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No effect of dual exposure to sulfoxaflor and a trypanosome parasite on bumblebee olfactory learning

  • Ollerton, J., Winfree, R. & Tarrant, S. How many flowering plants are pollinated by animals?. Oikos 120(3), 321–326 (2011).

    Article 

    Google Scholar 

  • Aizen, M. A. & Harder, L. D. The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr. Biol. 19(11), 915–918 (2009).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Potts, S. G. et al. Safeguarding pollinators and their values to human well-being. Nature 540(7632), 220–229. https://doi.org/10.1038/nature20588 (2016).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Rader, R. et al. Non-bee insects are important contributors to global crop pollination. Proc. Natl. Acad. Sci. 113(1), 146–151 (2016).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Osterman, J. et al. Global trends in the number and diversity of managed pollinator species. Agr. Ecosyst. Environ. 322, 107653 (2021).

    Article 

    Google Scholar 

  • Velthuis, H. H. W. & Van Doorn, A. A century of advances in bumblebee domestication and the economic and environmental aspects of its commercialization for pollination. Apidologie 37(4), 421–451 (2006).

    Article 

    Google Scholar 

  • 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. Royal Soc. B Biol. Sci. 285(1870), 20172140 (2018).

    Article 

    Google Scholar 

  • Brown, M. J. F. & Paxton, R. J. The conservation of bees: A global perspective. Apidologie 40(3), 410–416 (2009).

    Article 

    Google Scholar 

  • Cameron, S. A. & Sadd, B. M. Global trends in bumble bee health. Annu. Rev. Entomol. 65, 209–232 (2020).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Potts, S. G. et al. Global pollinator declines: Trends, impacts and drivers. Trends Ecol. Evol. 25(6), 345–353 (2010).

    PubMed 
    Article 

    Google Scholar 

  • Vanbergen, A. J. & Initiative, T. I. P. Threats to an ecosystem service: Pressures on pollinators. Front. Ecol. Environ. 11(5), 251–259 (2013).

    Article 

    Google Scholar 

  • David, A. et al. Widespread contamination of wildflower and bee-collected pollen with complex mixtures of neonicotinoids and fungicides commonly applied to crops. Environ. Int. 88, 169–178. https://doi.org/10.1016/j.envint.2015.12.011 (2016).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Gradish, A. E. et al. Comparison of pesticide exposure in honey bees (Hymenoptera: Apidae) and bumble bees (Hymenoptera: Apidae): implications for risk assessments. Environ. Entomol. 48(1), 12–21 (2019).

    PubMed 
    Article 

    Google Scholar 

  • Johnson, R. M., Ellis, M. D., Mullin, C. A. & Frazier, M. Pesticides and honey bee toxicity–USA. Apidologie 41(3), 312–331 (2010).

    CAS 
    Article 

    Google Scholar 

  • Johnson, R. M. et al. Ecologically appropriate xenobiotics induce cytochrome P450s in Apis mellifera. PLoS ONE 7(2), e31051. https://doi.org/10.1371/journal.pone.0031051 (2012).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Mullin, C. A. et al. High levels of miticides and agrochemicals in North American apiaries: Implications for honey bee health. PLoS ONE 5(3), e9754. https://doi.org/10.1371/journal.pone.0009754 (2010).

    ADS 
    CAS 
    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Cameron, S. A. et al. Patterns of widespread decline in North American bumble bees. Proc. Natl. Acad. Sci. 108(2), 662–667 (2011).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Goulson, D., Lye, G. C. & Darvill, B. Decline and conservation of bumble bees. Annu. Rev. Entomol. 53(1), 191–208. https://doi.org/10.1146/annurev.ento.53.103106.093454 (2008).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Meeus, I., Brown, M. J. F., de Graaf, D. C. & Smagghe, G. Effects of invasive parasites on bumble bee declines. Conserv. Biol. 25(4), 662–671. https://doi.org/10.1111/j.1523-1739.2011.01707.x (2011).

    Article 
    PubMed 

    Google Scholar 

  • O’Neal, S. T., Anderson, T. D. & Wu-Smart, J. Y. Interactions between pesticides and pathogen susceptibility in honey bees. Curr. Opin. Insect Sci. 26, 57–62. https://doi.org/10.1016/j.cois.2018.01.006 (2018).

