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Pesticide reduces bumblebee colony initiation and increases probability of population extinction

Nature Ecology & Evolution volume 1, pages 1308–1316 (2017)Cite this article

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Abstract

Pollinators are in global decline and agricultural pesticides are a potential driver of this. Recent studies have suggested that pesticides may significantly impact bumblebee colonies—an important and declining group of pollinators. Here, we show that colony-founding queens, a critical yet vulnerable stage of the bumblebee lifecycle, are less likely to initiate a colony after exposure to thiamethoxam, a neonicotinoid insecticide. Bombus terrestris queens were exposed to field-relevant levels of thiamethoxam and two natural stressors: the parasite Crithidia bombi and varying hibernation durations. Exposure to thiamethoxam caused a 26% reduction in the proportion of queens that laid eggs, and advanced the timing of colony initiation, although we did not detect impacts of any experimental treatment on the ability of queens to produce adult offspring during the 14-week experimental period. As expected from previous studies, the hibernation duration also had an impact on egg laying, but there was no significant interaction with insecticide treatment. Modelling the impacts of a 26% reduction in colony founding on population dynamics dramatically increased the likelihood of population extinction. This shows that neonicotinoids can affect this critical stage in the bumblebee lifecycle and may have significant impacts on population dynamics.

Bees play a vital role as pollinators in both agricultural and natural systems1,2,3,4. However, there is increasing concern about the state of wild bee populations. Nearly 10% of European bee species are currently considered threatened5 and bumblebees are declining on a global scale5,6,7,8,9. The cause of these declines is thought to be a combination of factors, particularly habitat loss10, parasites and diseases11,12,13, invasive species14, and climate change15,16. Pesticide use is also considered a major threat to wild bees17,18,19,20, and both laboratory21,22,23,24,25,26, semi-field27,28,29,30,31,32,33 and field studies34,35,36 have found negative impacts of pesticides on bumblebee behaviour, reproduction and colony success. However, information on the impacts of pesticides on the key life history stages of wild bees is still lacking. Bumblebees, like solitary bees, have an annual lifecycle whereby reproductive females (queens) initiate a colony in the spring37. Bumblebee queens are functionally solitary at this stage and do not have a colony to buffer them from environmental stress. Success depends entirely on the queen’s survival and ability to initiate a colony and, as such, this represents a critical but vulnerable period in the lifecycle. Although bumblebee queens are likely to be exposed to a range of pesticides throughout their lifecycle, particularly when foraging in the early spring on flowering crops such as OSR, to date there has been no research on the impacts of pesticides on founding queens and their ability to initiate a colony. Rundlöf et al.34 found that neonicotinoid treatment of OSR crops resulted in a lack of brood-cell building in solitary bees, but the mechanism remained unexplored. Negative impacts of neonicotinoids on the reproduction of the honeybee Apis mellifera queen have also been found38,39, but honeybee colonies are perennial and the way in which this relates to the annual cycle in bumblebees remains unknown. However, given these results, it is vital that we understand the potential impacts of pesticides on bumblebee queens40,26 and the resultant implications for wild populations.

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Fig. 1: Effect of hibernation length and pesticide exposure on colony initiation.
Fig. 2: Effect of pesticide exposure on egg laying.
Fig. 3: Effect of pesticide exposure on colony capacity.

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References

  1. Corbet, S. A., Williams, I. H. & Osborne, J. L. Bees and the pollination of crops and wild flowers in the European community. Bee World 72, 47–59 (1991).

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  4. Garibaldi, L. A. et al. Wild pollinators enhance fruit set of crops regardless of honey bee abundance. Science 339, 1608–1611 (2013).

    Article  PubMed  CAS  Google Scholar 

  5. Nieto, A. et al. European Red List of Bees (Publication Office of the European Union, Luxembourg, 2014).

    Google Scholar 

  6. Williams, P. H. The distribution and decline of British bumble bees (Bombus Latr). J. Apic. Res. 21, 236–245 (1982).

    Article  Google Scholar 

  7. Fitzpatrick, Ú. et al. Rarity and decline in bumblebees—a test of causes and correlates in the Irish fauna. Biol. Cons. 136, 185–194 (2007).

