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Effects of dietary lambda-cyhalothrin exposure on bumblebee survival, reproduction, and foraging behavior in laboratory and greenhouse

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Abstract

Bumblebees of Bombus terrestris are indispensible pollinators for ecosystems and for various agricultural crops. Unfortunately, bumblebees are challenged by various stress factors including insecticide applications. Today sublethal effects of various insecticides need to be thoroughly investigated to allow their combined use with pollinators and other beneficial organisms. In this study, we used lambda-cyhalothrin as a model pyrethroid insecticide and investigated lethal and sublethal effects by different dilutions, ranging from 1/10 to 1/100 of its maximum field recommended dosage (MFRC, 37.5 ppm), with the use of a chronic toxicity tests in the laboratory and in flight cages in the greenhouse. In the laboratory, small microcolonies with five bumblebee workers with one being pseudo-queen were used, while in the greenhouse we used queen-right mini-hives where the bumblebees need to fly for pyrethroid-contaminated food. We observed strong sublethal effects in the laboratory with treatments of 1/10 and 1/20 of the MFRC: the nest reproduction was reduced by 49 and 32 %, respectively, and the sugar water consumption by 36 %. With free-flying bumblebees, the toxic effects at 1/10 of the MFRC were more pronounced. A mortality of 88 ± 8 % was observed after only 2 weeks, being twice the mortality in the laboratory microcolonies test (43 ± 11 %). Besides, it should be mentioned that in the greenhouse experiment all queens were dead and most of the workers showed signs of incoordination and convulsion and gradually became apathetic. In conclusion, our results demonstrated the pyrethroid lambda-cyhalothrin with a range of lethal and sublethal effects, both crucial for the development and survival of the B. terrestris colonies. Moreover, this study supports the demand to test insecticide compounds on their safety, especially when the bees have to perform complex tasks such as foraging for their food.

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References

  • Aufauvre J, Biron DG, Vidau C, Fontbonne R, Roudel M, Diogon M (2012) Parasite-insecticide interactions: a case study of Nosema ceranae and fipronil synergy on honeybee. Sci Rep 2:326

    Article  PubMed Central  PubMed  Google Scholar 

  • Baron GL, Raine NE, Brown MJF (2014) Impact of chronic exposure to a pyrethroid pesticide on bumblebees and interactions with a trypanosome parasite. J Appl Ecol 51(2):460–469

    Article  CAS  Google Scholar 

  • Besard L, Mommaerts V, Abdu-Alla G, Smagghe G (2011) Laboratory assessment of lethal and sublethal side-effects supports a more benign profile of spinetoram compared to spinosad in the bumblebee Bombus terrestris. Pest Manag Sci 67(5):541–547

    Article  CAS  PubMed  Google Scholar 

  • Biondi A, Mommaerts V, Smagghe G, Viñuela E, Zappala L, Desneux N (2012) The non-target impacts of spinosyns on beneficial arthropods. Pest Manag Sci 68:1523–1536

    Article  CAS  PubMed  Google Scholar 

  • Biondi A, Zappala L, Desneux N, Aparo A, Siscaro G, Rapisarda C, Martin T, Tropea Garzia G (2015) Potential toxicity of α-cypermethrin-treated nets on Tuta absoluta (Lepidoptera: Gelechiidae). J Econ Entomol 108(3):1–7

    Article  Google Scholar 

  • Burr S, Ray DE (2004) Structure-activity and interaction effects of 14 different pyrethroids on voltage-gated chloride ion channels. Toxicol Sci 77(2):341–346

    Article  CAS  PubMed  Google Scholar 

  • Decourtye A, Pham-Delègue MH (2002) The proboscis extension response: assessing the sublethal effects of pesticides on the honey bee. In: Devillers J, Pham-Delègue MH (eds) Honey bees: estimating the environmental impact of chemicals. Taylor and Francis, London, pp 67–84

    Google Scholar 

  • Decourtye A, Henry M, Desneux N (2013) Environment: overhaul pesticide testing on bees. Nature 497(7448):188

    Article  CAS  PubMed  Google Scholar 

  • Desneux N, Pham-Delègue MH, Kaiser L (2004) Effects of sub-lethal and lethal doses of lambda-cyhalothrin on oviposition experience and host-searching behaviour of a parasitic wasp, Aphidius ervi. Pest Manag Sci 60(4):381–389

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Devillers J, Pham-Delègue MH (2002) Honey Bees: Estimating the environmental impact of chemicals. Taylor & Francis, London

    Book  Google Scholar 

  • Du Y, Nomura Y, Luo N, Liu Z, Lee JE, Khambay B, Dong K (2009) Molecular determinants on the insect sodium channel for the specific action of type II pyrethroid insecticides. Toxicol Appl Pharmacol 234(2):266–272

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • EFSA (2013) Guidance Document on the risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA J 11(7):3295

    Google Scholar 

  • EPPO (2001) Standards PP1/170. Test methods for evaluating the side effects of plant protection products on honeybees. Bull OEPP/EPPO 31:323–330

    Article  Google Scholar 

  • Fishel FM (2014) Pesticide toxicity profile: synthetic pyrethroid pesticides (1–3), IFAS extension, University of Florida

  • Garthwaite DG, Barker I, Parrish G, Smith C, Chippindale C, Pietravalle S (2010) Pesticide usage survey report 235: arable crops in the United Kingdom, York

  • Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491(7422):105–108

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Goulson D (2002) Can alloethism in workers of the bumblebee, Bombus terrestris, be explained in terms of foraging efficiency? Anim Behav 64(1):123–130

