Citizen science monitoring reveals links between honeybee health, pesticide exposure and seasonal availability of floral resources
The Insect Pollinators Initiative & Vanbergen, A. J. Threats to an ecosystem service: Pressures on pollinators. Front. Ecol. Environ. 11, 251–259 (2013).Article
Google Scholar
Powney, G. D. et al. Widespread losses of pollinating insects in Britain. Nat. Commun. 10, 1018. https://doi.org/10.1038/s41467-019-08974-9 (2019).ADS
CAS
Article
PubMed
PubMed Central
Google Scholar
Woodcock, B. A. et al. Impacts of neonicotinoid use on long-term population changes in wild bees in England. Nat. Commun. 7, 12459. https://doi.org/10.1038/ncomms12459 (2016).ADS
CAS
Article
PubMed
PubMed Central
Google Scholar
Potts, S. G. et al. Global pollinator declines: Trends, impacts and drivers. TREE 25, 345–353 (2010).PubMed
Google Scholar
Becher, M. A., Osborne, J. L., Thorbek, P., Kennedy, P. J. & Grimm, V. REVIEW: Towards a systems approach for understanding honeybee decline: A stocktaking and synthesis of existing models. J. Appl. Ecol. 50, 868–880 (2013).PubMed
PubMed Central
Article
Google Scholar
Becher, M. A. et al. BEEHAVE: A systems model of honeybee colony dynamics and foraging to explore multifactorial causes of colony failure. J. Appl. Ecol. 51, 470–482 (2014).PubMed
PubMed Central
Article
Google Scholar
Carvell, C. et al. Bumblebee family lineage survival is enhanced in high-quality landscapes. Nature 543, 547–549. https://doi.org/10.1038/nature21709 (2017).ADS
CAS
Article
PubMed
Google Scholar
Alaux, C., Ducloz, F., Crauser, D. & Le Conte, Y. Diet effects on honeybee immunocompetence. Biol. Lett. 6, 562–565 (2010).PubMed
PubMed Central
Article
Google Scholar
Dolezal, A. G. et al. Interacting stressors matter: Diet quality and virus infection in honeybee health. R. Soc. Open Sci. https://doi.org/10.1098/rsos.181803 (2019).Article
PubMed
PubMed Central
Google Scholar
Conti, I. et al. Sugar and protein content in different monofloral pollens – Building a database. Bull. Insectol. 69, 318–320 (2016).
Google Scholar
Rodney, S. & Kramer, V. J. Probabilistic assessment of nectar requirements for nectar-foraging honey bees. Apidologie 51, 180–200 (2020).Article
Google Scholar
Cartar, R. V. Colony energy-reuirements affect response to predation risk in foraging bumble bees. Ethology 87, 90–96 (1991).Article
Google Scholar
Cook, S. M., Awmack, C. S., Murray, D. A. & Williams, I. H. Are honey bees’ foraging preferences affected by pollen amino acid composition?. Ecol. Entomol. 28, 622–627 (2003).Article
Google Scholar
Baude, M. et al. Historical nectar assessment reveals the fall and rise of floral resources in Britain. Nature 530, 85–88. https://doi.org/10.1038/nature16532 (2016).ADS
CAS
Article
PubMed
PubMed Central
Google Scholar
Di Pasquale, G. et al. Influence of pollen nutrition on honey bee health: Do Pollen quality and diversity matter?. PLoS ONE https://doi.org/10.1371/journal.pone.0072016 (2013).Article
PubMed
PubMed Central
Google Scholar
Sanchez-Bayo, F. et al. Are bee diseases linked to pesticides?—A brief review. Environ. Int. 89–90, 7–11. https://doi.org/10.1016/j.envint.2016.01.009 (2016).CAS
Article
PubMed
Google Scholar
Park, M. G., Blitzer, E. J., Gibbs, J., Losey, J. E. & Danforth, B. N. Negative effects of pesticides on wild bee communities can be buffered by landscape context. Proc. R. Soc. Lond. B Biol. Sci. 282, 20150299. https://doi.org/10.1098/rspb.2015.0299 (2015).CAS
Article
Google Scholar
Woodcock, B. A. et al. Country-specific effects of neonicotinoid pesticides on honeybees and wild bees. Science 356, 1393–1395. https://doi.org/10.1126/science.aaa1190 (2017).ADS
CAS
Article
PubMed
Google Scholar
PPDB. The pesticide properties DataBase (PPDB) (Agriculture & Environment Research Unit (AERU), University of Hertfordshire, 2013).Belden, J. B. The acute toxicity of pesticide mixtures to honeybees. Integr. Environ. Assess. Manag. https://doi.org/10.1002/ieam.4595 (2022).Article
PubMed
Google Scholar
Battisti, L. et al. Is glyphosate toxic to bees? A meta-analytical review. Sci. Tot. Environ. 767, 145397. https://doi.org/10.1016/j.scitotenv.2021.145397 (2021).CAS
Article
Google Scholar
Siviter, H. et al. Agrochemicals interact synergistically to increase bee mortality. Nature 596, 389–392. https://doi.org/10.1038/s41586-021-03787-7 (2021).ADS
CAS
Article
PubMed
Google Scholar
