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Sublethal imidacloprid effects on honey bee flower choices when foraging

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Abstract

Neonicotinoids, systemic neuro-active pesticides similar to nicotine, are widely used in agriculture and are being investigated for a role in honey bee colony losses. We examined one neonicotinoid pesticide, imidacloprid, for its effects on the foraging behavior of free-flying honey bees (Apis mellifera anatoliaca) visiting artificial blue and white flowers. Imidacloprid doses, ranging from 1/5 to 1/50 of the reported LD50, were fed to bees orally. The study consisted of three experimental parts performed sequentially without interruption. In Part 1, both flower colors contained a 4 μL 1 M sucrose solution reward. Part 2 offered bees 4 μL of 1.5 M sucrose solution in blue flowers and a 4 μL 0.5 M sucrose solution reward in white flowers. In Part 3 we reversed the sugar solution rewards, while keeping the flower color consistent. Each experiment began 30 min after administration of the pesticide. We recorded the percentage of experimental bees that returned to forage after treatment. We also recorded the visitation rate, number of flowers visited, and floral reward choices of the bees that foraged after treatment. The forager return rate declined linearly with increasing imidacloprid dose. The number of foraging trips by returning bees was also affected adversely. However, flower fidelity was not affected by imidacloprid dose. Foragers visited both blue and white flowers extensively in Part 1, and showed greater fidelity for the flower color offering the higher sugar solution reward in Parts 2 and 3. Although larger samples sizes are needed, our study suggests that imidacloprid may not affect the ability to select the higher nectar reward when rewards were reversed. We observed acute, mild effects on foraging by honey bees, so mild that storage of imidacloprid tainted-honey is very plausible and likely to be found in honey bee colonies.

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References

  • Abramson CI, Wells PH, Wenner A, Wells H (2012) Odor, learning and behavior. In: Florio RM (ed) Bees, biology, threats and colonies. Nova Science Publishers Inc, New York, pp 125–145

    Google Scholar 

  • Abramson CI, Cakmak I, Duell ME, Bates-Albers LM, Zuniga EM, Pendegraft L, Barnett A, Cowo CL, Warren JJ, Albritton-Ford AC, Barthell JF, Hranitz JM, Wells H (2013) Feature-positive and feature-negative learning in honey bees. J Exp Biol 216:224–229

    Article  Google Scholar 

  • Aizen MA, Harder LD (2009) The global stock of domesticated honey bees is growing slower than agricultural demand for pollination. Curr Biol 19:915–918

    Article  CAS  Google Scholar 

  • Aizen MA, Garibaldi LA, Cunningham SA, Klein AM (2009) How much does agriculture depend on pollinators? Lessons from long-term trends in crop production. Ann Bot 103:1579–1588

    Article  Google Scholar 

  • Aliouane Y, el Hassani AK, Gary V, Armengaud C, Lambin M, Gauthier M (2009) Subchronic exposure of honeybees to sublethal doses of pesticides: effects on behavior. Environ Toxicol Chem 28:113–122

    Article  CAS  Google Scholar 

  • Allsopp MH, de Lange WJ, Veldtman R (2008) Valuing insect pollination services with cost of replacement. PLoS One. doi:10.1371/journal.pone.0003128

    Google Scholar 

  • Amaya-Marquez M, Hill PS, Abramson CI, Wells H (2014) Honey bee location- and time-linked memory use in novel foraging situations: floral color dependency. Insects 5(1):243–269. doi:10.3390/insects5010243

    Article  Google Scholar 

  • Arena M, Sgolastra F (2014) A meta-analysis comparing the sensitivity of bees to pesticides. Ecotoxicology 23:324–334

    Article  CAS  Google Scholar 

  • Avarques-Weber A, Giurfa M (2013) Conceptual learning by miniature brains. Proc Biol Sci 280:20131907

    Article  Google Scholar 

  • Blacquière T, Smagghe G, Vangestel CAM, Mommaerts V (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21:973–992. doi:10.1007/s10646-012-0863-x

    Article  Google Scholar 

  • Bonmatin JM, Marchand PA, Charvet R, Moineau I, Bengsh ER, Colin ME (2005) Quantification of imidacloprid uptake in maize crops. J Agric Food Chem 53:5336–5341