    Article 
    PubMed 

    Google Scholar 

  • Botías, C. et al. Multiple stressors interact to impair the performance of bumblebee Bombus terrestris colonies. J. Anim. Ecol. 90(2), 415–431 (2021).

    PubMed 
    Article 

    Google Scholar 

  • Dance, C., Botías, C. & Goulson, D. The combined effects of a monotonous diet and exposure to thiamethoxam on the performance of bumblebee micro-colonies. Ecotoxicol. Environ. Saf. 139, 194–201 (2017).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Fauser-Misslin, A., Sadd, B. M., Neumann, P. & Sandrock, C. Influence of combined pesticide and parasite exposure on bumblebee colony traits in the laboratory. J. Appl. Ecol. 51(2), 450–459 (2014).

    Article 

    Google Scholar 

  • Zaragoza-Trello, C., Vilà, M., Botías, C. & Bartomeus, I. Interactions among global change pressures act in a non-additive way on bumblebee individuals and colonies. Funct. Ecol. 35(2), 420–434 (2021).

    Article 

    Google Scholar 

  • Collett, M., Chittka, L. & Collett, T. S. Spatial memory in insect navigation. Curr. Biol. 23(17), R789–R800 (2013).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Klein, S., Cabirol, A., Devaud, J. M., Barron, A. B. & Lihoreau, M. Why bees are so vulnerable to environmental stressors. Trends Ecol. Evol. 32(4), 268–278 (2017).

    PubMed 
    Article 

    Google Scholar 

  • Dyer, A. G., Dorin, A., Reinhardt, V., Garcia, J. E. & Rosa, M. G. Bee reverse-learning behavior and intra-colony differences: simulations based on behavioral experiments reveal benefits of diversity. Ecol. Model. 277, 119–131 (2014).

    Article 

    Google Scholar 

  • Raine, N. E. & Chittka, L. No trade-off between learning speed and associative flexibility in bumblebees: A reversal learning test with multiple colonies. PLoS ONE 7(9), e45096 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Henry, M. et al. A common pesticide decreases foraging success and survival in honey bees. Science 336(6079), 348–350 (2012).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Siviter, H., Koricheva, J., Brown, M. J. F. & Leadbeater, E. Quantifying the impact of pesticides on learning and memory in bees. J. Appl. Ecol. 55(6), 2812–2821 (2018).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Bitterman, M. E., Menzel, R., Fietz, A. & Schäfer, S. Classical conditioning of proboscis extension in honeybees (Apis mellifera). J. Comp. Psychol. 97(2), 107–119. https://doi.org/10.1037/0735-7036.97.2.107 (1983).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Takeda, K. Classical conditioned response in the honey bee. J. Insect Physiol. 6(3), 168–179. https://doi.org/10.1016/0022-1910(61)90060-9 (1961).

    CAS 
    Article 

    Google Scholar 

  • Laloi, D. et al. Olfactory conditioning of the proboscis extension in bumble bees. Entomol. Exp. Appl. 90(2), 123–129 (1999).

    Article 

    Google Scholar 

  • Gómez-Moracho, T., Heeb, P. & Lihoreau, M. Effects of parasites and pathogens on bee cognition. Ecol. Entomol. 42, 51–64 (2017).

    Article 

    Google Scholar 

  • Garratt, M. P. D. et al. The identity of crop pollinators helps target conservation for improved ecosystem services. Biol. Cons. 169, 128–135 (2014).

    CAS 
    Article 

    Google Scholar 

  • Morandin, L. A., Laverty, T. M. & Kevan, P. G. Bumble bee (Hymenoptera: Apidae) activity and pollination levels in commercial tomato greenhouses. J. Econ. Entomol. 94(2), 462–467 (2001).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Siviter, H. et al. No evidence for negative impacts of acute sulfoxaflor exposure on bee olfactory conditioning or working memory. PeerJ 7, e7208 (2019).

    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Sparks, T. C. et al. Sulfoxaflor and the sulfoximine insecticides: Chemistry, mode of action and basis for efficacy on resistant insects. Pestic. Biochem. Physiol. 107(1), 1–7. https://doi.org/10.1016/j.pestbp.2013.05.014 (2013).

