in

Raised seasonal temperatures reinforce autumn Varroa destructor infestation in honey bee colonies

  • 1.

    IPCC. 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 (IPCC, 2014).

  • 2.

    Walther, G. R. et al. Ecological responses to recent climate change. Nature 416, 389–395 (2002).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 3.

    Parmesan, C. & Yohe, G. A globally coherent fingerprint of climate change impacts across natural systems. Nature 421, 37–42 (2003).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 4.

    Peñuelas, J. & Filella, I. Responses to a warming world. Science (80-). 294, 793–795 (2001).

    Google Scholar 

  • 5.

    Ockendon, N. et al. Mechanisms underpinning climatic impacts on natural populations: Altered species interactions are more important than direct effects. Glob. Change Biol. 20, 2221–2229 (2014).

    ADS 

    Google Scholar 

  • 6.

    Walther, G.-R. Community and ecosystem responses to recent climate change. Philos. Trans. R. Soc. B Biol. Sci. 365, 2019–2024 (2010).

    Google Scholar 

  • 7.

    Root, T. L. et al. Fingerprints of global warming on wild animals and plants. Nature 421, 57–60 (2003).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 8.

    Klein, A. M. et al. Importance of pollinators in changing landscapes for world crops. Proc. R. Soc. B Biol. Sci. 274, 303–313 (2007).

    Google Scholar 

  • 9.

    Vanbergen, A. J. et al. Threats to an ecosystem service: Pressures on pollinators. Front. Ecol. Environ. 11, 251–259 (2013).

    Google Scholar 

  • 10.

    Hung, K. L. J., Kingston, J. M., Albrecht, M., Holway, D. A. & Kohn, J. R. The worldwide importance of honey bees as pollinators in natural habitats. Proc. R. Soc. B Biol. Sci. 285, 20172140 (2018).

    Google Scholar 

  • 11.

    Watanabe, M. E. Pollination worries rise as honey bees decline. Science (80-). 265, 1170 (1994).

    CAS 
    ADS 

    Google Scholar 

  • 12.

    Chauzat, M.-P. et al. Demographics of the European apicultural industry. PLoS ONE 8, e79018 (2013).

    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 

  • 13.

    Conte, Y. L. & Navajas, M. Climate change: Impact on honey bee populations and diseases. OIE Rev. Sci. Tech. 27, 485–510 (2008).

    Google Scholar 

  • 14.

    Le Conte, Y., Ellis, M. & Ritter, W. Varroa mites and honey bee health: Can Varroa explain part of the colony losses?. Apidologie 41, 353–363 (2010).

    Google Scholar 

  • 15.

    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).

    PubMed 
    ADS 

    Google Scholar 

  • 16.

    Traynor, K. S. et al. Multiyear survey targeting disease incidence in US honey bees. Apidologie https://doi.org/10.1007/s13592-016-0431-0 (2016).

    Article 

    Google Scholar 

  • 17.

    Ramsey, S. D. et al. Varroa destructor feeds primarily on honey bee fat body tissue and not hemolymph. Proc. Natl. Acad. Sci. U. S. A. 116, 1792–1801 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 18.

    Rosenkranz, P., Aumeier, P. & Ziegelmann, B. Biology and control of Varroa destructor. J. Invertebr. Pathol. 103, S96–S119 (2010).

    PubMed 

    Google Scholar 

  • 19.

    Switanek, M., Crailsheim, K., Truhetz, H. & Brodschneider, R. Modelling seasonal effects of temperature and precipitation on honey bee winter mortality in a temperate climate. Sci. Total Environ. 579, 1581–1587 (2017).

    CAS 
    PubMed 
    ADS 

    Google Scholar 

  • 20.

    Genersch, E. et al. The German bee monitoring project: A long term study to understand periodically high winter losses of honey bee colonies. Apidologie 41, 332–352 (2010).

    CAS 

    Google Scholar 

  • 21.

    van Dooremalen, C. et al. Winter survival of individual honey bees and honey bee colonies depends on level of Varroa destructor infestation. PLoS One 7, e36285 (2012).

    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 

  • 22.

    Morawetz, L. et al. Health status of honey bee colonies (Apis mellifera) and disease-related risk factors for colony losses in Austria. PLoS One 14, e0219293 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 23.