    Article  CAS  Google Scholar 

  • Breeze TD, Bailey AP, Balcombe KG, Potts SG (2011) Pollination services in the UK: how important are honeybees? Agric Ecosyst Environ 142:137–143

    Article  Google Scholar 

  • Breeze TD, Vaissiere BE, Bommarco R, Petanidou T, Seraphides N, Kozak L, Scheper J, Biesmeijer JC, Kleijn D, Gyldenkaerne S, Moretti M, Holzschuh A, Steffan-Dewenter I, Stout JC, Paertel M, Zobel M, Potts SG (2014) Agricultural policies exacerbate honeybee pollination service supply-demand mismatches across Europe. PLoS One. doi:10.1371/journal.pone.0082996

    Google Scholar 

  • Brittain CA, Vighi M, Bommarco R, Settele J, Potts SG (2010) Impacts of a pesticide on pollinator species richness at different spatial scales. Basic Appl Ecol 11:106–115

    Article  CAS  Google Scholar 

  • Bryden J, Gill RJ, Mitton RAA, Raine NE, Jansen VAA (2013) Chronic sublethal stress causes bee colony failure. Ecol Lett 16:1463–1469

    Article  Google Scholar 

  • Cakmak I, Sanderson C, Blocker TD, Pham LL, Checotah S, Norman AA, Harader-Pate BK, Reidenbaugh T, Nenchev P, Barthell JF, Well H (2009) Different solutions by bees to a foraging problem. Anim Behav 77(5):1273–1280

    Article  Google Scholar 

  • Calderone NW (2012) Insect pollinated crops, insect pollinators and US Agriculture: trend analysis of aggregate data for the period 1992–2009. PLoS One. doi:10.1371/journal.pone.0037235

    Google Scholar 

  • Carreck N, Ratnieks F (2014) The dose makes the poison: have “field realistic” rates of exposure of bees to neonicitinoid insecticides been overestimated in laboratory studies? J Apic Res 53(5):607–614

    Article  Google Scholar 

  • Colin ME, Bonmatin JM, Moineau I, Gaimon C, Brun S, Vermandere JP (2004) A method to quantify and analyze the foraging activity of honey bees: relevance to the sublethal effects induced by systemic insecticides. Arch Environ Contam Toxicol 47:387–395

    Article  CAS  Google Scholar 

  • Cressey D (2013) Europe debates risk to bees. Nature 496:408

    Article  CAS  Google Scholar 

  • Cresswell JE (2011) A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20:149–157

    Article  CAS  Google Scholar 

  • Cresswell JE, Desneux N, vanEngelsdorp D (2012a) Dietary traces of neonicotinoid pesticides as a cause of population declines in honey bees: an evaluation by Hill’s epidemiological criteria. Pest Manag Sci 68:819–827

    Article  CAS  Google Scholar 

  • Cresswell JE, Page CJ, Uygun MB, Holmbergh M, Li Y, Wheeler JG, Laycock I, Pook CJ, de Ibarra NH, Smirnoff N, Tyler CR (2012b) Differential sensitivity of honey bees and bumble bees to a dietary insecticide (imidacloprid). Zoology 115:365–371

    Article  Google Scholar 

  • Dag A (2009) Interaction between pollinators and crop plants: the Israeli experience. Isr J Plant Sci 57:231–242

    Article  Google Scholar 

  • de Lange WJ, Veldtman R, Allsopp MH (2013) Valuation of pollinator forage services provided by Eucalyptus cladocalyx. J Environ Manag 125:12–18

    Article  Google Scholar 

  • Decourtye A, Lacassie E, Pham-Delegue MH (2003) Learning performances of honeybees (Apis mellifera L.) are differentially affected by imidacloprid according to the season. Pest Manag Sci 59:269–278

    Article  CAS  Google Scholar 

  • Decourtye A, Devillers J, Aupinel P, Brun F, Bagnis C, Fourrier J, Gauthier M (2011) Honeybee tracking with microchips: a new methodology to measure the effects of pesticides. Ecotoxicology 20(2):429–437

    Article  CAS  Google Scholar 

  • DeGrandi-Hoffman G, Sammataro D, Simonds R (2012) Are agrochemicals present in high fructose corn syrup fed to honey bees (Apis mellifera L.)? J Apic Res 51:371–372