    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Krupke, C. H., Hunt, G. J., Eitzer, B. D., Andino, G. & Given, K. Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS ONE 7(1), e29268 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Tomizawa, M. & Casida, J. E. Neonicotinoid insecticide toxicology: Mechanisms of selective action. Annu. Rev. Pharmacol. Toxicol. 45, 247–268 (2005).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Gill, R. J., Ramos-Rodriguez, O. & Raine, N. E. Combined pesticide exposure severely affects individual-and colony-level traits in bees. Nature 491(7422), 105–108 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Stanley, D. A., Russell, A. L., Morrison, S. J., Rogers, C. & Raine, N. E. Investigating the impacts of field-realistic exposure to a neonicotinoid pesticide on bumblebee foraging, homing ability and colony growth. J. Appl. Ecol. 53(5), 1440–1449 (2016).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Williamson, S. M. & Wright, G. A. Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. J. Exp. Biol. 216(10), 1799–1807 (2013).

    CAS 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Yang, E. C., Chuang, Y. C., Chen, Y. L. & Chang, L. H. Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J. Econ. Entomol. 101(6), 1743–1748 (2008).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Yang, E., Chang, H., Wu, W. & Chen, Y. Impaired olfactory associative behavior of honeybee workers due to contamination of imidacloprid in the larval stage. PLoS ONE 7(11), e49472 (2012).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Watson, G. B., Siebert, M. W., Wang, N. X., Loso, M. R. & Sparks, T. C. Sulfoxaflor–A sulfoximine insecticide: Review and analysis of mode of action, resistance and cross-resistance. Pestic. Biochem. Physiol. 178, 104924 (2021).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Cordes, N. et al. Interspecific geographic distribution and variation of the pathogens Nosema bombi and Crithidia species in United States bumble bee populations. J. Invertebr. Pathol. 109(2), 209–216 (2012).

    PubMed 
    Article 

    Google Scholar 

  • Gillespie, S. Factors affecting parasite prevalence among wild bumblebees. Ecol. Entomol. 35(6), 737–747 (2010).

    Article 

    Google Scholar 

  • Plischuk, S., Antúnez, K., Haramboure, M., Minardi, G. M. & Lange, C. E. Long-term prevalence of the protists Crithidia bombi and Apicystis bombi and detection of the microsporidium Nosema bombi in invasive bumble bees. Environ. Microbiol. Rep. 9(2), 169–173 (2017).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Shykoff, J. A. & Schmid-Hempel, P. Incidence and effects of four parasites in natural populations of bumble bees in Switzerland. Apidologie 22(2), 117–125 (1991).

    Article 

    Google Scholar 

  • Gegear, R. J., Otterstatter, M. C. & Thomson, J. D. Bumble-bee foragers infected by a gut parasite have an impaired ability to utilize floral information. Proc. Royal Soc. B Biol. Sci. 273(1590), 1073–1078 (2006).

    Article 

    Google Scholar 

  • Otterstatter, M. C., Gegear, R. J., Colla, S. R. & Thomson, J. D. Effects of parasitic mites and protozoa on the flower constancy and foraging rate of bumble bees. Behav. Ecol. Sociobiol. 58(4), 383–389 (2005).

    Article 

    Google Scholar 

  • Martin, C. D., Fountain, M. T. & Brown, M. J. F. Bumblebee olfactory learning affected by task allocation but not by a trypanosome parasite. Sci. Rep. 8(1), 1–8 (2018).

    Google Scholar 

  • Azpiazu, C. et al. Toxicity of the insecticide sulfoxaflor alone and in combination with the fungicide fluxapyroxad in three bee species. Sci. Rep. 11(1), 1–9 (2021).

    Article 
    CAS 

    Google Scholar 

  • European Food Safety Authority (EFSA) et al. Peer review of the pesticide risk assessment for the active substance sulfoxaflor in light of confirmatory data submitted. EFSA J. 17(3), e05633 (2019).

    Google Scholar 

  • Linguadoca, A., Rizzi, C., Villa, S. & Brown, M. J. F. Sulfoxaflor and nutritional deficiency synergistically reduce survival and fecundity in bumblebees. Sci. Total Environ. 795, 148680 (2021).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Sandor, A., Sarospataki, M. & Farkas, S. The mode of action of neonicotinoids on insects. Növényvédelem 51(1), 14–24 (2015).

