Abstract
Bumble bees are important pollinators whose populations have declined over recent years, raising widespread concern. One conspicuous threat to bumble bees is their unintended exposure to trace residues of systemic neonicotinoid pesticides, such as imidacloprid, which are ingested when bees forage on the nectar and pollen of treated crops. However, the demographic consequences for bumble bees of exposure to dietary neonicotinoids have yet to be fully established. To determine whether environmentally realistic levels of imidacloprid are capable of making a demographic impact on bumble bees, we exposed queenless microcolonies of worker bumble bees, Bombus terrestris, to a range of dosages of dietary imidacloprid between zero and 125 μg L−1 and examined the effects on ovary development and fecundity. Microcolonies showed a dose-dependent decline in fecundity, with environmentally realistic dosages in the range of 1 μg L−1 capable of reducing brood production by one third. In contrast, ovary development was unimpaired by dietary imidacloprid except at the highest dosage. Imidacloprid reduced feeding on both syrup and pollen but, after controlling statistically for dosage, microcolonies that consumed more syrup and pollen produced more brood. We therefore speculate that the detrimental effects of imidacloprid on fecundity emerge principally from nutrient limitation imposed by the failure of individuals to feed. Our findings raise concern about the impact of neonicotinoids on wild bumble bee populations. However, we recognize that to fully evaluate impacts on wild colonies it will be necessary to establish the effect of dietary neonicotinoids on the fecundity of bumble bee queens.
Similar content being viewed by others
References
Alaux C, Savarit F, Jaisson P, Hefetz A (2004) Does the queen win it all? Queen-worker conflict over male production in the bumblebee, Bombus terrestris. Naturwissenschaften 91:400–403
Alaux C, Boutot M, Jaisson P, Hefetz A (2007) Reproductive plasticity in bumblebee workers (Bombus terrestris)—reversion from fertility to sterility under queen influence. Behav Ecol Sociobiol 62:213–222
Allen-Wardell G et al (1998) The potential consequences of pollinator declines on the conservation of biodiversity and stability of food crop yields. Conserv Biol 12:8–17
Altaye SZ, Pirk CWW, Crewe RM, Nicolson SW (2010) Convergence of carbohydrate-biased intake targets in caged worker honeybees fed different protein sources. J Exp Biol 213:3311–3318
Amsalem E, Twele R, Francke W, Hefetz A (2009) Reproductive competition in the bumble-bee Bombus terrestris: do workers advertise sterility? Proc R Soc B 276:1295–1304
Ashman T-L et al (2009) Pollen limitation of plant reproduction: ecological and evolutionary causes and consequences. Ecology 85:2408–2421
Azevedo-Pereira HMVS, Lemos MFI, Soares AMVM (2011) Behaviour and growth of Chironomus riparius Meigen (Diptera: Chironomidae) under imidacloprid pulse and constant exposure scenarios. Water Air Soil Pollut 219:215–224
Blacquière T, Smagghe G, van Gestel CAM, Mommaerts V (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21:973–992
Boggs CL (1997) Dynamics of reproductive allocation from juvenile and adult feeding: radiotracer studies. Ecology 78:192–202
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 75:2027–2033
Bonmatin JM, Marchand PA, Charvet R, Moineau I, Bengsch ER, Colin ME (2005) Quantification of imidacloprid uptake in maize crops. J Agric Food Chem 53:5336–5341
Cameron SA, Lozier JD, Strange JP, Koch JB, Cordes N, Solter LF, Griswold TL (2011) Patterns of widespread decline in North American bumble bees. Proc Natl Acad Sci USA 108:662–667
Chauzat M-P, Faucon J-P, Martel A-C, Lachaize J, Cougoule N, Aubert M (2006) A survey of pesticide residues in pollen loads collected by honey bees in France. J Econ Entomol 99:253–262