    Article  Google Scholar 

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

    Article  PubMed  PubMed Central  Google Scholar 

  9. Schmid-Hempel, R. et al. The invasion of southern South America by imported bumblebees and associated parasites. J. Anim. Ecol. 83, 823–837 (2014).

    Article  PubMed  Google Scholar 

  10. Carvell, C. et al. Declines in forage availability for bumblebees at a national scale. Biol. Cons. 132, 481–489 (2006).

    Article  Google Scholar 

  11. Meeus, I., Brown, M. J. F., De Graaf, D. C. & Smagghe, G. Effects of invasive parasites on bumble bee declines. Cons. Biol. 25, 662–671 (2011).

    Article  Google Scholar 

  12. Fürst, M. A., McMahon, D. P., Osborne, J. L., Paxton, R. J. & Brown, M. J. F. Disease associations between honeybees and bumblebees as a threat to wild pollinators. Nature 506, 364–366 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  13. McMahon, D. P. et al. A sting in the spit: widespread cross‐infection of multiple RNA viruses across wild and managed bees. J. Anim. Ecol. 84, 615–624 (2015).

    Article  PubMed  PubMed Central  Google Scholar 

  14. Stout, J. C. & Morales, C. L. Ecological impacts of invasive alien species on bees. Apidologie 40, 388–409 (2009).

    Article  Google Scholar 

  15. Memmott, J., Craze, P. G., Waser, N. M. & Price, M. V. Global warming and the disruption of plant–pollinator interactions. Ecol. Lett. 10, 710–717 (2007).

    Article  PubMed  Google Scholar 

  16. Kerr, J. T. et al. Climate change impacts on bumblebees converge across continents. Science 349, 177–180 (2015).

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  18. Godfray, H. C. J. et al. A restatement of the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proc. R. Soc. Lond. B 281, 20140558 (2014).

    Article  Google Scholar 

  19. Godfray, H. C. J. et al. A restatement of recent advances in the natural science evidence base concerning neonicotinoid insecticides and insect pollinators. Proc. R. Soc. Lond. B 282, 20151821 (2015).

    Article  CAS  Google Scholar 

  20. Woodcock, B. A. et al. Impacts of neonicotinoid use on long-term population changes in wild bees in England. Nat. Commun. 7, 12459 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  21. Laycock, I., Lenthall, K. M., Barratt, A. T. & Cresswell, J. E. Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology 21, 1937–1945 (2012).

    Article  PubMed  CAS  Google Scholar 

  22. Bryden, J., Gill, R. J., Mitton, R. A. A., Raine, N. E. & Jansen, V. A. A. Chronic sublethal stress causes bee colony failure. Ecol. Lett. 16, 1463–1469 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  23. Baron, G. L., Raine, N. E. & Brown, M. J. F. Impact of chronic exposure to a pyrethroid pesticide on bumblebees and interactions with a trypanosome parasite. J. Appl. Ecol. 51, 460–469 (2014).

    Article  CAS  Google Scholar 

  24. 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, 450–459 (2014).

    Article  Google Scholar 

  25. 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).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  26. Baron, G. L., Raine, N. E. & Brown, M. J. F. General and species-specific impacts of a neonicotinoid insecticide on the ovary development and feeding of wild bumblebee queens. Proc. R. Soc. Lond. B 284, 20170123 (2017).

    Article  CAS  Google Scholar 

  27. Stanley, D. A. & Raine, N. E. Chronic exposure to a neonicotinoid pesticide alters the interactions between bumblebees and wild plants. Funct. Ecol. 30, 1132–1139 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

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

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  29. Whitehorn, P. R., O’Connor, S., Wackers, F. L. & Goulson, D. Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336, 351–352 (2012).

    Article  PubMed  CAS  Google Scholar 

  30. Gill, R. J. & Raine, N. E. Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure. Funct. Ecol. 28, 1459–1471 (2014).

    Article  Google Scholar 

  31. Feltham, H., Park, K. & Goulson, D. Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency. Ecotoxicology 23, 317–323 (2014).