    Fries, I., Imdorf, A. & Rosenkranz, P. Survival of mite infested (Varroa destructor) honey bee (Apis mellifera) colonies in a Nordic climate. Apidologie 37, 564–570 (2006).

    Google Scholar 

  • 24.

    Guzmán-Novoa, E. et al. Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie 41, 443–450 (2010).

    Google Scholar 

  • 25.

    Giacobino, A. et al. Environment or beekeeping management: What explains better the prevalence of honey bee colonies with high levels of Varroa destructor?. Res. Vet. Sci. 112, 1–6 (2017).

    PubMed 

    Google Scholar 

  • 26.

    van de Pol, M. et al. Identifying the best climatic predictors in ecology and evolution. Methods Ecol. Evol. 7, 1246–1257 (2016).

    Google Scholar 

  • 27.

    Leza, M. M., Miranda-Chueca, M. A. & Purse, B. V. Patterns in Varroa destructor depend on bee host abundance, availability of natural resources, and climate in Mediterranean apiaries. Ecol. Entomol. 41, 542–553 (2016).

    Google Scholar 

  • 28.

    Dietemann, V. et al. Standard methods for Varroa research. J. Apic. Res. 52, 1–54 (2013).

    Google Scholar 

  • 29.

    Branco, M. R., Kidd, N. A. C. & Pickard, R. S. A comparative evaluation of sampling methods for Varroa destructor (Acari: Varroidae) population estimation. Apidologie 37, 452–461 (2006).

    Google Scholar 

  • 30.

    Haylock, M. R. et al. A European daily high-resolution gridded data set of surface temperature and precipitation for 1950–2006. J. Geophys. Res. Atmos. 113, D20119 (2008).

    ADS 

    Google Scholar 

  • 31.

    Bailey, L. D. & van de Pol, M. climwin: An R toolbox for climate window analysis. PLoS One 11, 1–27 (2016).

    Google Scholar 

  • 32.

    Hartig, F. Residual Diagnostics for Hierachical (Multi-Level/Mixed) Regression Models. (2021).

  • 33.

    Bates, D., Mächler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 51 (2014).

    Google Scholar 

  • 34.

    Kuznetsova, A., Brockhoff, P. B. & Christensen, R. H. B. lmerTest Package: Tests in linear mixed effects models. J. Stat. Softw. 82, 1–26 (2017).

    Google Scholar 

  • 35.

    R Core Team. R: A Language and Environment for Statistical Computing. (2021).

  • 36.

    Seeley, T. D. & Morse, R. A. The nest of the honey bee (Apis mellifera L.). Insectes Soc. 23, 495–512 (1976).

    Google Scholar 

  • 37.

    Calis, J. N. M., Fries, I. & Ryrie, S. C. Population modelling of Varroa jacobsoni Oud. Apidologie 30, 111–124 (1999).

    Google Scholar 

  • 38.

    Fries, I., Hansen, H., Imdorf, A. & Rosenkranz, P. Swarming in honey bees (Apis mellifera) and Varroa destructor population development in Sweden. Apidologie 34, 389–397 (2003).

    Google Scholar 

  • 39.

    Wilde, J., Fuchs, S., Bratkowski, J. & Siuda, M. Distribution of Varroa destructor between swarms and colonies. J. Apic. Res. 44, 190–194 (2005).

    Google Scholar 

  • 40.

    Loftus, J. C., Smith, M. L. & Seeley, T. D. How honey bee colonies survive in the wild: Testing the importance of small nests and frequent swarming. PLoS One 11, 1–11 (2016).

    Google Scholar 

  • 41.

    Moretto, G., Goncalves, L. S., De Jong, D. & Bichuette, M. Z. The effects of climate and bee race on Varroa jacobsoni Oud infestations in Brazil. Apidologie 22, 197–203 (1991).

    Google Scholar 

  • 42.

    Guzmán-Novoa, E., Vandame, R. & Arechavaleta, M. E. Susceptibility of European and Africanized honey bees (Apis mellifera L.) to Varroa jacobsoni Oud. in Mexico. Apidologie 30, 173–182 (1999).

    Google Scholar 

  • 43.