Cresswell JE (2011) A meta-analysis of experiments testing the effects of a neonicotinoid insecticide (imidacloprid) on honey bees. Ecotoxicology 20:149–157
Cutler GC, Scott-Dupree CD (2007) Exposure to clothianidin seed-treated canola has no long-term impact on honey bees. J Econ Entomol 100:765–772
De la Rúa P, Jaffé R, Dall’Olio R, Muñoz I, Serrano J (2009) Biodiversity, conservation and current threats to European honeybees. Apidologie 40:263–284
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
Decourtye A, Devillers J, Cluzeau S, Charreton M, Pham-Delegue MH (2004) Effects of imidacloprid and deltamethrin on associative learning in honeybees under semi-field and laboratory conditions. Ecotoxicol Environ Saf 57:410–419
Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106
Elbert A, Haas M, Springer B, Thielert W, Nauen R (2008) Applied aspects of neonicotinoid uses in crop protection. Pest Manag Sci 64:1099–1105
Faucon J-P et al (2005) Experimental study on the toxicity of imidacloprid given in syrup to honey bee (Apis mellifera) colonies. Pest Manag Sci 61:111–125
Forbes VE, Calow P (1999) Is the per capita rate of increase a good measure of population-level effects in ecotoxicology? Environ Toxicol Chem 18:1544–1556
Goulson D (2003a) Conserving wild bees for crop pollination. J Food Agric Environ 1:142–144
Goulson D (2003b) Bumblebees: their behaviour and ecology. Oxford University Press, Oxford
Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumble bees. Annu Rev Entomol 53:191–208
Grier JW (1982) Ban of DDT and subsequent recovery of reproduction in bald eagles. Science 218:1232–1235
Hansard (2011) Neonicotinoid pesticides. House of Commons Hansard Debates. http://www.publications.parliament.uk/pa/cm201011/cmhansrd/cm110125/halltext/110125h0002.htm#11012550000630. Accessed 7 Jan 2012
He Y, Zhao J, Wu D, Wyckhuys KAG, Wu K (2011) Sublethal effects of imidacloprid on Bemisia tabaci (Hemiptera: Aleyrodidae) under laboratory conditions. J Econ Entomol 104:833–838
Henry M et al (2012) A common pesticide decreases foraging success and survival in honey bees. Science 336:348–350
Herbert IN, Svendsen C, Hankard PK, Spurgeon DJ (2004) Comparison of instantaneous rate of population increase and critical-effect estimates in Folsomia candida exposed to four toxicants. Ecotoxicol Environ Saf 57:175–183
Hoyle M, Hayter KE, Cresswell JE (2007) Effect of pollinator abundance on self-fertilization and gene flow: application to GM canola. Ecol Appl 17:2123–2135
Ihaka R, Gentleman R (1996) A language for data analysis and graphics. J Comput Graph Stat 5:299–314
Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant pollinator interactions. Ann Rev Ecol Syst 29:83–112
Klein A-M, Vaissière 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
Krupke CH, Hunt GJ, Eitzer BD, Andino G, Given K (2012) Multiple routes of pesticide exposure for honey bees living near agricultural fields. PLoS ONE 7:e29268
Lambin M, Armengaud C, Raymond S, Gauthier M (2001) Imidacloprid-induced facilitation of the proboscis extension reflex habituation in the honeybee. Arch Insect Biochem Physiol 48:129–134
Lopez-Vaamonde C, Koning JW, Brown RM, Jordan WC, Bourke AFG (2004) Social parasitism by male-producing reproductive workers in a eusocial insect. Nature 430:557–560
Lunn DJ, Thomas A, Best N, Spiegelhalter D (2000) WinBUGS—a Bayesian modelling framework: concepts, structure, and extensibility. Stat Comput 10:325–337
Manson JS, Thomson JD (2009) Post-ingestive effects of nectar alkaloids depend on dominance status of bumblebees. Ecol Entomol 34:421–426
Matsuda K, Buckingham SD, Kleier D, Rauh JJ, Grauso M, Sattelle DB (2001) Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci 22:573–580