    Google Scholar 

  • Stanley, D. A., Smith, K. E. & Raine, N. E. Bumblebee learning and memory is impaired by chronic exposure to a neonicotinoid pesticide. Sci. Rep. 5, 16508 (2015).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Alghamdi, A., Dalton, L., Phillis, A., Rosato, E. & Mallon, E. B. Immune response impairs learning in free-flying bumble-bees. Biol. Lett. 4(5), 479–481 (2008).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Mallon, E. B., Brockmann, A. & Schmid-Hempel, P. Immune response inhibits associative learning in insects. Proc. Royal Soc. London Series B Biol. Sci. 270(1532), 2471–2473 (2003).

    Article 

    Google Scholar 

  • Riddell, C. E. & Mallon, E. B. Insect psychoneuroimmunology: Immune response reduces learning in protein starved bumblebees (Bombus terrestris). Brain Behav. Immun. 20(2), 135–138 (2006).

    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Fries, I. et al. Molecular characterization of Nosema bombi (Microsporidia: Nosematidae) and a note on its sites of infection in Bombus terrestris (Hymenoptera: Apoidea). J. Apic. Res. 40(3–4), 91–96 (2001).

    CAS 
    Article 

    Google Scholar 

  • Siviter, H., Folly, A. J., Brown, M. J. F. & Leadbeater, E. Individual and combined impacts of sulfoxaflor and Nosema bombi on bumblebee (Bombus terrestris) larval growth. Proc. R. Soc. B 287(1932), 20200935 (2020).

    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Charbonneau, L. R., Hillier, N. K., Rogers, R. E., Williams, G. R. & Shutler, D. Effects of Nosema apis, N. ceranae, and coinfections on honey bee (Apis mellifera) learning and memory. Sci. Rep. 6, 22626 (2016).

    ADS 
    CAS 
    PubMed 
    PubMed Central 
    Article 

    Google Scholar 

  • Gage, S. L. et al. Nosema ceranae parasitism impacts olfactory learning and memory and neurochemistry in honey bees (Apis mellifera). J. Exp. Biol. 221(4), jeb161489. https://doi.org/10.1242/jeb.161489 (2018).

    Article 
    PubMed 

    Google Scholar 

  • Piiroinen, S. & Goulson, D. Chronic neonicotinoid pesticide exposure and parasite stress differentially affects learning in honeybees and bumblebees. Proc. Royal Soc. B Biol. Sci. 283(1828), 20160246 (2016).

    Article 
    CAS 

    Google Scholar 

  • Bell, H. C., Montgomery, C. N., Benavides, J. E. & Nieh, J. C. Effects of nosema ceranae (Dissociodihaplophasida: Nosematidae) and flupyradifurone on olfactory learning in honey bees, Apis mellifera (Hymenoptera: Apidae). J. Insect Sci. https://doi.org/10.1093/jisesa/ieaa130 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar 

  • Brown, M. J. F., Loosli, R. & Schmid-Hempel, P. Condition-dependent expression of virulence in a trypanosome infecting bumblebees. Oikos 91(3), 421–427. https://doi.org/10.1034/j.1600-0706.2000.910302.x (2000).

    Article 

    Google Scholar 

  • Siviter, H., Brown, M. J. F. & Leadbeater, E. Sulfoxaflor exposure reduces bumblebee reproductive success. Nature 561(7721), 109–112 (2018).

    ADS 
    CAS 
    PubMed 
    Article 

    Google Scholar 

  • Worden, B. D., Skemp, A. K. & Papaj, D. R. Learning in two contexts: The effects of interference and body size in bumblebees. J. Exp. Biol. 208(11), 2045–2053 (2005).

    PubMed 
    Article 

    Google Scholar 

  • Riveros, A. J. & Gronenberg, W. Olfactory learning and memory in the bumblebee Bombus occidentalis. Naturwissenschaften 96(7), 851–856. https://doi.org/10.1007/s00114-009-0532-y (2009).

    ADS 
    CAS 
    Article 
    PubMed 

    Google Scholar 

  • Mares, S., Ash, L. & Gronenberg, W. Brain allometry in bumblebee and honey bee workers. Brain Behav. Evol. 66(1), 50–61. https://doi.org/10.1159/000085047 (2005).