    Ruttner, F. Biogeography and Taxonomy of Honeybees (Springer, 1988). https://doi.org/10.1007/978-3-642-72649-1.

    Book 

    Google Scholar 

  • 44.

    Adam, B. Breeding the Honeybee: A Contribution to the Science of Bee Breeding (Northern Bee Books, 2013).

    Google Scholar 

  • 45.

    Tarpy, D. R., Hatch, S. & Fletcher, D. J. C. The influence of queen age and quality during queen replacement in honeybee colonies. Anim. Behav. 59, 97–101 (2000).

    CAS 
    PubMed 

    Google Scholar 

  • 46.

    Simeunovic, P. et al. Nosema ceranae and queen age influence the reproduction and productivity of the honey bee colony. J. Apic. Res. 53, 545–554 (2014).

    Google Scholar 

  • 47.

    Akyol, E., Yeninar, H., Karatepe, M., Karatepe, B. & Özkök, D. Effects of queen ages on Varroa (Varroa destructor) infestation level in honey bee (Apis mellifera caucasica) colonies and colony performance. Ital. J. Anim. Sci. 6, 143–149 (2007).

    Google Scholar 

  • 48.

    Harris, J. W., Harbo, J. R., Villa, J. D. & Danka, R. G. Variable population growth of Varroa destructor (Mesostigmata: Varroidae) in colonies of honey bees (Hymenoptera: Apidae) during a 10-year period. Environ. Entomol. 32, 1305–1312 (2003).

    Google Scholar 

  • 49.

    Kruuk, L. E. B., Osmond, H. L. & Cockburn, A. Contrasting effects of climate on juvenile body size in a Southern Hemisphere passerine bird. Glob. Change Biol. 21, 2929–2941 (2015).

    ADS 

    Google Scholar 

  • 50.

    Dainat, B., Evans, J. D., Chen, Y. P., Gauthier, L. & Neumann, P. Predictive markers of honey bee colony collapse. PLoS One 7, e32151 (2012).

    CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar 

  • 51.

    Peck, D. T., Smith, M. L. & Seeley, T. D. Varroa destructor mites can nimbly climb from flowers onto foraging honey bees. PLoS One 11, e0167798 (2016).

    PubMed 
    PubMed Central 

    Google Scholar 

  • 52.

    Peck, D. T. & Seeley, T. D. Mite bombs or robber lures? The roles of drifting and robbing in Varroa destructor transmission from collapsing honey bee colonies to their neighbors. PLoS One 14, e0218392 (2019).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 53.

    Seeley, T. D. & Smith, M. L. Crowding honeybee colonies in apiaries can increase their vulnerability to the deadly ectoparasite Varroa destructor. Apidologie 46, 716–727 (2015).

    Google Scholar 

  • 54.

    Vetharaniam, I. Predicting reproduction rate of Varroa. Ecol. Model. 224, 11–17 (2012).

    Google Scholar 

  • 55.

    Nürnberger, F., Härtel, S. & Steffan-Dewenter, I. 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 (2018).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • 56.

    Seeley, T. D. & Visscher, P. K. Survival of honeybees in cold climates: The critical timing of colony growth and reproduction. Ecol. Entomol. 10, 81–88 (1985).

    Google Scholar 

  • 57.

    Martin, S. J. Ontogenesis of the mite Varroa jacobsoni Oud. in worker brood of the honeybee Apis mellifera L. under natural conditions. Exp. Appl. Acarol. https://doi.org/10.1007/BF00055033 (1994).

    Article 

    Google Scholar 

  • 58.

    Martin, S. J. Reproduction of Varroa jacobsoni in cells of Apis mellifera containing one or more mother mites and the distribution of these cells. J. Apic. Res. 34, 187–196 (1995).

    Google Scholar 

  • 59.

    Sparks, T. H. et al. Advances in the timing of spring cleaning by the honeybee Apis mellifera in Poland. Ecol. Entomol. 35, 788–791 (2010).

    Google Scholar 

  • 60.

    Langowska, A. et al. Long-term effect of temperature on honey yield and honeybee phenology. Int. J. Biometeorol. 61, 1125–1132 (2017).

    PubMed 
    ADS 

    Google Scholar 

  • 61.