    Article  CAS  Google Scholar 

  • Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

    Article  CAS  Google Scholar 

  • Devillers J, Decourtye A, Budzinski H, Pham-Delegue MH, Cluzeau S, Maurin G (2003) Comparative toxicity and hazards of pesticides to Apis and non-Apis bees: a chemometrical study. SAR QSAR Environ Res 14:389–403

    Article  CAS  Google Scholar 

  • Dively GP, Embrey MS, Kamel A, Hawthorne DJ, Pettis JS (2015) Assessment of chronic sublethal effects of imidacloprid on honey bee colony health. PLoS One 10:e0118748

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Fischer J, Muller T, Spatz AK, Greggers U, Grunewald B, Menzel R (2014) Neonicotinoids interfere with specific components of navigation in honeybees. PLoS One. doi:10.1371/journal.pone.0091364

    Google Scholar 

  • Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491:105–119

    Article  CAS  Google Scholar 

  • Girolami V, Mazzon L, Squartini A, Mori N, Marzaro M, Di Bernardo A, Greatti M, Giorio C, Tapparo A (2009) Translocation of neonicotinoid insecticides from coated seeds to seedling guttation drops: a novel way of intoxication for bees. J Econ Entomol 102:1808–1815

    Article  CAS  Google Scholar 

  • Goulson D (2013) Review: an overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol 50:977–987

    Article  Google Scholar 

  • 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 19:1612–1619

    Article  CAS  Google Scholar 

  • Hill PSM, Wells PH, Wells H (1997) Spontaneous flower constancy and learning in honey bees as a function of colour. Anim Behav 54:615–627

    Article  Google Scholar 

  • Iwasa T, Motoyama N, Ambrose JT, Roe RM (2004) Mechanism for the differential toxicity of neonicotinoid insecticides in the honey bee, Apis mellifera. Crop Prot 23(5):371–378

    Article  CAS  Google Scholar 

  • Johnson DL, Wenner AM (1966) A relationship between conditioning and communication in honey bees. Anim Behav 14:261–265

    Article  CAS  Google Scholar 

  • Kandemir I, Kence M, Kence A (2000) Genetic and morphometric variation in honey bee (Apis mellifera L.) population of Turkey. Apidology 31:343–356

    Article  CAS  Google Scholar 

  • Kearns C, Inouye D, Waser N (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Syst Evol 29:83–112

    Article  Google Scholar 

  • Laycock I, Cotterell KC, O’shea-Wheller TA, Cresswell JE (2014) Effects of the neonicotinoid pesticide thiamethoxam at field-realistic levels on microcolonies of Bombus terrestris worker bumble bees. Ecotoxicol Environ Saf 100:153–158

    Article  CAS  Google Scholar 

  • Lu C, Warchol KM, Callahan RA (2012) In situ replication of honey bee colony collapse disorder. Bull Insectol 65:99–106

    Google Scholar 

  • Lu C, Warchol KM, Callahan RA (2014) Sub-lethal exposure to neonicotinoids impaired honey bees winterization before proceeding to colony collapse disorder. Bull Insectol 67:125–130

    CAS  Google Scholar 

  • Menzel R (2001) Searching for he memory trace in mini-brain the honeybee. Learn Mem 8:53–62

    Article  CAS  Google Scholar 

  • Michener CD (2007) The bees of the world, 2nd edn. The John Hopkins University Press, Baltimore

    Google Scholar 

  • Potts SG, Petanidou T, Roberts S, O’Toole C, Hulbert A, Willmer P (2006) Plant-pollinator biodiversity and pollination services in a complex Mediterranean landscape. Biol Conserv 129:519–529

    Article  Google Scholar 

  • Ramirez-Romero R, Chaufaux J, Pham-Delegue MH (2005) Effects of Cry1Ab prototoxin, deltamethrin and imidacloprid on the foraging activity and the learning performances of the honeybee, Apis mellifera: a comparative approach. Apidologie 36:601–611

    Article  CAS  Google Scholar 

  • Ramirez-Romero R, Desneux N, Decourtye A, Chaffiol A, Pham-Delegue MH (2008) Does Cry1Ab protein affect learning performances of the honeybee Apis mellifera L. (Hymenoptera, Apidae)? Ecotoxicol Environ Saf 70:327–333

