Advertisement

Ecotoxicology

, Volume 25, Issue 6, pp 1150–1159 | Cite as

The neonicotinoid pesticide, imidacloprid, affects Bombus impatiens (bumblebee) sonication behavior when consumed at doses below the LD50

  • Callin M. SwitzerEmail author
  • Stacey A. Combes
Article

Abstract

We investigated changes in sonication (or buzz-pollination) behavior of Bombus impatiens bumblebees, after consumption of the neonicotinoid pesticide, imidacloprid. We measured sonication frequency, sonication length, and flight (wing beat) frequency of marked bees collecting pollen from Solanum lycopsersicum (tomato), and then randomly assigned bees to consume 0, 0.0515, 0.515, or 5.15 ng of imidacloprid. We recorded the number of bees in each treatment group that resumed sonication behavior after consuming imidacloprid, and re-measured sonication and flight behavior for these bees. We did not find evidence that consuming 0.0515 ng imidacloprid affected the sonication length, sonication frequency, or flight frequency for bees that sonicated after consuming imidacloprid; we were unable to test changes in these variables for bees that consumed 0.515 or 5.15 ng because we did not observe enough of these bees sonicating after treatment. We performed Cox proportional hazard regression to determine whether consuming imidacloprid affected the probability of engaging in further sonication behavior on S. lycopersicum and found that bumblebees who consumed 0.515 or 5.15 ng of imidacloprid were significantly less likely to sonicate after treatment than bees who consumed no imidacloprid. At the end of the experiment, we classified bees as dead or alive; our data suggest a trend of increasing mortality with higher doses of imidacloprid. Our results show that even modest doses of imidacloprid can significantly affect the likelihood of bumblebees engaging in sonication, a behavior critical for the pollination of a variety of crops and other plants.

Keywords

Buzz pollination Native bees Pollination Solanum Tomato Vibration 

Notes

Acknowledgments

We thank Justin Dower for assistance in data collection for preliminary trials of this experiment. C.S. was supported through the National Defense Science & Engineering Graduate Fellowship (NDSEG) Program, 32 CFR 168a. This project was funded by the National Science Foundation (CAREER IOS-1253677) to S.C.

Funding

We have also included all sources of funding in the acknowledgments.

Compliance with ethical standards

Conflict of Interest

The authors declare that they have no conflict of interest.

Ethical statement

The manuscript has not been submitted to other journal simultaneously. It has not been published previously. The study has not been split into several parts to increase the quantity of submissions. The data have not been fabricated or manipulated. No theories or text are plagiarized, though the methods section is very similar to the methods presented in another submitted manuscript of ours. All authors have given consent to submit the article, and all authors have contributed significantly to the manuscript.

