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Lethal and sublethal effects of azadirachtin on the bumblebee Bombus terrestris (Hymenoptera: Apidae)

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Abstract

Azadirachtin is a biorational insecticide commonly reported as selective to a range of beneficial insects. Nonetheless, only few studies have been carried out with pollinators, usually emphasizing the honeybee Apis mellifera and neglecting other important pollinator species such as the bumblebee Bombus terrestris. Here, lethal and sublethal effects of azadirachtin were studied on B. terrestris via oral exposure in the laboratory to bring out the potential risks of the compound to this important pollinator. The compound was tested at different concentrations above and below the maximum concentration that is used in the field (32 mg L−1). As most important results, azadirachtin repelled bumblebee workers in a concentration-dependent manner. The median repellence concentration (RC50) was estimated as 504 mg L−1. Microcolonies chronically exposed to azadirachtin via treated sugar water during 11 weeks in the laboratory exhibited a high mortality ranging from 32 to 100 % with a range of concentrations between 3.2 and 320 mg L−1. Moreover, no reproduction was scored when concentrations were higher than 3.2 mg L−1. At 3.2 mg L−1, azadirachtin significantly inhibited the egg-laying and, consequently, the production of drones during 6 weeks. Ovarian length decreased with the increase of the azadirachtin concentration. When azadirachtin was tested under an experimental setup in the laboratory where bumblebees need to forage for food, the sublethal effects were stronger as the numbers of drones were reduced already with a concentration of 0.64 mg L−1. Besides, a negative correlation was found between the body mass of male offspring and azadirachtin concentration. In conclusion, our results as performed in the laboratory demonstrated that azadirachtin can affect B. terrestris with a range of sublethal effects. Taking into account that sublethal effects are as important as lethal effects for the development and survival of the colonies of B. terrestris, this study confirms the need to test compounds on their safety, especially when they have to perform complex tasks such as foraging. The latter agrees with the recent European Food Safety Authority guidelines to assess ‘potentially deleterious’ compounds for sublethal effects on behavior.

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References

  • Allison PD (1998) Survival analysis using SAS: a practical guide. SAS Institute Inc., Cary

    Google Scholar 

  • Alves JE (2010) Toxicidade do nim (Azadirachta indica A. Juss.: Meliaceae) para Apis mellifera e sua importância apícola na Caatinga e Mata Litorânea cearense. Thesis, Universidade Federal do Ceará

  • Amin MR, Bussière LF, Goulson D (2012) Effects of male age and size on mating success in the bumblebee Bombus terrestris. Insect Behav 25:362–374

    Article  Google Scholar 

  • Arno J, Gabarra R (2011) Side effects of selected insecticides on the Tuta absoluta (Lepidoptera: Gelechiidae) predators Macrolophus pygmaeus and Nesidiocoris tenuis (Hemiptera: Miridae). J Pest Sci 84:513–520

    Article  Google Scholar 

  • Barnby MA, Klocke JA (1990) Effects of azadirachtin on levels of ecdysteroids and prothoracicotropic hormone-like activity in Heliothis virescens (Fabr.) larvae. J Insect Physiol 36(125):131

    Google Scholar 

  • Blacquiere 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

    Article  CAS  Google Scholar 

  • Blaney WM, Simmonds MSJ, Ley WV, Anderson JC, Toogood PL (1990) Antifeedant effects of azadirachtin and structurally related compounds on lepidopterous larvae. Entomol Exp Appl 55:149–160

    Article  CAS  Google Scholar 

  • Bloch G, Borst DW, Huang Z-Y, Robinson GE, Cnaani J, Hefetz A (2000a) Juvenile hormone titers, juvenile hormone biosynthesis, ovarian development and social environment in Bombus terrestris. J Insect Physiol 46:47–57

    Article  CAS  Google Scholar 

  • Bloch G, Hefetz A, Hartfelder K (2000b) Ecdysteroid titer, ovary status, and dominance in adult worker and queen bumble bees (Bombus terrestris). J Insect Physiol 46:1033–1040

    Article  CAS  Google Scholar 

  • Boeke SJ, Boersma MG, Alink GM, van Loona JJA, van Huis A, Dicke M, Rietjens IMCM (2004) Safety evaluation of neem (Azadirachta indica) derived pesticides. J Ethnopharmacol 94:25–41