    Article 
    PubMed 

    Google Scholar 

  • Arce, A. N. et al. Foraging bumblebees acquire a preference for neonicotinoid-treated food with prolonged exposure. Proc. Royal Soc. B Biol. Sci. 285(1885), 20180655. https://doi.org/10.1098/rspb.2018.0655 (2018).

    CAS 
    Article 

    Google Scholar 

  • Muth, F., Gaxiola, R. L. & Leonard, A. S. No evidence for neonicotinoid preferences in the bumblebee Bombus impatiens. Royal Soc. Open Sci. 7(5), 191883 (2020).

    ADS 
    CAS 
    Article 

    Google Scholar 

  • Rutrecht, S. T. & Brown, M. J. F. Differential virulence in a multiple-host parasite of bumble bees: resolving the paradox of parasite survival?. Oikos 118(6), 941–949 (2009).

    Article 

    Google Scholar 

  • Schmid-Hempel, P., Puhr, K., Krüger, N., Reber, C. & Schmid-Hempel, R. Dynamic and genetic consequences of variation in horizontal transmission for a microparasitic infection. Evolution 53(2), 426–434 (1999).

    PubMed 
    Article 

    Google Scholar 

  • Evans, L. J., Raine, N. E. & Leadbeater, E. Reproductive environment affects learning performance in bumble bees. Behav. Ecol. Sociobiol. 70(12), 2053–2060 (2016).

    Article 

    Google Scholar 

  • Cole, R. J. The application of the “triangulation” method to the purification of nosema spores from insect tissues. J. Invertebr. Pathol. 15(2), 193–195. https://doi.org/10.1016/0022-2011(70)90233-8 (1970).

    Article 

    Google Scholar 

  • Folly, A. J., Barton-Navarro, M. & Brown, M. J. F. Exposure to nectar-realistic sugar concentrations negatively impacts the ability of the trypanosome parasite (Crithidia bombi) to infect its bumblebee host. Ecol. Entomol. 45(6), 1495–1498 (2020).

    Article 

    Google Scholar 

  • Schlüns, H., Sadd, B. M., Schmid-Hempel, P. & Crozier, R. H. Infection with the trypanosome Crithidia bombi and expression of immune-related genes in the bumblebee Bombus terrestris. Dev. Comp. Immunol. 34(7), 705–709 (2010).

    PubMed 
    Article 
    CAS 

    Google Scholar 

  • Yourth, C., Brown, M. J. F. & Schmid-Hempel, P. Effects of natal and novel Crithidia bombi (trypanosomatidae) infections on Bombus terrestris hosts. Insectes Soc. 55(1), 86–90. https://doi.org/10.1007/s00040-007-0974-1 (2008).

    Article 

    Google Scholar 

  • Fournier, A., Rollin, O., Le Féon, V., Decourtye, A. & Henry, M. Crop-emptying rate and the design of pesticide risk assessment schemes in the honey bee and wild bees (Hymenoptera: Apidae). J. Econ. Entomol. 107(1), 38–46 (2014).

    PubMed 
    Article 

    Google Scholar 

  • Samuelson, E. E. W., Chen-Wishart, Z. P., Gill, R. J. & Leadbeater, E. Effect of acute pesticide exposure on bee spatial working memory using an analogue of the radial-arm maze. Sci. Rep. 6(1), 1–11 (2016).

    Article 
    CAS 

    Google Scholar 

  • R Core Team. (2020). R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

  • Kassambara, A., Kosinski, M., Biecek, P., & Fabian, S. (2020). survminer: drawing survival curves using ‘ggplot2’. R package version 0.4. 8. 2019.

  • Therneau, T. M. & Lumley, T. Package ‘survival’. R Top Doc 128(10), 28–33 (2020).

    Google Scholar 

  • Bartoń, K. (2020). MuMIn: Multi-Model Inference. R package ver. 1.43. 17. CRAN: The Comprehensive R Archive Network, Berkeley, CA, USA.

  • Wickham, H. ggplot2: Elegant Graphics for Data Analysis (Springer-Verlag, 2016).

    MATH 
    Book 

    Google Scholar 

  • Burnham, K. P., & Anderson, D. R. (2002). A practical information-theoretic approach. Model selection and multimodel inference, 2.


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