Ecotoxicology

, Volume 25, Issue 4, pp 814–823 | Cite as

A sublethal imidacloprid concentration alters foraging and competition behaviour of ants

Article

Abstract

Neonicotinoid pesticides, such as the widely used compound imidacloprid, are suspected to impair cognitive capacity, behaviour, and fitness of a number of non-target species. We tested whether sublethal imidacloprid concentrations alter the foraging and aggression behaviour of two European ant species. Even though the nestmate-recruitment of Lasius niger was not affected by pesticide exposure, these ants required more time to become active and the number of foraging workers was lower than in sub-colonies not exposed to imidacloprid. In interspecific confrontations, imidacloprid increased the aggressiveness of a usually subordinate species (Lasius flavus) enormously (3.7-fold increase in average number of aggressive encounters), whereas they did not affect a subdominant species (L. niger) that severely (1.2-fold increase in average number of aggressive encounters). The high frequency of aggressive encounters of L. flavus vs. non-exposed L. niger workers, reduced their survival probability significantly down to 60 %. The observed behavioural alterations of the two ant species have the potential to impair their viability and co-occurrence with behaviourally dominate species due to a decreased exploitative competition and a reduced chance to locate and use resources before competitors. As competition is considered key in structuring ant communities, changes in aggressiveness are likely to alter established dominance hierarchies and thereby the dynamic and structure of ant communities.

Keywords

Neonicotinoid Neurotoxicity Interspecific confrontation Non-target species Sublethal effects 