    Article  PubMed  CAS  Google Scholar 

  32. Stanley, D. A. et al. Investigating the impacts of field-realistic exposure to a neonicotinoid pesticide on bumblebee foraging, homing ability and colony growth. J. Appl. Ecol. 53, 1440–1449 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  33. Stanley, D. A. et al. Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature 528, 548–550 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  34. Rundlöf, M. et al. Seed coating with a neonicotinoid insecticide negatively affects wild bees. Nature 521, 77–80 (2015).

    Article  PubMed  CAS  Google Scholar 

  35. Woodcock, B. A. et al. Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science 356, 1393–1395 (2017).

    Article  PubMed  CAS  Google Scholar 

  36. Ellis, C. et al. The neonicotinoid insecticide thiacloprid impacts upon bumblebee colony development under field conditions. Environ. Sci. Technol. 51, 1727–1732 (2017).

    Article  PubMed  CAS  Google Scholar 

  37. Sladen, F. W. L. The Humble-Bee: its Life-History and How to Domesticate it, With Descriptions of All the British Species, of Bombus and Psithyrus (Macmillan, London, 1912).

    Book  Google Scholar 

  38. Williams, G. R. et al. Neonicotinoid pesticides severely affect honey bee queens. Sci. Rep. 5, 14621 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  39. Wu-Smart, J. & Spivak, M. Sub-lethal effects of dietary neonicotinoid insecticide exposure on honey bee queen fecundity and colony development. Sci. Rep. 6, 32108 (2016).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  40. Fauser, A., Sandrock, C., Neumann, P. & Sadd, B. M. Neonicotinoids override a parasite exposure impact on hibernation success of a key bumblebee pollinator. Ecol. Entomol. 42, 306–314 (2017).

    Article  Google Scholar 

  41. Goulson, D. An overview of the environmental risks posed by neonicotinoid insecticides. J. Appl. Ecol. 50, 977–987 (2013).

    Article  Google Scholar 

  42. Forister, M. L. et al. Increasing neonicotinoid use and the declining butterfly fauna of lowland California. Biol. Lett. 12, 2016047 (2016).

    Article  Google Scholar 

  43. Hallmann, C. A., Foppen, R. P., van Turnhout, C. A., de Kroon, H. & Jongejans, E. Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature 511, 341–343 (2014).

    Article  PubMed  CAS  Google Scholar 

  44. Alford, D. V. A study of the hibernation of bumblebees (Hymenoptera: Bombidae) in southern England. J. Anim. Ecol. 38, 149–170 (1969).

    Article  Google Scholar 

  45. Holm, S. N. Weight and life length of hibernating bumble bee queens (Hymenoptera: Bombidae) under controlled conditions. Entomol. Scand. 3, 313–320 (1972).

    Article  Google Scholar 

  46. Beekman, M., van Stratum, P. & Lingeman, R. Diapause survival and post-diapause performance in bumblebee queens (Bombus terrestris). Entomol. Exp. Appl. 89, 207–214 (1998).

    Article  Google Scholar 

  47. Korner, P. & Schmid-Hempel, P. Effects of sperm on female longevity in the bumble-bee Bombus terrestris L. Proc. R. Soc. Lond. B 270, S227–S229 (2003).

    Article  Google Scholar 

  48. Yourth, C. P., Brown, M. J. F. & Schmid-Hempel, P. Effects of natal and novel Crithidia bombi (Trypanosomatidae) infections on Bombus terrestris hosts. Insectes Soc. 55, 86–90 (2008).

    Article  Google Scholar 

  49. Brown, M. J. F., Schmid-Hempel, R. & Schmid-Hempel, P. Strong context-dependent virulence in a host-parasite system: reconciling genetic evidence with theory. J. Anim. Ecol. 72, 994–1002 (2003).

    Article  Google Scholar 

  50. Hanski, I. & Ovaskainen, O. The metapopulation capacity of a fragmented landscape. Nature 404, 755–758 (2000).

    Article  PubMed  CAS  Google Scholar 

  51. Baer, B. & Schmid-Hempel, P. Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris. Evolution 55, 1639–1643 (2001).