    Bordier, C. et al. Colony adaptive response to simulated heat waves and consequences at the individual level in honeybees (Apis mellifera). Sci. Rep. 7, 1–11 (2017).

    CAS 

    Google Scholar 

  • 62.

    Fahrenholz, L., Lamprecht, I. & Schricker, B. Thermal investigations of a honey bee colony: Thermoregulation of the hive during summer and winter and heat production of members of different bee castes. J. Comp. Physiol. B 159, 551–560 (1989).

    Google Scholar 

  • 63.

    Villa, J. D., Gentry, C. & Taylor, O. R. Jr. Preliminary observations on thermoregulation, clustering, and energy utilization in African and European Honey Bees. J. Kansas Entomol. Soc. 60, 4–14 (1987).

    Google Scholar 

  • 64.

    Anderson, D. L. & Trueman, J. W. H. Varroa jacobsoni (Acari: Varroidae) is more than one species. Exp. Appl. Acarol. 24, 165–189 (2000).

    CAS 
    PubMed 

    Google Scholar 

  • 65.

    Kottek, M., Grieser, J., Beck, C., Rudolf, B. & Rubel, F. World Map of the Köppen–Geiger climate classification updated. Meteorol. Zeitschrift 15, 259–263 (2006).

    ADS 

    Google Scholar 

  • 66.

    Schmickl, T. & Crailsheim, K. Cannibalism and early capping: Strategy of honeybee colonies in times of experimental pollen shortages. J. Comp. Physiol. A Sens. Neural Behav. Physiol. 187, 541–547 (2001).

    CAS 

    Google Scholar 

  • 67.

    Requier, F., Odoux, J. F., Henry, M. & Bretagnolle, V. The carry-over effects of pollen shortage decrease the survival of honeybee colonies in farmlands. J. Appl. Ecol. 54, 1161–1170 (2017).

    Google Scholar 

  • 68.

    Seeley, T. D. Honeybee Ecology. A Study of Adaptation in Social Life (Princeton University Press, 1985).

    Google Scholar 

  • 69.

    Martin, S. J. Ontogenesis of the mite Varroa jacobsoni Oud. in drone brood of the honeybee Apis mellifera L. under natural conditions. Exp. Appl. Acarol. 19, 199–210 (1995).

    ADS 

    Google Scholar 

  • 70.

    Amiri, E., Strand, M. K., Rueppell, O. & Tarpy, D. R. Queen quality and the impact of honey bee diseases on queen health: Potential for interactions between two major threats to colony health. Insects 8, 48 (2017).

    PubMed Central 

    Google Scholar 

  • 71.

    Giacobino, A. et al. Risk factors associated with failures of Varroa treatments in honey bee colonies without broodless period. Apidologie 46, 573–582 (2015).

    Google Scholar 

  • 72.

    Locke, B. Natural Varroa mite-surviving Apis mellifera honeybee populations. Apidologie 47, 467–482 (2016).

    Google Scholar 

  • 73.

    FAO. Good beekeeping practices: Practical manual on how to identify and control the main diseases of the honeybee (Apis mellifera). TECA—Technologies and practices for small agricultural producers. (2020).

  • 74.

    Harbo, J. R. Effect of population size on brood production, worker survival and honey gain in colonies of honeybees. J. Apic. Res. 25, 22–29 (1986).

    Google Scholar 

  • 75.

    Döke, M. A., McGrady, C. M., Otieno, M., Grozinger, C. M. & Frazier, M. Colony size, rather than geographic origin of stocks, predicts overwintering success in honey bees (Hymenoptera: Apidae) in the Northeastern United States. J. Econ. Entomol. 112, 525–533 (2019).

    PubMed 

    Google Scholar 

  • 76.

    Martin, S. J. The role of Varroa and viral pathogens in the collapse of honeybee colonies: A modelling approach. J. Appl. Ecol. 38, 1082–1093 (2001).

    Google Scholar 


  • Source: Ecology - nature.com

    Unexpected myriad of co-occurring viral strains and species in one of the most abundant and microdiverse viruses on Earth

    Effect of biostimulants on the growth, yield and nutritional value of Capsicum annuum grown in an unheated plastic tunnel