, Volume 24, Issue 6, pp 1221–1228 | Cite as

Different acute toxicity of fipronil baits on invasive Linepithema humile supercolonies and some non-target ground arthropods

  • Daisuke Hayasaka
  • Naoki Kuwayama
  • Azuma Takeo
  • Takanobu Ishida
  • Hiroyuki Mano
  • Maki N. Inoue
  • Takashi Nagai
  • Francisco Sánchez-Bayo
  • Koichi Goka
  • Takuo Sawahata


Fipronil is one of the most effective insecticides to control the invasive ant Linepithema humile, but its effectiveness has been assessed without considering the genetic differences among L. humile supercolonies. We hypothesized that the susceptibility of the ant to fipronil might differ among supercolonies. If so, dosage and concentration of fipronil may need to be adjusted for effective eradication of each supercolony. The relative sensitivities of four L. humile supercolonies established in Hyogo (Japan) to fipronil baits were examined based on their acute toxicity (48-h LC50). Toxicities of fipronil to seven ground arthropods, including four native ant species, one native isopoda, and two cockroaches were also determined and compared to that of L. humile supercolonies using species sensitivity distributions. Marked differences in susceptibility of fipronil were apparent among the supercolonies (P < 0.008), with the ‘Japanese main supercolony’ (271 μg L−1) being five to ten times more sensitive to fipronil than other colonies (1183–2782 μg L−1). Toxicities to non-target species (330–2327 μg L−1) were in the same range as that of L. humile, and SSDs between the two species groups were not significantly different (t = −1.389, P = 0.180), suggesting that fipronil’s insecticidal activity is practically the same for L. humile as for non-target arthropods. Therefore, if the invasive ant is to be controlled using fipronil, this would also affect the local arthropod biodiversity. Only the ‘Japanese main supercolony’ can be controlled with appropriate bait dosages of fipronil that would have little impact on the other species.


Chemical controls Eradication Intra- and inter-species variation Invasive species Species sensitivity distributions (SSD) Susceptibility Terrestrial arthropods 



