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Imidacloprid alters ant sociobehavioral traits at environmentally relevant concentrations

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Abstract

Much research has focused on the effects of neonicotinoids on honey bees, however, relatively few studies have investigated their effects on ants, a taxonomically-related eusocial insect of high ecological importance. This study quantified how dietary exposures to environmentally-relevant levels of a neonicotinoid insecticide (imidacloprid) affected foraging and nest building of the western harvester ant over 14 days. Using a replicated design, statistically-significant reductions in ant foraging success (50% or greater) occurred at concentrations as low as 50 ppb compared to controls. Both the number of ants entering the maze and the percentage of foraging ants able to locate food were impacted by imidacloprid exposure. Ants exposed to 50 ppb also took three times longer than controls to find food in a test maze. This concentration is among the lowest levels of imidacloprid reported to affect ants and is well within the range of concentrations found in pollen and nectar of imidacloprid-treated plants. Ant foraging success was also impaired at comparable levels as those reported for the honey bee. Although more refinement and research are needed, results from this study suggest that the western harvester ant may be useful for screening the effects of neurotoxic chemicals on their navigation and foraging, two behaviors which are critical to maintaining colony health of ants and the ecological services they provide.

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References

  • Abbott VA, Nadeau JL, Higo HA, Winston ML (2008) Lethal and sublethal effects of imidacloprid on Osmia lignaria and clothianidin on Megachile rotundata (Hymenoptera: Megachilidae). J Econ Entomol 101(3):784–96

    Article  CAS  Google Scholar 

  • Agrawal AA, Fordyce JA (2000) Induced indirect defense in a lycaenid-ant association: the regulation of a resource in a mutualism Proc R Soc Lond B 267:1857–61

    Article  CAS  Google Scholar 

  • Barbieri RF, Lester PJ, Miller AS, Ryan KG (2013) A neurotoxic pesticide changes the outcome of aggressive interactions between native and invasive ants. Proc R Soc B 367 280: 20132157.

    Article  Google Scholar 

  • Beattie AJ (1985) The evolutionary ecology of ant–plant mutualisms. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Beattie AJ, Culver DC (1981) The guild of myrmecochores in the herbaceous flora of West Virginia forests. Ecology 62:107–11

    Article  Google Scholar 

  • Bee Informed Partnership (2016) Colony loss 2014–2015: preliminary results. https://beeinformed.org/results/colony-loss-2014-2015-preliminary-results/. Accessed 12 Mar 2016

  • Bolton B (1995) A taxonomic and zoogeographical census of the extant ant taxa (Hymenoptera, Formicidae). J Nat Hist 29(4):1037–1056

    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 7(5):e37235

    Article  CAS  Google Scholar 

  • Cerdá X, Arnan X, Retana J (2013) Is competition a significant hallmark of ant (Hymenoptera: Formicidae) ecology?. Myrmecol. News 18:131–147

    Google Scholar 

  • Codling G, Naggar YA, Giesy JP, Robertson AJ (2018) Concentrations of neonicotinoid insecticides in honey, pollen and honey bees (Apis mellifera L.) in central Saskatchewan, Canada. Ecotoxicology 27:122. https://doi.org/10.1007/s10646-017-1876-2

    Article  CAS  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 

  • Currie CR, Poulsen M, Boomsma JJ, Billen J (2006) Coevolved crypts and exocrine glands support mutualistic bacteria in fungus-growing ants. Science 311:81–83

    Article  CAS  Google Scholar 

  • Davidson DW, Morton SR (1981) Myrmecochory in some plants (F. chenopodiaceae) of the Australian arid zone. Oecologia 50(3):357–366

    Article  CAS  Google Scholar 

  • Di Prisco G, Cavaliere V, Annoscia D, Varricchio P, Caprio E, Nazzi F, Gargiulo G, Pennacchio F (2013) Neonicotinoid clothianidin adversely affects insect immunity and promotes replication of a viral pathogen in honey bees Proc Natl Acad Sci USA 110:18466–18471

    Article  CAS  Google Scholar 

  • Eiri DM, Nieh JC (2012) A nicotinic acetylcholine receptor agonist affects honey bee sucrose responsiveness and decreases waggle dancing. J Exp Biol 215:2022–2029. https://doi.org/10.1242/jeb.068718

    Article  CAS  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, Grünewald B, Menzel R (2014) Neonicotinoids interfere with specific components of navigation in honeybees. PLoS One 9(3):e91364

    Article  Google Scholar 

  • Galvanho JP, Carrera MP, Moreira DDO, Erthal M, Silva CP, Samuels RI (2013) Imidacloprid inhibits behavioral defences of the leaf-cutting ant Acromyrmex subterraneus subterraneus (Hymenoptera:Formicidae). J Insect Behav 26(1):1–13

    Article  Google Scholar 

  • García MB, Antor RJ, Espadaler X (1995) Ant pollination of the palaeoendemic dioecious Borderea pyrenaica (Dioscoreaceae). Plant Syst Evol 198(1–2):17–27