    Article  PubMed  CAS  Google Scholar 

  52. Zuur, A., Hilbe, J. M. & Ieno, E. N. A Beginner’s Guide to GLM and GLMM with R (Highland Statistics, Newburgh, 2013).

    Google Scholar 

  53. Thornhill, J. A., Jones, J. T. & Kusel, J. R. Increased oviposition and growth in an immature Biomphalaria glabrata after exposure to Schistoma mansoni. Parasitology 93, 443–450 (1986).

    Article  PubMed  Google Scholar 

  54. Chadwick, W. & Little, T. J. A parasite-mediated life-history shift in Daphnia magna. Proc. R. Soc. Lond. B 272, 505–509 (2005).

    Article  Google Scholar 

  55. Sakwinska, O. Response to fish kairomone in Daphnia galeata life history traits relies on shift to earlier instar at maturation. Oecologia 131, 409–417 (2002).

    Article  PubMed  Google Scholar 

  56. Moret, Y. & Schmid-Hempel, P. Social life-history response to individual immune challenge of workers of Bombus terrestris L.: a possible new cooperative phenomenon. Ecol. Lett. 7, 146–152 (2004).

    Article  Google Scholar 

  57. Boncristiani, H. et al. Direct effect of acaricides on pathogen loads and gene expression levels in honey bees Apis mellifera. J. Insect Physiol. 58, 613–620 (2012).

    Article  PubMed  CAS  Google Scholar 

  58. Aufauvre, J. et al. Transcriptome analyses of the honeybee response to Nosema ceranae and insecticides. PLoS ONE 9, e91686 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Elston, C., Thompson, H. M. & Walters, K. F. A. Sub-lethal effects of thiamethoxam, a neonicotinoid pesticide, and propiconazole, a DMI fungicide, on colony initiation in bumblebee (Bombus terrestris) micro-colonies. Apidologie 44, 563–574 (2013).

    Article  CAS  Google Scholar 

  60. Sandrock, C. et al. Sublethal neonicotinoid insecticide exposure reduces solitary bee reproductive success. Agric. For. Entomol. 16, 119–128 (2014).

    Article  Google Scholar 

  61. Cresswell, J. E., Merritt, S. Z. & Martin, M. M. The effect of dietary nicotine on the allocation of assimilated food to energy metabolism and growth in fourth-instar larvae of the southern armyworm, Spodoptera eridania (Lepidoptera: Noctuidae). Oecologia 89, 449–453 (1992).

    Article  PubMed  Google Scholar 

  62. Cresswell, J. E., Robert, F.-X. L., Florance, H. & Smirnoff, N. Clearance of ingested neonicotinoid pesticide (imidacloprid) in honey bees (Apis mellifera) and bumblebees (Bombus terrestris). Pest Manag. Sci. 70, 332–337 (2014).

    Article  PubMed  CAS  Google Scholar 

  63. 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, e29268 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  64. Stewart, S. D. et al. Potential exposure of pollinators to neonicotinoid insecticides from the use of insecticide seed treatments in the mid-Southern United States. Environ. Sci. Technol. 48, 9762–9769 (2014).

    Article  PubMed  CAS  Google Scholar 

  65. Botías, C. et al. Neonicotinoid residues in wildflowers, a potential route of chronic exposure for bees. Environ. Sci. Technol. 49, 12731–12740 (2015).

    Article  PubMed  CAS  Google Scholar 

  66. Garthwaite, D. et al. Arable Crops in the United Kingdom 2014 (Food and Environment Research Agency, York, 2014).

    Google Scholar 

  67. Kessler, S. C. et al. Bees prefer foods containing neonicotinoid pesticides. Nature 521, 74–76 (2015).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  68. Scholer, J. & Krischik, V. Chronic exposure of imidacloprid and clothianidin reduce queen survival, foraging, and nectar storing in colonies of Bombus impatiens. PLoS ONE 9, e91573 (2014).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  69. Carolan, J. C. et al. Colour patterns do not diagnose species: quantitative evaluation of a DNA barcoded cryptic bumblebee complex. PLoS ONE 7, e29251 (2012).