References

  1. Armstrong R, Hilton A (2010) Stepwise multiple regression. In: Armstrong R, Hilton A (eds) Statistical analysis in microbiology: statNotes, 1st edn. Wiley, New Jersey, pp 135–138Google Scholar
  2. Audacity Development Team (2015) Audacity (Version 1.2. 6). https://sourceforge.net/projects/audacity/
  3. Beketov MA, Liess M (2008) Acute and delayed effects of the neonicotinoid insecticide thiacloprid on seven freshwater arthropods. Environ Toxicol Chem 27(2):461–470CrossRefGoogle Scholar
  4. Bertsch A (1984) Foraging in male bumblebees (Bombus lucorum L.): maximizing energy or minimizing water load? Oecologia 62(3):325–336CrossRefGoogle Scholar
  5. Beutler R (1951) Time and distance in the life of the foraging bee. Bee World 32:25–27CrossRefGoogle Scholar
  6. Blacquiere T, Smagghe G, Van Gestel CA, Mommaerts V (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21(4):973–992CrossRefGoogle Scholar
  7. Bonmatin JM, Moineau I, Charvet R, Fleche C, Colin ME, Bengsch ER (2003) A LC/APCI-MS/MS method for analysis of imidacloprid in soils, in plants, and in pollens. Anal Chem 75(9):2027–2033CrossRefGoogle Scholar
  8. Bortolotti L, Montanari R, Marcelino J, Medrzycki P, Maini S, Porrini C (2003) Effects of sub-lethal imidacloprid doses on the homing rate and foraging activity of honey bees. Bull Insectol 56:63–68Google Scholar
  9. Buchmann SL (1983) Buzz pollination in angiosperms. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. van Nostrand Reinhold Company Inc., New York, pp 73–113Google Scholar
  10. Byrne FJ, Visscher PK, Leimkuehler B, Fischer D, Grafton-Cardwell EE, Morse JG (2014) Determination of exposure levels of honey bees foraging on flowers of mature citrus trees previously treated with imidacloprid. Pest Manag Sci 70(3):470–482CrossRefGoogle Scholar
  11. Crailsheim K, Schneider LHW, Hrassnigg N, Bühlmann G, Brosch U, Gmeinbauer R, Schöffmann B (1992) Pollen consumption and utilization in worker honeybees (Apis mellifera carnica): dependence on individual age and function. J Insect Physiol 38(6):409–419CrossRefGoogle Scholar
  12. Decourtye A, Lacassie E, Pham-Delègue MH (2003) Learning performances of honeybees (Apis mellifera L.) are differentially affected by imidacloprid according to the season. Pest Manag Sci 59(3):269–278CrossRefGoogle Scholar
  13. Decourtye A, Henry M, Desneux N (2013) Environment: overhaul pesticide testing on bees. Nature 497(7448):188CrossRefGoogle Scholar
  14. Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106CrossRefGoogle Scholar
  15. European Commission (2013) Bee health: EU-wide restrictions on pesticide use to enter into force. European Commission, BrusselsGoogle Scholar
  16. Feltham H, Park K, Goulson D (2014) Field realistic doses of pesticide imidacloprid reduce bumblebee pollen foraging efficiency. Ecotoxicology 23(3):317–323CrossRefGoogle Scholar
  17. Fischer J, Müller T, Spatz AK, Greggers U, Gruenewald B, Menzel R (2014) Neonicotinoids interfere with specific components of navigation in honeybees. PLoS One 9(3):e91364CrossRefGoogle Scholar
  18. Gallai N, Salles JM, Settele J, Vaissière BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68(3):810–821CrossRefGoogle Scholar
  19. Gervais JA, Luukinen B, Buhl K, Stone D (2010) Imidacloprid technical fact sheet. National Pesticide Information Center, Oregon State University Extension Services. http://npic.orst.edu/factsheets/archive/imidacloprid.html. Accessed 11 Jan 2016
  20. Gill RJ, Raine NE (2014) Chronic impairment of bumblebee natural foraging behaviour induced by sublethal pesticide exposure. Funct Ecol 28(6):1459–1471CrossRefGoogle Scholar
  21. Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severely affects individual-and colony-level traits in bees. Nature 491(7422):105–108CrossRefGoogle Scholar
  22. Goulson D (2013) Review: an overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol 50(4):977–987CrossRefGoogle Scholar
  23. Goulson D, Nicholls E, Botías C, Rotheray EL (2015) Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347(6229):1255957CrossRefGoogle Scholar