Robinson, R. A. & Sutherland, W. J. Post-war changes in arable farming and biodiversity in Great Britain. J. Appl. Ecol. 39, 157–176 (2002).Article
Google Scholar
Carvell, C. et al. Declines in forage availability for bumblebees at a national scale. Biol. Conserv. 132, 481–489 (2006).Article
Google Scholar
Carmona, C. P. et al. Agriculture intensification reduces plant taxonomic and functional diversity across European arable systems. Funct. Ecol. 34, 1448–1460 (2020).Article
Google Scholar
Storkey, J. & Westbury, D. B. Managing arable weeds for biodiversity. Pest Manag. Sci. 63, 517–523 (2007).CAS
PubMed
Article
Google Scholar
Hutchinson, L. A. et al. Using ecological and field survey data to establish a national list of the wild bee pollinators of crops. Agric. Ecosyst. Environ. 315, 107447. https://doi.org/10.1016/j.agee.2021.107447 (2021).Article
Google Scholar
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).Article
Google Scholar
Alburaki, M., Gregorc, A., Adamczyk, J. & Stewart, S. D. Insights on pollen diversity of honey bee (Apis mellifera L.) colonies Located in various agricultural landscapes. Southwest. Nat. 63, 49–58 (2018).Article
Google Scholar
Donkersley, P., Rhodes, G., Pickup, R. W., Jones, K. C. & Wilson, K. Honeybee nutrition is linked to landscape composition. Ecol. Evol. 4, 4195–4206 (2014).PubMed
PubMed Central
Article
Google Scholar
Cole, L. J., Brocklehurst, S., Robertson, D., Harrison, W. & McCracken, D. I. Exploring the interactions between resource availability and the utilisation of semi-natural habitats by insect pollinators in an intensive agricultural landscape. Agric. Ecosyst. Environ. 246, 157–167 (2017).Article
Google Scholar
Steffan-Dewenter, I. & Kuhn, A. Honeybee foraging in differentially structured landscapes. Proc. R. Soc. Lond. B Biol. Sci. 270, 569–575 (2003).Article
Google Scholar
Woodcock, B. A. et al. Enhancing floral resources for pollinators in productive agricultural grasslands. Biol. Conserv. 171, 44–51 (2014).Article
Google Scholar
Requier, F. et al. Honey bee diet in intensive farmland habitats reveals an unexpectedly high flower richness and a major role of weeds. Ecol. App. 25, 881–890 (2015).Article
Google Scholar
Ausseil, A. G. E., Dymond, J. R. & Newstrom, L. Mapping floral resources for honey bees in New Zealand at the catchment scale. Ecol. Appl. 28, 1182–1196. https://doi.org/10.1002/eap.1717 (2018).Article
PubMed
Google Scholar
Kamo, T. et al. A DNA barcoding method for identifying and quantifying the composition of pollen species collected by European honeybees, Apis mellifera (Hymenoptera: Apidae). Appl. Entomol. Zool. 53, 353–361 (2018).CAS
PubMed
PubMed Central
Article
Google Scholar
Nurnberger, F., Keller, A., Hartel, S. & Steffan-Dewenter, I. Honey bee waggle dance communication increases diversity of pollen diets in intensively managed agricultural landscapes. Mol. Ecol. 28, 3602–3611 (2019).PubMed
Article
Google Scholar
Richardson, R. T. et al. Applications of ITS2 metabarcoding to determine the provenance of pollen collected by honey bees in an agroecosystem. Appl. Plant Sci. https://doi.org/10.3732/apps.1400066 (2015).Article
PubMed
PubMed Central
Google Scholar
Oliver, A. E. et al. Integration of DNA extraction, metabarcoding and an informatics pipeline to underpin a national citizen science honey monitoring scheme. MethodsX 8, 101303. https://doi.org/10.1016/j.mex.2021.101303 (2021).Article
PubMed
PubMed Central
Google Scholar
Jones, L. et al. Shifts in honeybee foraging reveal historical changes in floral resources. Commun. Biol. 4, 37. https://doi.org/10.1038/s42003-020-01562-4 (2021).Article
PubMed
PubMed Central
Google Scholar
Barroso-Arevalo, S., Vicente-Rubiano, M., Ruiz, J. A., Bentabol, A. & Sanchez-Vizcaino, J. M. Does pollen diversity influence honey bee colony health?. Sp. J. Agric. Res. https://doi.org/10.5424/sjar/2019173-13991 (2019).Article
Google Scholar
Bansch, S., Tscharntke, T., Ratnieks, F. L. W., Hartel, S. & Westphal, C. Foraging of honey bees in agricultural landscapes with changing patterns of flower resources. Agric. Ecosyst. Environ. https://doi.org/10.1016/j.agee.2019.106792 (2020).Article
Google Scholar
Danner, N., Molitor, A. M., Schiele, S., Hartel, S. & Steffan-Dewenter, I. Season and landscape composition affect pollen foraging distances and habitat use of honey bees. Ecol. Appl. 26, 1920–1929 (2016).PubMed
Article
Google Scholar
EFSA. EFSA Guidance Document on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA J. 11, 3295 (2014).