    Article  CAS  Google Scholar 

  • Rondeau G, Sanchez-Bayo F, Tennekes HA, Decourtye A, Ramırez-Romero R, Desneux N (2013) Delayed and time-cumulative toxicity of imidacloprid in bees, ants and termites. Sci Rep 4:5566

    Google Scholar 

  • 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 36:71–83

    Article  CAS  Google Scholar 

  • Ruttner F (1988) Biogeography and taxonomy of honey-bees. Springer, Berlin

    Google Scholar 

  • Sall F, Lehman A (1996) JMP IN; SAS institute, Inc. Ducksberry Press, Belmont

    Google Scholar 

  • Sanderson CE, Cook P, Hill PSM, Orozco BS, Abramson CI, Wells H (2013) Nectar quality perception by honey bees (Apis mellifera ligustica). J Comp Psychol 127:341–351

    Article  Google Scholar 

  • Sandrock C, Tanadini M, Tanadini LG, Fauser-Misslin A, Potts SG, Neumann P (2014) Impact of chronic neonicotinoid exposure on honeybee colony performance and queen supersedure. PLoS One 9:e103592

    Article  Google Scholar 

  • Scholer J, Krischik V (2014) Chronic exposure of imidacloprid and clothianidin reduce queen survival, foraging, and nectar storing in colonies of Bombus impatiens. PLoS One. doi:10.1371/journal.pone.0091573

    Google Scholar 

  • Seeley TD (1995) The wisdom of the hive: the social physiology of honey bee colonies. Harvard University Press, Cambridge

    Google Scholar 

  • Sirinivasan M (2010) Honey bees as a model for vision, perception, and cognition. Annu Rev Entomol 55:267–284

    Article  Google Scholar 

  • Sokal RR, Rohlf RJ (1995) Biometry: the principles and practice of statistics in biological research, 3rd edn. W. H. Freeman and Co, New York

    Google Scholar 

  • Stoner KA, Eitzer BD (2012) Movement of soil-applied imidacloprid and thiamethoxam into nectar and pollen of squash (Cucurbita pepo). PLoS One. doi:10.1371/journal.pone.0039114

    Google Scholar 

  • Von Frisch K (1967) The dance language and orientation of bees. Belknap Press of Harvard University, Cambridge

    Google Scholar 

  • Wells H, Wells PH (1986) Optimal diet, minimal uncertainty and individual constancy in the foraging of honey bees, Apis mellifera. J Anim Ecol 55:881–891

    Article  Google Scholar 

  • Wenner AM (1989) Concept-centered versus organism-centered biology. Am Zool 29:1177–1197

    Article  Google Scholar 

  • Wenner AM, Wells PH (1990) Anatomy of a controversy: the question of a “language” among bees. Columbia University Press, New York

    Google Scholar 

  • Wenner AM, Wells PH, Johnson DL (1969) Honeybee recruitment to food sources: olfaction or language? Science 164:84–86

    Article  CAS  Google Scholar 

  • Whitehorn PR, O’Connor S, Wackers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumble bee colony growth and queen production. Science 336:351–352

    Article  CAS  Google Scholar 

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Acknowledgments

We thank S. Çakmak along with NSF-REU students L. Blatzheim, C. Bower and T. Polk for their help while at the Beekeeping Development, Application and Research Center (BDARC) of Uludag University. We are grateful to D. Ikizoğlu, M. Ertürk, H.Ç. Özbayram, A. Çakır for assistance with these field studies while at the BDARC of Uludag University. We thank the Research and Technology Department of Süleyman Demirel University for financial support. We thank the National Science Foundation (DBI #1263327) for supporting research in Turkey by students and faculty from the USA. We also thank Dr. C. Abramson and Dr. C. L. Mayack and anonymous reviewers for improvement of the manuscript. This study was conducted in partial fulfillment for the Master of Science degree of Ahmed Karahan.

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Correspondence to Ibrahim Çakmak.

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Karahan, A., Çakmak, I., Hranitz, J.M. et al. Sublethal imidacloprid effects on honey bee flower choices when foraging. Ecotoxicology 24, 2017–2025 (2015). https://doi.org/10.1007/s10646-015-1537-2

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