    Article  CAS  Google Scholar 

  • Brittain C, Potts SG (2011) The potential impacts of insecticides on the life-history traits of bees and the consequences for pollination. Basic Appl Ecol 12:321–331

    Article  Google Scholar 

  • Brown MJF, Paxton RJ (2009) The conservation of bees: a global perspective. Apidologie 40:410–416

    Article  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 

  • Cantrell CL, Dayan FE, Duke SO (2012) Natural products as sources for new pesticides. J Natural Prod 75:1231–1242

    Article  CAS  Google Scholar 

  • Cassida JE, Quistad GB (2004) Why insecticides are more toxic to insects than people: the unique toxicology of insects. J Pestic Sci 29:81–86

    Article  Google Scholar 

  • Chen Y, Ruberson JR (2008) Starvation effects on larval development of beet armyworm (Lepidoptera: Noctuidae). J Entomol Sci 43:247–253

    Google Scholar 

  • Cooper J, Dobson H (2007) The benefits of pesticides to mankind and the environment. Crop Prot 26:1337–1348

    Article  CAS  Google Scholar 

  • Decourtye A, Armengaud C, Renou M, Devillers J, Cluzeau S, Gauthier M, Pham-Delegue MH (2004) Imidacloprid impairs memory and brain metabolism in the honeybee (Apis mellifera L.). Pestic Biochem Physiol 78:83–92

    Article  CAS  Google Scholar 

  • Dorn A, Rademacher JM, Sehn E (1986) Effects of azadirachtin on the moulting cycle, endocrine system and ovaries in last-instar larvae of the milkweed bug, Oncopeltus fasciatus. J Insect Physiol 32:231–238

    Article  CAS  Google Scholar 

  • European Food Safety Authority (2012) Scientific opinion on the science behind the development of a risk assessment of plant protection products on bees (Apis mellifera, Bombus spp. and solitary bees). EFSA J 10:2668

  • Freitas BM, Imperatriz-Fonseca VL, Medina LM, Kleinert ADP, Galetto L, Nates-Parra G, Quezada-Euan JJG (2009) Diversity, threats and conservation of native bees in the Neotropics. Apidologie 40:332–346

    Article  Google Scholar 

  • Gallai N, Salles JM, Settele J, Vaissiere BE (2009) Economic valuation of the vulnerability of world agriculture confronted with pollinator decline. Ecol Econ 68:810–821

    Article  Google Scholar 

  • Gels JA, Held DW, Potter DA (2002) Hazards of insecticides to the bumble bees Bombus impatiens (Hymenoptera: Apidae) foraging on flowering white clover in turf. J Econ Entomol 95:722–728

    Article  CAS  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 U119

    Article  CAS  Google Scholar 

  • Goulson D, Lye GC, Darvill B (2008) Decline and conservation of bumble bees. Annu Rev Entomol 53:191–208

    Article  CAS  Google Scholar 

  • Isman MB (2006) Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu Rev Entomol 51:45–66

    Article  CAS  Google Scholar 

  • Jeschke P, Nauen R (2008) Neonicotinoids—from zero to hero in insecticide chemistry. Pest Manag Sci 64:1084–1098

    Article  CAS  Google Scholar 

  • Johnson RM, Dahlgren L, Siegfried BD, Ellis MD (2013) Acaricide, fungicide and drug interactions in honey bees (Apis mellifera). PLoS ONE 8:e54092

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

  • Kovacova J, Hrbek V, Kloutvorova J, Kocourek V, Drabova L, Hajslova J (2013) Assessment of pesticide residues in strawberries grown under various treatment regimes. Food Addit Contam Part A Chem Anal Control Expo Risk Assess 30:2123–2135

    Article  CAS  Google Scholar 

  • Kumar P, Poehling H-M (2006) Persistence of soil and foliar azadirachtin treatments to control sweetpotato whitefly Bemisia tabaci Gennadius (Homoptera: Aleyrodidae) on tomatoes under controlled (laboratory) and field (netted greenhouse) conditions in the humid tropics. J Pest Sci 79:189–199

    Article  Google Scholar 

  • Lamberth C, Jeanmart S, Luksch T, Plant A (2013) Current challenges and trends in the discovery of agrochemicals. Science 341:742–746