Google Scholar
Hatjina, F. et al. Citizen scientist initiative for measuring varroa damage thresholds: Common efforts for data collection—CSI varroa. Bee World 98, 132–135 (2021).Article
Google Scholar
Gratzer, K. & Brodschneider, R. How and why beekeepers participate in the INSIGNIA citizen science honey bee environmental monitoring project. Environ. Sci. Pollut. Res. 28, 37995–38006 (2021).Article
Google Scholar
Brodschneider, R. et al. CSI pollen: Diversity of honey bee collected pollen studied by citizen scientists. Insects 12, 987. https://doi.org/10.3390/insects12110987 (2021).Article
PubMed
PubMed Central
Google Scholar
Brodschneider, R. et al. A citizen science supported study on seasonal diversity and monoflorality of pollen collected by honey bees in Austria. Sci. Rep. https://doi.org/10.1038/s41598-019-53016-5 (2019).Article
PubMed
PubMed Central
Google Scholar
Taberlet, P., Coissac, E., Hajibabaei, M. & Rieseberg, L. H. Environmental DNA. Mol. Ecol. 21, 1789–1793 (2012).CAS
PubMed
Article
Google Scholar
Deiner, K. et al. Environmental DNA metabarcoding: Transforming how we survey animal and plant communities. Mol. Ecol. 26, 5872–5895. https://doi.org/10.1111/mec.14350 (2017).Article
PubMed
Google Scholar
Nagaharu, U. Genome analysis in brassica with special reference to the experimental formation of B. Napus and peculiar mode of fertilization. Jpn. J. Bot. 7, 389–452 (1935).
Google Scholar
Herbertsson, L., Lindstrom, S. A. M., Rundlof, M., Bornmarco, R. & Smith, H. G. Competition between managed honeybees and wild bumblebees depends on landscape context. Basic Appl. Ecol. 17, 609–616 (2016).Article
Google Scholar
Magrach, A., Gonzalez-Varo, J. P., Boiffier, M., Vila, M. & Bartomeus, I. Honeybee spillover reshuffles pollinator diets and affects plant reproductive success. Nat. Ecol. Evol. 1, 1299–1307 (2017).PubMed
Article
Google Scholar
Adams-Groom, B., Martin, P. & Banon, A. Pollen characterization of English honey from Worcestershire, West Midlands (UK). Bee World https://doi.org/10.1080/0005772X.2019.1698105 (2019).Article
Google Scholar
Smart, M. D. et al. A comparison of honey bee-collected pollen from working agricultural lands using light microscopy and ITS metabarcoding. Environ. Entomol. 46, 38–49 (2017).CAS
PubMed
Google Scholar
Danner, N., Keller, A., Hartel, S. & Steffan-Dewenter, I. Honey bee foraging ecology: Season but not landscape diversity shapes the amount and diversity of collected pollen. PLoS ONE https://doi.org/10.1371/journal.pone.0183716 (2017).Article
PubMed
PubMed Central
Google Scholar
Piroux, M. et al. Correlating the pollens gathered by Apis mellifera with the landscape features in Western France. Appl. Ecol. Environ. Res. 12, 423–439 (2014).Article
Google Scholar
Di Pasquale, G. et al. Variations in the availability of pollen resources affect honey bee health. PLoS ONE https://doi.org/10.1371/journal.pone.0162818 (2016).Article
PubMed
PubMed Central
Google Scholar
Donkersley, P. et al. Nutritional composition of honey bee food stores vary with floral composition. Oecologia 185, 749–761 (2017).ADS
PubMed
PubMed Central
Article
Google Scholar
Shaw, R. F. et al. Mass-flowering crops have a greater impact than semi-natural habitat on crop pollinators and pollen deposition. Landsc. Ecol. 35, 513–527 (2020).Article
Google Scholar
LoCascio, G. M., Aguirre, L., Irwin, R. E. & Adler, L. S. Pollen from multiple sunflower cultivars and species reduces a common bumblebee gut pathogen. R. Soc. Open Sci. https://doi.org/10.1098/rsos.190279 (2019).Article
PubMed
PubMed Central
Google Scholar
Egan, P. A. et al. Plant toxin levels in nectar vary spatially across native and introduced populations. J. Ecol. 104, 1106–1115 (2016).CAS
Article
Google Scholar