    Article  Google Scholar 

  • Goulson D (2010) Bumblebees behaviour, ecology and conservation. Oxford University Press, Oxford

    Google Scholar 

  • Hatfield R, Jepsen S, Mader E, Hoffman S, Sheperd M (2012) Conserving bumble bees. The Xerxes Society for Invertebrate Conservation, Portland

    Google Scholar 

  • He L, Troiano J, Wang A, Goh K (2008) Environmental chemistry, ecotoxicity, and fate of lambda-cyhalotrin. Rev Environ Contam Toxicol 195:71–91

    CAS  PubMed  Google Scholar 

  • He Y, Zhao J, Zheng Y, Weng Q, Biondi A, Desneux N, Wu K (2013) Assesment of potential sublethal effects of various insecticides on key biological traits of the tobacco whitefly, Bemisia tabaci. Int J Biol Sci 9(3):246–255

    Article  PubMed Central  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • ICPBR (2000) Guideline for the efficacity evaluation of plant protection products. In: Pélissier C, Belzunces LP (eds) Hazards of pesticides to bees. IOBC wprs Bulletin, Avignon, pp 51–55

    Google Scholar 

  • Kremen C, Williams NM, Aizen M, Gemmill-Herren B, LeBuhn G, Minckley R, Ricketts TH (2007) Pollination and other ecosystem services produced by mobile organisms: a conceptual framework for the effects of land-use change. Ecol Lett 10(4):299–314

    Article  PubMed  Google Scholar 

  • Mommaerts V, Smagghe G (2010) Side-effects of pesticides on the pollinator Bombus: an overview. In: Stoytcheva M (ed) Pesticides in the modern world: pests control andpesticides exposure and toxicity assessment. InTech, Rijeka, pp 507–552

    Google Scholar 

  • Mommaerts V, Sterk G, Smagghe G (2006) Hazards and uptake of chitin synthesis inhibitors in bumblebees Bombus terrestris. Pest Manag Sci 62:752–758

    Article  CAS  PubMed  Google Scholar 

  • 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(1):207–215

    Article  CAS  PubMed  Google Scholar 

  • Müller CB, Schmid-Hempel P (1992) Correlates of reproductive success among field colonies of Bombus lucorum: the importance of growth and parasites. Ecol Entomol 17(4):343–353

    Article  Google Scholar 

  • Osborne JL (2012) Bumblebees and pesticides. Nature 491(44):43–45

    Article  CAS  PubMed  Google Scholar 

  • Palmquist K, Salatas J, Fairbrother A (2012) Pyrethroid insecticides: use, environmental fate, and ecotoxicology. In: Perveen F (ed) Insecticides - advances in integrated pest management. InTech, pp 251–278

  • Pansa M, Blandino M, Ingegno B, Ferrari E, Reyneri A, Tavella L (2015) Toxicity and persistence of three pyrethroids for the control of cereal bugs on common wheat. J Pest Sci 88:201–208

    Article  Google Scholar 

  • 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):345–353

    Article  PubMed  Google Scholar 

  • Schneider CW, Tautz J, Grunewald B, Fuchs S (2012) RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLoS One 7:e30023

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Smagghe G, Deknopper J, Meeus I, Mommaerts V (2013) Dietary chlorantraniliprole suppresses reproduction in worker bumblebees. Pest Manag Sci 69(7):787–791

    Article  CAS  PubMed  Google Scholar 

  • Sutcliffe GH, Plowright RC (1988) The effects of food-supply on adult size in the bumble bee Bombus terricola Kirby (Hymenoptera, Apidae). Can Entomol 120:1051–1058

    Article  Google Scholar 

  • Thompson HM (2003) Behavioural effects of pesticides in bees: their potential for use in risk assessment. Ecotoxicology 12:317–330

    Article  CAS  PubMed  Google Scholar 

  • Thompson H, Wilkins S (2003) Assessment of the synergy and repellency of pyrethroid/fungicide mixtures. Bull Insectol 56(1):131–134

    Google Scholar 

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

    Article  Google Scholar 

  • Wolf S, Moritz RFA (2008) Foraging distance in Bombus terrestris L. (Hymenoptera : Apidae). Apidologie 39:419–427

    Article  Google Scholar 

Download references

Acknowledgments

This research was supported by the Special Research Fund of Ghent University (BOF-UGent), the Fund for Scientific Research-Flanders (FWO, Brussels), and the Institute for Agricultural and Fisheries Research (ILVO).

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Authors and Affiliations

  1. Department of Crop Protection, Faculty of Bioscience Engineering, Ghent University, Ghent, Belgium

    Bob Ceuppens, Maxime Eeraerts & Guy Smagghe

  2. Plant Sciences Unit, Institute for Agricultural and Fisheries Research (ILVO), Melle, Belgium

    Bob Ceuppens, Tim Vleugels, Gerda Cnops & Isabel Roldan-Ruiz

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  1. Bob Ceuppens
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  2. Maxime Eeraerts
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  3. Tim Vleugels
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  4. Gerda Cnops
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  5. Isabel Roldan-Ruiz
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  6. Guy Smagghe
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Correspondence to Guy Smagghe.

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Communicated by A. Biondi.

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Ceuppens, B., Eeraerts, M., Vleugels, T. et al. Effects of dietary lambda-cyhalothrin exposure on bumblebee survival, reproduction, and foraging behavior in laboratory and greenhouse. J Pest Sci 88, 777–783 (2015). https://doi.org/10.1007/s10340-015-0676-9

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  • DOI: https://doi.org/10.1007/s10340-015-0676-9

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