnas.1115559108
Bates D, Maechler M, Bolker B, Walker S (2014) lme4: Linear mixed-effects models using Eigen and S4. R package version 1.1-7. Retrieved from http://CRAN.R-project.org/package=lme4
Benjamini Y, Yekutieli D (2001) The control of the false discovery rate in multiple testing under dependency. Ann Stat 29:1165–1188
Berry DA (1987) Logarithmic transformations in ANOVA. Biometrics 43:439–456. https://doi.org/10.2307/2531826
Both C, Van Asch M, Bijlsma RG, Van Den Burg AB, Visser ME (2009) Climate change and unequal phenological changes across four trophic levels: constraints or adaptations? J Anim Ecol 78:73–83. https://doi.org/10.1111/j.1365-2656.2008.01458.x
Calatayud F, Verdu M (1993) Hive debris counts in honeybee colonies: a method to estimate the size of small populations and rate of growth of the miteVarroa jacobsoni Oud. (Mesostigmata: Varroidae). Exp Appl Acarol 17:889–894. https://doi.org/10.1007/BF02328065
Costa C et al (2012) A Europe-wide experiment for assessing the impact of genotype-environment interactions on the vitality and performance of honey bee colonies: experimental design and trait evaluation . J Apic Sci 56:147. https://doi.org/10.2478/v10289-012-0015-9
Crane E (2005) Some effects of latitude on honey bee colonies. Bee World 86:54–55
Danner N, Molitor AM, Schiele S, Härtel S, Steffan-Dewenter I (2016) Season and landscape composition affect pollen foraging distances and habitat use of honey bees. Ecol Appl 26:1920–1929. https://doi.org/10.1890/15-1840.1
Dawson TP, Jackson ST, House JI, Prentice IC, Mace GM (2011) Beyond predictions: biodiversity conservation in a changing climate. Science 332:53–58. https://doi.org/10.1126/science.1200303
Durant JM, Hjermann DØ, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33:271–283. https://doi.org/10.3354/cr033271
Farrar CL (1931) A measure of some factors affecting the development of the honeybee colony. PhD thesis, Massachusetts State College
Forrest JR, Thomson JD (2011) An examination of synchrony between insect emergence and flowering in Rocky Mountain meadows. Ecol Monogr 81:469–491. https://doi.org/10.1890/10-1885.1
Genersch E (2010) Honey bee pathology: current threats to honey bees and beekeeping. Appl Microbiol Biotechnol 87:87–97
Genersch E et al (2010) The German bee monitoring project: a long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41:332–352. https://doi.org/10.1051/apido/2010014
Gordo O, Sanz JJ (2005) Phenology and climate change: a long-term study in a Mediterranean locality. Oecologia 146:484–495. https://doi.org/10.1007/s00442-005-0240-z
Gordo O, Sanz JJ (2006) Temporal trends in phenology of the honey bee Apis mellifera (L.) and the small white Pieris rapae (L.) in the Iberian Peninsula (1952–2004). Ecol Entomol 31:261–268. https://doi.org/10.1111/j.1365-2311.2006.00787.x
Hegland SJ, Nielsen A, Lázaro A, Bjerknes AL, Totland Ø (2009) How does climate warming affect plant-pollinator interactions? Ecol Lett 12:184–195. https://doi.org/10.1111/j.1461-0248.2008.01269.x
Imdorf A, Buehlmann G, Gerig L, Kilchenmann V, Wille H (1987) A test of the method of estimation of brood areas and number of worker bees in free-flying colonies. Apidologie 18:137–146. https://doi.org/10.1051/apido:19870204
IPCC (2014) Climate change 2014: synthesis report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on climate change. IPCC, Geneva
Keller I, Fluri P, Imdorf A (2005) Pollen nutrition and colony development in honey bees—Part II. Bee World 86:27–34. https://doi.org/10.1080/0005772X.2005.11099650
Kramer U, Theiler P (1901) Der schweizerische Bienenvater. Sauerländer & Co., Aarau
Kronenberg F, Heller HC (1982) Colonial thermoregulation in honey bees (Apis mellifera). J Comp Physiol B 148:65–76
Kudo G, Nishikawa Y, Kasagi T, Kosuge S (2004) Does seed production of spring ephemerals decrease when spring comes early? Ecol Res 19:255–259. https://doi.org/10.1111/j.1440-1703.2003.00630.x
Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:26. https://doi.org/10.18637/jss.v082.i13
Le Conte Y, Navajas M (2008) Climate change: impact on honey bee populations and diseases. Rev Sci Tech Off Int Epizoot 27:499–510
Le Conte Y, Ellis M, Ritter W (2010) Varroa mites and honey bee health: can varroa explain part of the colony losses? Apidologie 41:353–363. https://doi.org/10.1051/apido/2010017
Meixner MD et al (2010) Conserving diversity and vitality for honey bee breeding. J Apic Res 49:85–92. https://doi.org/10.3896/IBRA.1.49.1.12
Meixner MD, Kryger P, Costa C (2015) Effects of genotype, environment, and their interactions on honey bee health in Europe. Curr Opin Insect Sci 10:177–184. https://doi.org/10.1016/j.cois.2015.05.010
Miller-Rushing AJ, Høye TT, Inouye DW, Post E (2010) The effects of phenological mismatches on demography. Philos Trans R Soc Lond B Biol Sci 365:3177–3186. https://doi.org/10.1098/rstb.2010.0148