Abbreviations

AI

Active ingredient

ANOVA

Analysis of variance

b

Standard error of log

Coxph

Cox proportional hazard regression model

df

Degrees of freedom

GLM

Generalized linear model

LF

Lasius flavus

LMM

Linear mixed model

LN

Lasius niger

noAI

No active ingredient

SE

Standard error of the mean

z

Log-likelihood

References

  1. Anon (2006) Draft assessment Report (DAR)—public version—Initial risk assessment provided by the rapporteur Member State Germany for the existing active substance imidacloprid. Volume 3, Annex B, B.8, February 2006Google Scholar
  2. Arnan X, Gaucherel C, Andersen AN (2011) Dominance and species co-occurrence in highly diverse ant communities: a test of the interstitial hypothesis and discovery of a competition cascade. Oecologia 166:783–794CrossRefGoogle Scholar
  3. Arnan X, Cerdá X, Retana J (2012) Distinctive life traits and distribution along environmental gradients of dominant and subordinate Mediterranean ant species. Oecologia 170:489–500CrossRefGoogle Scholar
  4. 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. doi:10.1098/rspb.2013.2157 Google Scholar
  5. Blacquiere T, Smagghe G, Van Gestel CAM, Mommaerts V (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21:973–992CrossRefGoogle Scholar
  6. Bonmatin JM, Moineau I, Charvet R, Collin ME, Fleche C, Bengsch ER (2005) Behavior of imidacloprid in fields. Toxicity for honey bees. In: Lichtfourse E, Schwarzbauer J, Robert D (eds) Environmental chemistry: green chemistry and pollutants in ecosystems. Springer, New York, pp 482–494Google Scholar
  7. Bortolotti L, Montanari R, Marcelino J, Medrzycki P, Maini S, Porrini C (2003) Effect of sublethal imidacloprid doses on the homing rate and foraging activity of honey bees. Bull Insectol 56:63–67Google Scholar
  8. Cerdá X, Arnan X, Retana J (2013) Is competition a significant hallmark of ant (Hymenoptera: Formicidae) ecology? Myrmecol News 18:131–147Google Scholar
  9. Chen Z, Qu Y, Xiao D, Song L, Zhang S, Gao X, Desneux N, Song D (2015) Lethal and social-mediated effects of ten pesticide on the subterranean termite Reticulitermes speratus. J Pest Sci 88:741–751CrossRefGoogle Scholar
  10. Cordeiro EMG, Correa AS, Guedes RNC (2014) Insecticide-mediated shift in ecological dominance between two competing species of grain beetles. PLoS ONE 9:e100990CrossRefGoogle Scholar
  11. Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106CrossRefGoogle Scholar
  12. Devigne C, Detrain C (2002) Collective exploration and area marking in the ant Lasius niger. Insect Soc 49:357–362CrossRefGoogle Scholar
  13. Farooqui T (2013) A potential link among biogenic amines-based pesticides, learning and memory, and colony collapse disorder: a unique hypothesis. Neurochem Int 62:122–136CrossRefGoogle Scholar
  14. Gill RJ, Ramos-Rodriguez O, Raine NE (2012) Combined pesticide exposure severely affects individual- and colony-level traits in bees. Nature 491:105–108CrossRefGoogle Scholar
  15. Goulson D (2013) An overview of the environmental risks posed by neonicotinoid insecticides. J Appl Ecol 50:977–987CrossRefGoogle Scholar
  16. Guedes RNC, Smagghe G, Stark JD, Desneux N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu Rev Entomol 61:3.1–3.20Google Scholar
  17. IBM Corporation (2013) IBM SPSS statistics for Macintosh, Version 22.0. IBM Corp, ArmonkGoogle Scholar
  18. Jeschke P, Neuen R, Schindler M, Elbert A (2011) Overview of the status and global strategy for neonicotinoids. J Agric Food Chem 59:2897–2908CrossRefGoogle Scholar
  19. Matsuda K, Buckingham SD, Kleier D, Rauh JJ, Grauso M, Sattelle DB (2001) Neonicotinoids: insecticides acting on insect nicotinic acetylcholine receptors. Trends Pharmacol Sci 22:573–580CrossRefGoogle Scholar
  20. Mommaerts M, Reynders S, Boulet J, Besard L, Sterk G, Smagghe G (2010) Risk assessment for side-effects of neonicotinoids against bumblebess with and without impairing behavior. Ecotoxicology 19:207–215CrossRefGoogle Scholar
  21. Ozaki M, Wada-Katsuma A, Fujikawa K, Iwasaki M, Yokohari F, Satoji Y, Nisimura T, Yamaoka R (2005) Ant nestmate and non-nestmate discrimination by a chemosensory sensillum. Science 309:311–314CrossRefGoogle Scholar
  22. Parr CL (2008) Dominant ants can control assemblage species richness in a South African savanna. J Anim Ecol 77:1191–1198CrossRefGoogle Scholar
  23. Pontin J (1961) Population stabilization and competition between the ants Lasius flavus (F.) and L. niger (L.). J Anim Ecol 30:47–54CrossRefGoogle Scholar
  24. Reitz SR, Trumble JT (2002) Competitive displacement among insects and arachnids. Annu Rev Entomol 47:435–465CrossRefGoogle Scholar
  25. Riley JR, Greggers U, Smith AD, Reynolds DR, Menzel R (2005) The flight paths of honeybee recruited by the waggle dance. Nature 435:205–207CrossRefGoogle Scholar
  26. Rodriguez-Cabal MA, Stuble KL, McCormick GL, Juric I, Dunn RR, Sanders NJ (2013) Tradeoffs, competition, and coexistence in eastern deciduous forest ant communities. Oecologia 171:981–992CrossRefGoogle Scholar
  27. SAS Institute (2013) JMP® for Macintosh, Version 11.1.1. Cary, SAS Institute IncGoogle Scholar
  28. Savolainen R, Vepsäläinen K, Wuorenrinne H (1989) Ant assemblages in the taiga biome: testing the role of territorial wood ants. Oecologia 81:481–486CrossRefGoogle Scholar
  29. Seifert B (2007) Die Ameisen Mittel- und Nordeuropas. Lutra, GörlitzGoogle Scholar
  30. Sih A, Cote J, Evans M, Fogarty S, Pruitt J (2012) Ecological implications of behavioural syndromes. Ecol Lett 15:278–289CrossRefGoogle Scholar
  31. Suarez AV, Tsutsui ND, Holway DA, Case TJ (1999) Behavioral and genetic differentiation between native and introduced populations of the Argentine ant. Biol Invasions 1:43–53CrossRefGoogle Scholar
  32. Sur R, Stork A (2003) Uptake, translocation and metabolism of imidacloprid in plants. Bull Insectol 56:35–40Google Scholar
  33. R Development Core Team (2013) R: A language and environment for statistical computing. 3.0.1 ed. Vienna, R foundation for statistical computingGoogle Scholar
  34. Therneau T (2013) A package for survival analysis in S. R package version 2.37-4Google Scholar
  35. Thorne BL, Breisch NL (2001) Effects of sublethal exposure to imidacloprid on subsequent behavior of subterranean termite Reticulitermes virginicus (Isoptera: Rhinotermitidae). J Econ Entomol 94:492–498CrossRefGoogle Scholar
  36. Tomé HVV, Martins GF, Lima MAP, Campos LAO, Guedes RNC (2012) Imidacloprid induced impairment of mushroom bodies and behavior of the native stingless bee Melipona quadrifasciata anthidioides. PLoS ONE 7:e38406CrossRefGoogle Scholar
  37. Vepsäläinen K, Pisarski B (1982) Assembly of island ant communities. Ann Zool Fennici 19:327–335Google Scholar
  38. Whitehorn PR, O`Conner S, Wackers FL, Goulson D (2012) Neonicotinoid pesticide reduces bumblebee colony growth and queen production. Science 20(336):351–352CrossRefGoogle Scholar
  39. Williamson SM, Wright GA (2013) Exposure to multiple cholinergic pesticides impairs olfactory learning and memory in honeybees. J Exp Biol 216:1799–1807CrossRefGoogle Scholar
  40. Wolf M, Weissing FJ (2012) Animal personalities—consequences for ecology and evolution. Trends Ecol Evol. doi:10.1016/j.tree.2012.05.001 Google Scholar
  41. Yang EC, Ciiuang YC, Ciien YL, Ciiang L (2008) Abnormal foraging behaviour induced by sublethal dosage of imidacloprid in the honey bee (Hymenoptera:Apidae). J Econ Entomol 107:1743–1748CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  1. 1.Department of Biodiversity and Nature ConservationInstitute for Biology Philipps-University of MarburgMarburgGermany
  2. 2.Animal Physiological Ecology, Institute for Evolution and EcologyEberhard Karls University of TübingenTübingenGermany

Personalised recommendations