  24. Han P, Niu CY, Lei CL, Cui JJ, Desneux N (2010) Use of an innovative T-tube maze assay and the proboscis extension response assay to assess sublethal effects of GM products and pesticides on learning capacity of the honey bee Apis mellifera L. Ecotoxicology 19(8):1612–1619CrossRefGoogle Scholar
  25. Henry M, Beguin M, Requier F, Rollin O, Odoux J, Aupinel P, Aptel J, Tchamitchian S, Decourtye A (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336(6079):348–350CrossRefGoogle Scholar
  26. Horikoshi M, Tang Y (2015) ggfortify: data visualization tools for statistical analysis results. R package version 0.0.4. http://CRAN.R-project.org/package=ggfortify. Accessed 11 Jan 2016
  27. Kagabu S, Kato C, Nishimura K (2004) Insecticidal and neuroblocking activities toward American cockroach (Periplaneta americana L.) of imidacloprid metabolites, 5-hydroxy-, 4, 5-dihydroxy-and 4, 5-dehydroimidacloprid. J Pestic Sci 29(4):376–379CrossRefGoogle Scholar
  28. Karahan A, Çakmak I, Hranitz JM, Karaca I, Wells H (2015) Sublethal imidacloprid effects on honey bee flower choices when foraging. Ecotoxicology 24(9):2017–2025CrossRefGoogle Scholar
  29. Klein AM, Vaissiere BE, Cane JH, Steffan-Dewenter I, Cunningham SA, Kremen C, Tscharntke T (2007) Importance of pollinators in changing landscapes for world crops. Proc R Soc B 274:303–313. doi: 10.1098/rspb.2006.3721 CrossRefGoogle Scholar
  30. Krischik VA, Landmark AL, Heimpel GE (2007) Soil-applied imidacloprid is translocated to nectar and kills nectar-feeding Anagyrus pseudococci (Girault) (Hymenoptera: Encyrtidae). Environ Entomol 36(5):1238–1245CrossRefGoogle Scholar
  31. Laycock I, Lenthall KM, Barratt AT, Cresswell JE (2012) Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology 21(7):1937–1945CrossRefGoogle Scholar
  32. Ligges U, Krey S, Mersmann O, Schnackenberg S (2013) tuneR: Analysis of music. R package. http://r-forge.r-project.org/projects/tuner/. Accessed 11 Jan 2016
  33. Malone LA, Burgess E, Stefanovic D, Gatehouse HS (2000) Effects of four protease inhibitors on the survival of worker bumblebees, Bombus terrestris L. Apidologie 31(1):25–38CrossRefGoogle Scholar
  34. Manso R, Fortin M, Calama R, Pardos M (2013) Modelling seed germination in forest tree species through survival analysis. The Pinus pinea L. case study. Forest Ecol Manag 289:515–524CrossRefGoogle Scholar
  35. Marletto F, Patetta A, Manino A (2003) Laboratory assessment of pesticide toxicity to bumblebees. Bull Insectol 56(1):155–158Google Scholar
  36. McGregor SE (1976) USDA agriculture handbook No. 496. Insect pollination of cultivated crops. USDA, WashingtonGoogle Scholar
  37. Meffe GK (1998) The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conserv Biol 12(1):8–17CrossRefGoogle Scholar
  38. Mullin CA, Frazier M, Frazier JL, Ashcraft S, Simonds R, Pettis JS (2010) High levels of miticides and agrochemicals in North American apiaries: implications for honey bee health. PLoS One 5(3):e9754CrossRefGoogle Scholar
  39. Mullins JW (1993) Imidacloprid. A new nitroguanidine insecticide. ACS Symp Ser 524:183–198CrossRefGoogle Scholar
  40. Nagata K, Iwanaga Y, Shono T, Narahashi T (1997) Modulation of the neuronal nicotinic acetylcholine receptor channel by imidacloprid and cartap. Pestic Biochem Physiol 59(2):119–128CrossRefGoogle Scholar
  41. Pohorecka K, Skubida P, Miszczak A, Semkiw P, Sikorski P, Zagibajło K, Teper D, Kołtowski Z, Skubida M, Zdańska D, Bober A (2012) Residues of neonicotinoid insecticides in bee collected plant materials from oilseed rape crops and their effect on bee colonies. J Apic Sci 56(2):115–134. doi: 10.2478/v10289-012-0029-3 Google Scholar
  42. Pollak P, Vouillamoz R (2011) Ullman’s fine chemicals. Wiley, GermanyCrossRefGoogle Scholar
  43. Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25(6):345–353CrossRefGoogle Scholar
  44. R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. https://www.R-project.org/
  45. Raine NE, Chittka L (2007) Pollen foraging: learning a complex motor skill by bumblebees (Bombus terrestris). Naturwissenschaften 94(6):459–464CrossRefGoogle Scholar
  46. Roessink I, Merga LB, Zweers HJ, Van den Brink PJ (2013) The neonicotinoid imidacloprid shows high chronic toxicity to mayfly nymphs. Environ Toxicol Chem 32(5):1096–1100CrossRefGoogle Scholar