    Article  Google Scholar 

  • Lowery DT, Bellerose S, Smirle MJ, Vincent C, Pilon JG (1996) Effect of neem on the growth and development of the obliquebanded leafroller, Choristoneura rosaceana. Entomol Exp Appl 79:203–209

    Article  CAS  Google Scholar 

  • Lucantoni L, Giusti F, Cristofaro M, Pasqualini L, Esposito F, Lupetti P, Habluetzel A (2006) Effects of a neem extract on blood feeding, oviposition and oocyte ultrastructure in Anopheles stephensi Liston (Diptera: Culicidae). Tissue Cell 38:361–371

    Article  CAS  Google Scholar 

  • Melathopoulos AP, Winston ML, Whittington R, Smith T, Lindberg C, Mukai A, Moore M (2000) Comparative laboratory toxicity of neem pesticides to honey bees (Hymenoptera: Apidae), their mite parasites Varroa jacobsoni (Acari: Varroidae) and Acarapis woodi (Acari: Tarsonemidae), and brood pathogens Paenibacillus larvae and Ascophaera apis. J Econ Entomol 93:199–209

    Article  CAS  Google Scholar 

  • Metcalf RL (1980) Changing role of insecticides in crop protection. Annu Rev Entomol 25:219–255

    Article  CAS  Google Scholar 

  • Michener CD (1974) The social behaviour of the bees. Harvard University Press, Cambridge

    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 19:207–215

    Article  CAS  Google Scholar 

  • Mordue (Luntz) AJ, Nisbet AJ (2000) Azadirachtin from the neem tree Azadirachta indica: its action against insects. An Soc Entomol Brasil 29:615–632

  • Mordue (Luntz) AJ, Simmonds MSJ, Ley SV, Blaney WM, Mordue W, Nasiruddin M, Nisbet AJ (1998) Actions of azadirachtin, a plant allelochemical, against insects. Pest Sci 54:277–284

  • Morgan ED (2009) Azadirachtin, a scientific gold mine. Bioorgan Med Chem 17:4096–4105

    Article  CAS  Google Scholar 

  • Munyiri FN, Asano W, Shintani Y, Ishikawa Y (2003) Threshold weight for starvation-triggered metamorphosis in the yellow-spotted longicorn beetle, Psacothea hilaris (Coleoptera: Cerambycidae). Appl Entomol Zool 38:509–515

    Article  Google Scholar 

  • Nathan SS, Choi MY, Paik CH, Seo HY, Kim JD, Kang SM (2007) The toxic effects of neem extract and azadirachtin on the brown planthopper, Nilaparvata lugens (Stal) (BPH) (Homoptera: Delphacidae). Chemosphere 67:80–88

    Article  CAS  Google Scholar 

  • Naumann K, Isman MB (1996) Toxicity of a neem (Azadirachta indica A. Juss) insecticide to larval honey bees. Am Bee J 136:518–520

    Google Scholar 

  • Salehzadeh A, Jabbar A, Jennens L, Ley SV, Annadurai RS, Adams R, Strang RH (2002) The effects of phytochemical pesticides on the growth of cultured invertebrate and vertebrate cells. Pest Manag Sci 58:268–276

    Article  CAS  Google Scholar 

  • Sayah F (2002) Ultrastructural changes in the corpus allatum after azadirachtin and 20-hydroxyecdysone treatment in adult females of Labidura riparia (Dermaptera). Tissue Cell 34:53–62

    Article  CAS  Google Scholar 

  • Sayah F, Fayet C, Idaomar M, Karlinsky A (1996) Effects of azadirachtin on vitellogenesis of Labidura riparia (Insecta: Dermaptera). Tissue Cell 28:741–749

    Article  CAS  Google Scholar 

  • Sayah F, Idaomar M, Soranzo L, Karlinsky A (1998) Endocrine and neuroendocrine effects of azadirachtin in adult females of the earwig Labidura riparia. Tissue Cell 30:86–94

    Article  CAS  Google Scholar 

  • Schluns H, Schluns EA, van Praagh J, Moritz RFA (2003) Sperm numbers in drone honeybees (Apis mellifera) depend on body size. Apidologie 34:577–584