    Article  Google Scholar 

  • Godfray HCJ, BlacquiŠre T, Field LM, Hails RS, Potts SG, Raine NE, Vanbergen AJ, McLean AR (2015) A restatement of recent advances in the natural science evidence base concerning neonicotinoid insecticides and insect pollinators Proc R Soc B 282:20151821

    Article  Google Scholar 

  • Goulson D, Nicholls E, Botias C, Rotheray E (2015) Bee declines driven by combined stress from parasites, pesticides and lack of flowers. Science 347 (6229): https://doi.org/10.1126/science.1255957

    Article  Google Scholar 

  • Hladik M, Vandever M, Smalling KL (2016) Exposure of native bees foraging in an agricultural landscape to current-use pesticides. Sci Total Environ 542:469–477

    Article  CAS  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants. Belknap Press of Harvard University, Cambridge, MA

    Book  Google Scholar 

  • Krischik V, Rogers M, Gupta G, Varshney A (2015) Soil-applied imidacloprid translocates to ornamental flowers and reduces survival of adult Coleomegilla maculata, Harmonia axyridis, and Hippodamia convergens lady beetles, and larval Danaus plexippus and Vanessa cardui butterflies. PLoS One 10(3):e0119133. https://doi.org/10.1371/journal

    Article  Google Scholar 

  • Lach L, Parr C, Abbott K (2010) Ant ecology. Oxford University Press, Oxford, UK

    Google Scholar 

  • LaLone CA, Villeneuve DL, Wu-Smart J, Milsk RY, Sappington K, Garber KV, Housenger J, Ankley GT (2017) Weight of evidence evaluation of a network of adverse outcome pathways linking activation of the nicotinic acetylcholine receptor in honey bees to colony death. Sci Total Environ 15:584–585. 751–775

    Google Scholar 

  • Lavelle P, Spain AV (2001) Soil ecology. Kluwer Scientific Publications, Amsterdam, p 691

    Book  Google Scholar 

  • Laycock I, Cresswell JE (2013) Repression and recuperation of brood production in Bombus terrestris bumble bees exposed to a pulse of the neonicotinoid pesticide imidacloprid. PLoS One 8(11):e79872. https://doi.org/10.1371/journal.pone.0079872

    Article  CAS  Google Scholar 

  • Laycock et al. (2012) Effects of imidacloprid, a neonicotinoid pesticide, on reproduction in worker bumble bees (Bombus terrestris). Ecotoxicology 21:1937–1945

    Article  CAS  Google Scholar 

  • Lundin O, Rundlöf M, Smith HG, Fries I, Bommarco R (2015) Neonicotinoid insecticides and their impacts on bees: a systematic review of research approaches and identification of knowledge gaps. PLoS One 10(8):e0136928

    Article  Google Scholar 

  • Mommaerts V, Sterk G, Smagghe G (2006) Bumblebees can be used in combination with juvenile hormone analogues and ecdysone agonists. Ecotoxicology 15(6):513–521

    Article  CAS  Google Scholar 

  • Moza P, Hustert K, Feicht E, Kettrup A (1998) Photolysis of imidacloprid in aqueous solution. Chemosphere 36:497–502. https://doi.org/10.1016/S0045-6535(97)00359-7

    Article  CAS  Google Scholar 

  • NAS (2007) Status of pollinators in North America. National Academy of Sciences. National Academies Press, Washington, DC

    Google Scholar 

  • Paine MD (1996) Repeated measures designs. Environ Toxicol Chem 15:1439–1441. https://doi.org/10.1002/etc.5620150901

    Article  CAS  Google Scholar 

  • Penn HJ, Dale AM (2016) Imidacloprid seed treatments affect individual ant behavior and community structure but not egg predation, pest abundance or soybean yield. Pest Manage Sci 73:1625–1632

    Article  Google Scholar 

  • Pisa LW et al. (2015) Effects of neonicotinoids and fipronil on non-target invertebrates. Environ Sci Pollut Res 22:68–102

    Article  CAS  Google Scholar 

  • Rust MK, Reierson DA, Klotz JH (2004) Delayed toxicity as a critical factor in the efficacy of aqueous baits for controlling Argentine ants (Hymenoptera: Formicidae). J Econ Entomol 97:1017–1024

    Article  CAS  Google Scholar 

  • Sanders D, Frank van Veen FJ (2011) Ecosystem engineering and predation: the multi-trophic impact of two ant species. J Anim Ecol 80:569–576

    Article  Google Scholar 

  • Sánchez-Bayo F, Yamashita H, Osaka R, Yoneda M, Goka K (2007) Ecological effects of imidacloprid on arthropod communities in and around a vegetable crop. J Environ Sci Health Part B 42(3):279–286. https://doi.org/10.1080/03601230701229239

    Article  CAS  Google Scholar 

  • Schneider CW, Tautz J, Grünewald B, Fuchs S (2012) RFID tracking of sublethal effects of two neonicotinoid insecticides on the foraging behavior of Apis mellifera. PLoS One 7(1):e30023