  47. Rogers RE, Kemp JR (2003) Imidacloprid, potatoes, and honey bees in Atlantic Canada: is there a connection? Bull Insectol 56(1):83–88Google Scholar
  48. Rondeau G, Sánchez-Bayo F, Tennekes HA, Decourtye A, Ramírez-Romero R, Desneux N (2014) Delayed and time-cumulative toxicity of imidacloprid in bees, ants and termites. Sci Rep 4:5566CrossRefGoogle Scholar
  49. Rortais A, Arnold G, Halm MP, Touffet-Briens F (2005) Modes of honeybees exposure to systemic insecticides: estimated amounts of contaminated pollen and nectar consumed by different categories of bees. Apidologie 36(1):71–83CrossRefGoogle Scholar
  50. Schmuck R, Schöning R, Stork A, Schramel O (2001) Risk posed to honeybees (Apis mellifera L., Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Manag Sci 57(3):225–238CrossRefGoogle Scholar
  51. Silvola J (1984) Respiration and energetics of the bumblebee Bombus terrestris queen. Ecography 7(2):177–181CrossRefGoogle Scholar
  52. Stanley DA, Garratt MPD, Wickens JB, Potts SG, Raine NE (2015a) Neonicotinoid pesticide exposure impairs crop pollination services provided by bumblebees. Nature. doi: 10.1038/nature16167 Google Scholar
  53. Stanley DA, Smith KE, Raine NE (2015b) Bumblebee learning and memory is impaired by chronic exposure to a neonicotinoid pesticide. Sci Rep 5:16508. doi: 10.1038/srep16508 CrossRefGoogle Scholar
  54. Stoner KA, Eitzer BD (2012) Movement of soil-applied imidacloprid and thiamethoxam into nectar and pollen of squash (Cucurbita pepo). PLoS One 7(6):e39114CrossRefGoogle Scholar
  55. Suchail S, Guez D, Belzunces LP (2001) Discrepancy between acute and chronic toxicity induced by imidacloprid and its metabolites in Apis mellifera. Environ Toxicol Chem 20(11):2482–2486CrossRefGoogle Scholar
  56. Sueur J, Aubin T, Simonis C (2008) Equipment review: seewave, a free modular tool for sound analysis and synthesis. Bioacoustics 18(2):213–226CrossRefGoogle Scholar
  57. Switzer CM, Hogendoorn K, Ravi S, Combes SA (2016) Shakers and head bangers: differences in sonication behavior between Australian Amegilla murrayensis (blue-banded bees) and North American Bombus impatiens (bumblebees). Arthropod-Plant Interact 10(1):1–8CrossRefGoogle Scholar
  58. Tan K, Chen W, Dong S, Liu X, Wang Y, Nieh JC (2015) A neonicotinoid impairs olfactory learning in Asian honey bees (Apis cerana) exposed as larvae or as adults. Sci Rep 5:10989CrossRefGoogle Scholar
  59. Tennekes HA, Sánchez-Bayo F (2011) Time-dependent toxicity of neonicotinoids and other toxicants: implications for a new approach to risk assessment. J Environ Anal Toxicol S4:S4-001Google Scholar
  60. Therneau TM, Grambsch PM (2000) Modeling survival data: extending the cox model. Springer, New YorkCrossRefGoogle Scholar
  61. Thorp RW (2000) The collection of pollen by bees. Plant Syst Evol 222:211–223CrossRefGoogle Scholar
  62. Tomizawa M, Casida JE (2005) Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol 45:247–268CrossRefGoogle Scholar
  63. Unwin DM, Corbet SA (1984) Wingbeat frequency, temperature and body size in bees and flies. Physiol Entomol 9(1):115–121CrossRefGoogle Scholar
  64. Van den Brink PJ, Van Smeden JM, Bekele RS, Dierick W, De Gelder DM, Noteboom M, Roessink I (2016) Acute and chronic toxicity of neonicotinoids to nymphs of a mayfly species and some notes on seasonal differences. Environ Toxicol Chem 35(1):128–133CrossRefGoogle Scholar
  65. vanEngelsdorp D, Evans JD, Saegerman C, Mullin C, Haubruge E, Nguyen BK et al (2009) colony collapse disorder: a descriptive study. PLoS One 4(8):e6481sCrossRefGoogle Scholar
  66. Whitehorn PR, O’Connor S, Wackers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336(6079):351–352CrossRefGoogle Scholar
  67. Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer, New YorkCrossRefGoogle Scholar
  68. Zheng W, Liu WP, Wen YZ, Lee SJ (2003) Photochemistry of insecticide imidacloprid: direct and sensitized photolysis in aqueous medium. J Environ Sci (China) 16(4):539–542Google Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Department of Organismic and Evolutionary BiologyHarvard UniversityCambridgeUSA
  2. 2.Department of Neurobiology, Physiology, and BehaviorUniversity of California, DavisDavisUSA

Personalised recommendations