    Article  Google Scholar 

  • Simmonds MSJ, Blaney WM, Ley SV, Anderson JC, Banteli R, Denholm AA, Green PCW, Grossman RB, Gutteridge C, Jennens L, Smith SC, Toogood PL, Wood A (1995) Behavioral and neurophysiological responses of Spodoptera littoralis to azadirachtin and a range of synthetic analogs. Entomol Exp Appl 77:69–80

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Thoeming G, Poehling HM (2006) Soil application of different neem products to control Ceratothripoides claratris (Thysanoptera: Thripidae) on tomatoes grown under protected cultivation in the humid tropics (Thailand). Int J Pest Manage 52:239–248

    Article  CAS  Google Scholar 

  • Thompson DG, Kreutzweiser DP, Staznik B, Chartrand D, Capell S (2002) Fate and persistence of azadirachtin a following applications to mesocosms in a small forest lake. Bull Environ Contam Toxicol 69:250–256

    Article  CAS  Google Scholar 

  • Thompson HM, Wilkins S, Battersby AH, Waite RJ, Wilkinson D (2005) The effects of four insect growth-regulating (IGR) insecticides on honeybee (Apis mellifera L.) colony development, queen rearing and drone sperm production. Ecotoxicology 14:757–769

    Article  CAS  Google Scholar 

  • Timmins WA, Reynolds SF (1992) Azadirachtin inhibits secretion of trypsin in midgut of Manduca sexta caterpillars: reduced growth due to impaired protein digestion. Entomol Exp Appl 63:47–54

    Article  CAS  Google Scholar 

  • Trumm P, Dorn A (2000) Effects of azadirachtin on the regulation of midgut peristalsis by the stomatogastric nervous system in Locusta migratoria. Phytoparasitica 28:7–26

    Article  CAS  Google Scholar 

  • van Doom A, Heringa J (1986) The ontogeny of a dominance hierarchy in colonies of the bumble bee Bombus terrestris (Hymenoptera: Apidae). Insect Soc 33:3–25

    Article  Google Scholar 

  • van Honk CGJ, Roseler PF, Hoogeveen JC (1981) Factors influencing the egg laying of workers in a captive colony Bombus terrestris. Behav Ecol Sociobiol 9:9–14

    Article  Google Scholar 

  • vanEngelsdorp D, Meixner MD (2010) A historical review of managed bee populations in Europe and United States and the factors that may affect them. J Invertebr Pathol 103:S80–S95

    Article  Google Scholar 

  • Velthuis HHW, 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 

  • Villaverde JJ, Sevilla-Moran B, Sandin-Espana P, Lopez-Goti C, Alonso-Prados JL (2014) Biopesticides in the framework of the European Pesticide Regulation (EC) No. 1107/2009. Pest Manag Sci 70:2–5

    Article  CAS  Google Scholar 

  • Wu JY, Anelli CM, Sheppard WS (2011) Sub-lethal effects of pesticide residues in brood comb on worker honey bee (Apis mellifera) development and longevity. PLoS ONE 6:e14720

    Article  CAS  Google Scholar 

  • Yang EC, Chuang YC, Chen YL, Chang LH (2008) Abnormal foraging behavior induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera: Apidae). J Econ Entomol 101:1743–1748

    Article  CAS  Google Scholar 

  • Zanuncio JC, Molina-Rugama AJ, Santos GP, Ramalho FD (2002) Effect of body weight on fecundity and longevity of the stinkbug predator Podisus rostralis. Pesqui Agropecu Bras 37:1225–1230

    Article  Google Scholar 

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Acknowledgments

We thank the CAPES Foundation (Brazilian Ministry of Education) for the scholarship and financial support to W.F. Barbosa. This project was also support by the Research Council of Ghent University (BOF-UGent) and the Flemish government agency for Innovation by Science and Technology (IWT, Belgium).

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Correspondence to Guy Smagghe.

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Barbosa, W.F., De Meyer, L., Guedes, R.N.C. et al. Lethal and sublethal effects of azadirachtin on the bumblebee Bombus terrestris (Hymenoptera: Apidae). Ecotoxicology 24, 130–142 (2015). https://doi.org/10.1007/s10646-014-1365-9

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