    Article  CAS  Google Scholar 

  • Stoner KA, Eitzer BD (2012) Movement of soil-applied imidacloprid and thiamethoxam into nectar and pollen of squash (Cucurbita pepo). PLoS One 7(6):e39114

    Article  CAS  Google Scholar 

  • Tan K, Chen W, Dong S, Liu X, Wang Y, Nieh JC (2014) Imidacloprid alters foraging and decreases bee avoidance of predators. PLoS One 9(7):e102725

    Article  Google Scholar 

  • Tattar TA, Dotson JA, Ruizzo MS, Steward VB (2008) Translocation of imidacloprid in three tree species when trunk- and soil-injected. J Arboric 24(1):54–56

    Google Scholar 

  • Thiel S, Kölhler H (2016) A sublethal imidacloprid concentration alters foraging and competition behaviour of ants. Ecotoxicology 5:814–823

    Article  Google Scholar 

  • Tollerup K, Rust M, Dorschner K, Phillips P, Klotz J (2004) Low-toxicity baits control ants in citrus orchards and grape vineyards. Calif Agr 58(4):213–217

    Article  Google Scholar 

  • Tsvetkov N, Samson-Robert O, Sood K, Patel HS, Malena DA, Gajiwala PH, Maciukiewicz P, Fournier V, Zayed A (2017) Chronic exposure to neonicotinoids reduced honey bee health near corn crops. Science 356:1395–1397. https://doi.org/10.1126/science.aam7470

    Article  CAS  Google Scholar 

  • USDA (2016) Honey bee colonies. National Agricultural Statistics Service, Agricultural Statistics Board, United States Department of Agriculture. 17. https://www.usda.gov/nass/PUBS/TODAYRPT/hcny0516.pdf. Accessed 19 Nov 2017

  • USEPA (2016) Preliminary pollinator risk assessment for imidacloprid. EPA-HQ-OPP-2008-0844-0140. U.S. Environmental Protection Agency, Washington, DC. https://www.epa.gov/pollinator-protection/schedule-review-neonicotinoid-pesticides

    Google Scholar 

  • USEPA (2017) Preliminary bee risk assessment to support the registration review of clothianidin and thiamethoxam. EPA-HQ-OPP-2011-0865-0173. U.S. Environmental Protection Agency, Washington, DC. https://www.epa.gov/pollinator-protection/schedule-review-neonicotinoid-pesticides

    Google Scholar 

  • Wagner D, Johnes JB, Gordon DM (2004) Development of harvester ant colonies alters soil chemistry. Soil Bio Biochem 36:797–804

    Article  CAS  Google Scholar 

  • Wang L, Zeng L, Chen J (2015) Impact of imidacloprid on new queens of imported fire ants, Solenopsis invicta. Sci Rep 5:17938. https://doi.org/10.1038/srep17938

    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(6079):351–352. https://doi.org/10.1126/science.1215025

    Article  CAS  Google Scholar 

  • Williamson SM, Willis SJ, Wright GA (2014) Exposure to neonicotinoids influences the motor function of adult worker honeybees. Ecotoxicology 23:1409–1418. https://doi.org/10.1007/s10646-014-1283-x

    Article  CAS  Google Scholar 

  • Wood TJ, Goulson D (2017) The environmental risks of neonicotinoid pesticides: a review of evidence post 2013. Environ Sci Pollut Res 24:17285–17325. https://doi.org/10.1007/s11356-017-9240-x

    Article  CAS  Google Scholar 

  • Woodcock BA, Bullock JM, Shore RF, Heard MS, Pereira MG, Redhead J, Ridding L, Dean H, Sleep D, Henrys P, Peyton J, Hulmes S, Hulmes L, Sárospataki M, Saure C, Edwards M, Genersch E, Knäbe S, Pywell RF (2017) Country-specific effects of neonicotinoid pesticides on honey bees and wild bees. Science 356:1393–1395. https://doi.org/10.1126/science.aaa1190

    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(6):1743–1748

    Article  CAS  Google Scholar 

  • Zaiontz, C (2017) Real statistics for excel, release 5.3. www.real-statistics.com

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Acknowledgements

I wish to thank the judges at the 2017 Intel International Science and Engineering Fair (ISEF) and the Anne Arundel County Regional Science and Engineering Fair for recognizing this research with various awards and encouraging me to publish my findings. I thank the Board of Education of Anne Arundel County for financially supporting my travel to ISEF and poster production. I thank Keith Sappington, my science mentor for his guidance and support, particularly on the statistical analysis and also two anonymous reviewers for their valuable comments. Lastly, I thank Dr. Edward O. Wilson, whose book “Letters to a Young Scientist” inspired me to consider using this amazing species of harvester ants to assess pesticide safety.

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  1. South River High School, 201 E. Central Avenue, Edgewater, MD, USA

    James D. Sappington

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Sappington, J.D. Imidacloprid alters ant sociobehavioral traits at environmentally relevant concentrations. Ecotoxicology 27, 1179–1187 (2018). https://doi.org/10.1007/s10646-018-1976-7

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