Moritz RF, Härtel S, Neumann P (2005) Global invasions of the western honeybee (Apis mellifera) and the consequences for biodiversity. Ecoscience 12:289–301
Nürnberger F, Steffan-Dewenter I, Härtel S (2017) Combined effects of waggle dance communication and landscape heterogeneity on nectar and pollen uptake in honey bee colonies. PeerJ 5:e3441. https://doi.org/10.7717/peerj.3441
Nürnberger F, Härtel S, Steffan-Dewenter I (2018) The influence of temperature and photoperiod on the timing of brood onset in hibernating honey bee colonies. PeerJ 6:e4801. https://doi.org/10.7717/peerj.4801
Oldroyd BP (1999) Coevolution while you wait: Varroa jacobsoni, a new parasite of western honeybees. Trends Ecol Evol 14:312–315. https://doi.org/10.1016/S0169-5347(99)01613-4
Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669. https://doi.org/10.1146/annurev.ecolsys.37.091305.110100
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353. https://doi.org/10.1016/j.tree.2010.01.007
Potts SG et al (2016) Safeguarding pollinators and their values to human well-being. Nature 540:220–229. https://doi.org/10.1038/nature20588
R Core Team (2017) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Requier F, Odoux J-F, Henry M, Bretagnolle V (2016) The carry-over effects of pollen shortage decrease the survival of honeybee colonies in farmlands. J Appl Ecol. https://doi.org/10.1111/1365-2664.12836
Rosenkranz P, Aumeier P, Ziegelmann B (2010) Biology and control of Varroa destructor. J Invertebr Pathol 103:96–119. https://doi.org/10.1016/j.jip.2009.07.016
Ruttner F (1988) Biogeography and taxonomy of honeybees. Springer, Berlin
Schenk M, Krauss J, Holzschuh A (2018) Desynchronizations in bee–plant interactions cause severe fitness losses in solitary bees. J Anim Ecol 87:139–149. https://doi.org/10.1111/1365-2656.12694
Scheper J et al (2015) Local and landscape-level floral resources explain effects of wildflower strips on wild bees across four European countries. J Appl Ecol 52:1165–1175. https://doi.org/10.1111/1365-2664.12479
Seeley TD (1995) The wisdom of the hive: the social physiology of honey bee colonies. Harvard University Press, Cambridge
Seeley TD, Visscher PK (1985) Survival of honeybees in cold climates: the critical timing of colony growth and reproduction. Ecol Entomol 10:81–88. https://doi.org/10.1111/j.1365-2311.1985.tb00537.x
Singer MC, Parmesan C (2010) Phenological asynchrony between herbivorous insects and their hosts: signal of climate change or pre-existing adaptive strategy? Philos Trans R Soc B Biol Sci 365:3161–3176. https://doi.org/10.1098/rstb.2010.0144
Smith ML, Ostwald MM, Seeley TD (2016) Honey bee sociometry: tracking honey bee colonies and their nest contents from colony founding until death. Insectes Soc 63:553–563. https://doi.org/10.1007/s00040-016-0499-6
Straka JR, Starzomski BM (2014) Humming along or buzzing off? The elusive consequences of plant-pollinator mismatches. J Pollinat Ecol 13:129–145
Switanek M, Crailsheim K, Truhetz H, Brodschneider R (2017) Modelling seasonal effects of temperature and precipitation on honey bee winter mortality in a temperate climate. Sci Total Environ 579:1581–1587. https://doi.org/10.1016/j.scitotenv.2016.11.178
Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363. https://doi.org/10.1111/j.1461-0248.2008.01250.x
van Dooremalen C, Gerritsen L, Cornelissen B, van der Steen JJ, van Langevelde F, Blacquière T (2012) Winter survival of individual honey bees and honey bee colonies depends on level of Varroa destructor infestation. PLoS One 7:e36285. https://doi.org/10.1371/journal.pone.0036285
van Engelsdorp D et al (2009) Colony collapse disorder: a descriptive study. PLoS One 4:e6481. https://doi.org/10.1371/journal.pone.0006481
Visser ME, Both C (2005) Shifts in phenology due to global climate change: the need for a yardstick. Proc R Soc Lond B Biol Sci 272:2561–2569. https://doi.org/10.1098/rspb.2005.3356
Visser ME, Both C, Lambrechts MM (2004) Global climate change leads to mistimed avian reproduction. Adv Ecol Res 35:89–110. https://doi.org/10.1016/S0065-2504(04)35005-1
Williams CM, Henry HAL, Sinclair BJ (2015) Cold truths: how winter drives responses of terrestrial organisms to climate change. Biol Rev 90:214–235. https://doi.org/10.1111/brv.12105
Acknowledgements
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.
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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.
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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.
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Communicated by Riccardo Bommarco.
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Nürnberger, F., Härtel, S. & Steffan-Dewenter, I. Seasonal timing in honey bee colonies: phenology shifts affect honey stores and varroa infestation levels. Oecologia 189, 1121–1131 (2019). https://doi.org/10.1007/s00442-019-04377-1
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DOI: https://doi.org/10.1007/s00442-019-04377-1