Flombaum, P., Sala, O. E. & Rastetter, E. B. Interactions among resource partitioning, sampling effect, and facilitation on the biodiversity effect: A modeling approach. Oecologia 174, 559–566 (2014).ADS
PubMed
Article
Google Scholar
Cullen, M. G., Thompson, L. J., Carolan, J. C., Stout, J. C. & Stanley, D. A. Fungicides, herbicides and bees: A systematic review of existing research and methods. PLoS ONE https://doi.org/10.1371/journal.pone.0225743 (2019).Article
PubMed
PubMed Central
Google Scholar
Siviter, H. et al. Agrochemicals interact synergistically to increase bee mortality. Nature https://doi.org/10.1038/s41586-021-03787-7 (2021).Article
PubMed
Google Scholar
Haber, A. I., Steinhauer, N. A. & van Engelsdorp, D. Use of chemical and nonchemical methods for the control of Varroa destructor (Acari: Varroidae) and associated winter colony losses in U.S. beekeeping operations. J. Econ. Entomol. 112, 1509–1525 (2019).CAS
PubMed
Article
Google Scholar
Martin, S. J. et al. Global honey bee viral landscape altered by a parasitic mite. Science 336, 1304. https://doi.org/10.1126/science.1220941 (2012).ADS
CAS
Article
PubMed
Google Scholar
Jarvis, S. G. et al. CEH land cover plus: Pesticides 2012-2017 (England, Scotland and Wales). NERC Environmental Information Data Centre. https://doi.org/10.5285/99a2d3a8-1c7d-421e-ac9f-87a2c37bda62 (2020).Simon-Delso, N. et al. Honeybee colony disorder in crop areas: The role of pesticides and viruses. PLoS ONE https://doi.org/10.1371/journal.pone.0103073 (2014).Article
PubMed
PubMed Central
Google Scholar
Greenleaf, S. G., Williams, N. M., Winfree, R. & Kremen, C. Bee foraging ranges and their relationship to body size. Oecologia 153, 589–596 (2007).ADS
PubMed
Article
Google Scholar
FERA. PUS STAT: Pesticide usage surveys. https://secure.fera.defra.gov.uk/pusstats/myindex.cfm (2015).McMurdie, P. J. & Holmes, S. phyloseq: An R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217. https://doi.org/10.1371/journal.pone.0061217 (2013).ADS
CAS
Article
PubMed
PubMed Central
Google Scholar
UKCEH. Land cover plus: Crops © NERC (CEH) 2019. (Remote Sensing Applications Consultants Ltd., 2019).Zuur, A. F., Ieno, E. N. & Elphick, C. S. A protocol for data exploration to avoid common statistical problems. Methods Ecol. Evol. 1, 3–14 (2010).Article
Google Scholar
Kovach, J., Petzoldt, C., Degni, J. & Tette, J. A method to measure the environmental impact of pesticides, Vol. 139 1–8 (New York Food and Life Sciences Bulletin, 1992).Juraske, R., Antón, A. & Castells, F. Estimating half-lives of pesticides in/on vegetation for use in multimedia fate and exposure models. Chemosphere 70, 1748–1755 (2008).ADS
CAS
PubMed
Article
Google Scholar
Thompson, H. M., Fryday, S. L., Harkin, S. & Milner, S. Potential impacts of synergism in honeybees (Apis mellifera) of exposure to neonicotinoids and sprayed fungicides in crops. Apidologie 45, 545–553. https://doi.org/10.1007/s13592-014-0273-6 (2014).CAS
Article
Google Scholar
Biddinger, D. J. et al. Comparative toxicities and synergism of apple orchard pesticides to Apis mellifera (L.) and Osmia cornifrons (Radoszkowski). PLoS ONE https://doi.org/10.1371/journal.pone.0072587 (2013).Article
PubMed
PubMed Central
Google Scholar
Ridley, L. et al. Pesticide usage survey report 295. Arable crops in the United Kingdom 2020 (Food & Environment Research Agency, 2020).Dormann, C. F., Gruber, B. & Fründ, J. Introducing the bipartite package: analysing ecological networks. R News 8, 8–11 (2008).
Google Scholar
R Core Development Team. R: Version 3.6.3. A language and environment for statistical computing. R Foundation for Statistical Computing, Bristol, UK. http://cran.r-project.org (2021).Pinheiro, J. C., Bates, D. & DebRoy, S. The R core team nlme: Linear and nonlinear mixed effects models. R Package nlme Version 3, 1–83 (2007).
Google Scholar More