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  70. Cole, R. J. Application of triangulation method to purification of Nosema spores from insect tissues. J. Invertebr. Pathol. 15, 193–195 (1970).

    Article  Google Scholar 

  71. Ulrich, Y., Sadd, B. M. & Schmid-Hempel, P. Strain filtering and transmission of a mixed infection in a social insect. J. Evol. Biol. 24, 354–362 (2011).

    Article  PubMed  CAS  Google Scholar 

  72. Thompson, H. et al. Effects of Neonicotinoid Seed Treatments on Bumble Bee Colonies under Field Conditions (Food and Environment Research Agency, York, 2013).

    Google Scholar 

  73. 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 (2016).

    Article  PubMed  CAS  Google Scholar 

  74. R Development Core Team. R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, Vienna, Austria, 2014).

    Google Scholar 

  75. Bates, D., Maechler, M., Bolker, B. & Walker, S. lme4: Linear Mixed-Effects Models using ‘Eigen’ and S4. R Package Version 1.1–7 (2014); http://lme4.r-forge.r-project.org/.

  76. Therneau, T. A Package for Survival Analysis in S. R package v. 2.37-7 (2014); https://CRAN.R-project.org/package=survival.

  77. Zuur, A., Ieno, E. N., Walker, N., Saveliev, A. A. & Smith, G. M. Mixed Effects Models and Extensions in Ecology with R (Springer, New York, 2009).

    Book  Google Scholar 

  78. Johnson, J. B. & Omland, K. S. Model selection in ecology and evolution. Trends Ecol. Evol. 19, 101–108 (2004).

    Article  PubMed  Google Scholar 

  79. Baer, B. & Schmid-Hempel, P. Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397, 151–154 (1999).

    Article  CAS  Google Scholar 

  80. Mills, M. Introducing Survival and Event History Analysis (SAGE, London, 2011).

    Book  Google Scholar 

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Acknowledgements

The authors thank S. Baldwin, B. McCrea, O. Ramos-Rodriguez and D. Wells for assistance in the laboratory and L. Evans, M. Fürst, C. Jones, E. Leadbeater, F. Manfredini, K. Smith and D. Stanley for comments. We thank The Crown Estate for permission to collect wild bumblebees at Windsor Great Park and S. Doble for permission to survey fields at Shiplake Farm. This study was supported by the UK Insect Pollinators Initiative grants BB/I000178/1 (awarded to N.E.R.) and BB/1000151/1 (awarded to M.J.F.B. and V.A.A.J.), funded jointly by the Living with Environmental Change programme, Biotechnology and Biological Sciences Research Council, Wellcome Trust, Scottish Government, Department for Environment, Food and Rural Affairs and Natural Environment Research Council, and a Natural Environment Research Council studentship to G.L.B. N.E.R. is supported as the Rebanks Family Chair in Pollinator Conservation by The W. Garfield Weston Foundation.

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  1. Mark J. F. Brown and Nigel E. Raine contributed equally to this work.

Authors and Affiliations

  1. School of Biological Sciences, Royal Holloway University of London, Egham, TW20 0EX, UK

    Gemma L. Baron, Vincent A. A. Jansen, Mark J. F. Brown & Nigel E. Raine

  2. School of Environmental Sciences, University of Guelph, Guelph, Ontario, N1G 2W1, Canada

    Nigel E. Raine

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G.L.B., M.J.F.B. and N.E.R. conceived the project and designed the experiment. G.L.B. carried out the experiment and statistical analyses. V.A.A.J. carried out the modelling. All authors contributed to writing the paper.

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Correspondence to Gemma L. Baron, Vincent A. A. Jansen, Mark J. F. Brown or Nigel E. Raine.

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Baron, G.L., Jansen, V.A.A., Brown, M.J.F. et al. Pesticide reduces bumblebee colony initiation and increases probability of population extinction. Nat Ecol Evol 1, 1308–1316 (2017). https://doi.org/10.1038/s41559-017-0260-1

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