Medler JT (1962) Morphometric studies on bumble bees. Ann Entomol Soc Am 55:212–218
Mommaerts V, Reynders S, Boulet J, Besard L, Sterk G, Smagghe G (2010) Risk assessment for side-effects of neonicotinoids against bumblebees with and without impairing foraging behavior. Ecotoxicology 19:207–215
Morandin LA, Winston ML (2003) Effects of novel pesticides on bumble bee (Hymenoptera: Apidae) colony health and foraging ability. Environ Entomol 32:555–563
Murphy DM, Launer AE, Ehrlich PR (1983) The role of adult feeding in egg production and population dynamics of the checkerspot butterfly Euphydryas editha. Oecologia 56:257–263
Nauen R (1995) Behaviour modifying effects of low systemic concentrations of imidacloprid on Myzus persicae with special reference to an antifeeding response. Pesticide Sci 44:145–153
O’Brien DM, Schrag DP, Martinez del Rio C (2000) Allocation to reproduction in a hawkmoth: a quantitative analysis using stable carbon isotopes. Ecology 81:2822–2831
Potts SG, Biesmeijer JC, Kremen C, Neumann P, Schweiger O, Kunin WE (2010) Global pollinator declines: trends, impacts and drivers. Trends Ecol Evol 25:345–353
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
Schmuck R, Schoning R, Stork A, Schramel O (2001) Risk posed to honeybees (Apis mellifera L. Hymenoptera) by an imidacloprid seed dressing of sunflowers. Pest Manag Sci 57:225–238
Sur R, Stork A (2003) Uptake, translocation and metabolism of imidacloprid in plants. Bull Insectol 56:35–40
Takino M, Tanaka T (2006) Determination of 44 pesticides in foodstuffs by LC/MS/MS. Agilent Technologies. http://www.chem.agilent.com/Library/applications/5989-5459EN.pdf. Accessed 21 March 2012
Tasei J-N, Lerin J, Ripault G (2000) Sub-lethal effects of imidacloprid on bumblebees, Bombus terrestris (Hymenoptera: Apidae), during a laboratory feeding test. Pest Manag Sci 56:784–788
Thompson HM, Hunt LV (1999) Extrapolating from honeybees to bumblebees in pesticide risk assessment. Ecotoxicology 8:147–166
van Engelsdorp D, Hayes J, Underwood RM, Pettis JS (2010) A survey of honey bee colony losses in the United States, fall 2008 to spring 2009. J Apic Res 49:7–14
Walthall WK, Stark JD (1997) A comparison of acute mortality and population growth rate as endpoints of toxicological effect. Ecotoxicol Environ Saf 37:45–52
Webster RP, Stoffolano JG, Prokopy RJ (1979) Long-term intake of protein and sucrose in relation to reproductive behavior of wild and laboratory cultured Rhagoletis pomonella. Ann Entomol Soc Am 72:41–46
Wheeler D (1996) The role of nourishment in oogenesis. Annu Rev Entomol 41:407–431
Whitehorn PR, O’Connor S, Wackers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumblebee colony growth and queen production. Science 336:351–352
Williams PH, Osborne JL (2009) Bumblebee vulnerability and conservation world-wide. Apidologie 40:367–387
Acknowledgments
We thank Dr. Hannah Florance for assistance with LC–MS analysis of imidacloprid and Roberta Hope for assistance with maintenance of microcolonies. Ian Laycock was supported by a studentship from the Natural Environment Research Council (NERC). Andrew Barratt was supported by a summer internship from NERC.
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical standards
The work reported here conforms to the regulatory requirements for animal experimentation in the UK and has been approved by the Biosciences Ethics Committee at the University of Exeter.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Laycock, I., Lenthall, K.M., Barratt, A.T. et al. Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology 21, 1937–1945 (2012). https://doi.org/10.1007/s10646-012-0927-y
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-012-0927-y