Some specimens of the two cockroach species and of Pristomyrmex punctatus were provided by Earth Chemical Co., Ltd., Japan. We thank Kurumi Morishita for her kind assistance with the toxicity tests. The authors wish to thank Dr. Rafael Barbieri and Dr. Tomoyuki Yokoi for valuable technical advices. Our special thanks to Shinobu Ando of Ministry of the Environment, Japan for permission to raise the invasive Linepithema humile in our laboratory (permit number 13000057). This study was supported by the Environment Research and Technology Development Fund (ERTDF) (4-1401, Leader: Koichi Goka) of the Ministry of the Environment, Japan, 2014. The paper benefited from the constructive comments of two anonymous reviewers as referees.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Aldenberg T, Jaworska JS (2000) Uncertainty of the hazardous concentration and fraction affected for normal species sensitivity distributions. Ecotoxicol Environ Saf 46:1–18CrossRefGoogle Scholar
  2. ANZECC (2000) Australian and New Zealand guidelines for fresh and marine water quality. Australian and New Zealand Environment and Conservation CouncilGoogle Scholar
  3. Baird DJ, Barber I, Bradley M, Soares AMVM, Calow P (1991) A comparative study of genotype sensitivity to acute toxic stress using clones of Daphnia magna Straus. Ecotoxicol Environ Saf 21:257–265CrossRefGoogle Scholar
  4. Barata C, Baird DJ, Soares AMVM (2002a) Determining genetic variability in the distribution of sensitivities to toxic stress among and within field populations of Daphnia magna. Environ Sci Tech 36:3045–3049CrossRefGoogle Scholar
  5. Barata C, Baird DJ, Mitchell SE, Soares AMVM (2002b) Among- and within-population variability in tolerance to cadmium stress in natural populations of Daphnia magna: implications for ecological risk assessment. Environ Toxicol Chem 21:1058–1064CrossRefGoogle Scholar
  6. 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 Ser B 280:20132157CrossRefGoogle Scholar
  7. Beketov MA, Liess M (2008) Acute and delayed effects of the neonicotinoid insecticide thiacloprid on seven freshwater arthropods. Environ Toxicol Chem 27:461–470CrossRefGoogle Scholar
  8. Brix KV, DeForest DK, Adams WJ (2001) Assessing acute and chronic copper risks to freshwater aquatic life using species sensitivity distributions for different taxonomic groups. Environ Toxicol Chem 20:1846–1856CrossRefGoogle Scholar
  9. Chagnon NL, Guttman SI (1989) Differential survivorship of allozyme genotypes in mosquitofish populations exposed to copper or cadmium. Environ Toxicol Chem 8:319–326CrossRefGoogle Scholar
  10. Choe D-H, Vetter RS, Rust MK (2010) Development of virtual bait stations to control Argentine ants (Hymenoptera: Formicidae) in environmentally sensitive habitats. J Econ Entomol 103:1761–1769CrossRefGoogle Scholar
  11. Cole LM, Nicholson RA, Casida JE (1993) Action of phenylpyrazole insecticides at the Gaba-Gated chloride channel. Pestic Biochem Physiol 46:47–54CrossRefGoogle Scholar
  12. Collins HL, Callcott AMA (1998) Fipronil: an ultra-low-dose bait toxicant for control of red imported fire ants (Hymenoptera: Formicidae). Florida Entomol 81:407–415CrossRefGoogle Scholar
  13. Costa HS, Rust MK (1999) Mortality and foraging rates of Argentine ant (Hymenoptera: Formicidae) colonies exposed to potted plants treated with fipronil. J Agric Urban Entomol 16:37–48Google Scholar
  14. Duboudin C, Ciffroy P, Magaud H (2004) Effects of data manipulation and statistical methods on species sensitivity distributions. Environ Toxicol Chem 23:489–499CrossRefGoogle Scholar
  15. ECB (2003) Technical guidance document on risk assessment. Part II Environmental risk assessment, European Chemical BureauGoogle Scholar
  16. Frampton GK, Jänsch S, Scott-Fordsmand JJ, Römbke J, van den Brink PJ (2006) Effects of pesticides on soil invertebrates in laboratory studies: a review and analysis using species sensitivity distributions. Environ Toxicol Chem 25:2480–2489CrossRefGoogle Scholar
  17. Gant DB, Chalmers AE, Wolff MA, Hoffman HB, Bushey DF (1998) Fipronil: action at the GABA receptor. In: Kuhr RJ, Motoyama N (eds) Pesticides and the Future. IOS Press, Amsterdam, pp 147–156Google Scholar
  18. García-Muñoz E, Guerrero F, Parra G (2010) Intraspecific and interspecific tolerance to copper sulphate in five Iberian amphibian species at two developmental stages. Arch Environ Contam Toxicol 59:312–321CrossRefGoogle Scholar
  19. Gentz MC (2009) A review of chemical control options for invasive social insects in island ecosystems. J Appl Entomol 133:229–235CrossRefGoogle Scholar
  20. Giraud T, Pedersen JS, Keller L (2002) Evolution of supercolonies: the Argentine ants of southern Europe. Proc Natl Acad Sci USA 99:6075–6079CrossRefGoogle Scholar
  21. Gunasekara AS, Truong T, Goh KS, Spurlock F, Tjeerdema RS (2007) Environmental fate and toxicology of fipronil. J Pestic Sci 32:189–199CrossRefGoogle Scholar
  22. Harris RJ (2002) Potential impact of the Argentine ant (Linepithema humile) in New Zealand and options for its control. Sci Conserv 196:1–36Google Scholar
  23. Hayasaka D (2015) Study of the impacts of systemic insecticides and their environmental fate in aquatic communities of paddy mesocosms. J Pestic Sci 39:172–173 CrossRefGoogle Scholar
  24. Hayasaka D, Korenaga T, Sánchez-Bayo F, Goka K (2012a) Differences in ecological impacts of systemic insecticides with different physicochemical properties on biocenosis of experimental paddy fields. Ecotoxicology 21:191–201CrossRefGoogle Scholar
  25. Hayasaka D, Korenaga T, Suzuki K, Saito F, Sánchez-Bayo F, Goka K (2012b) Cumulative ecological impacts of two successive annual treatments of imidacloprid and fipronil on aquatic communities of paddy mesocosms. Ecotoxicol Environ Saf 80:355–362CrossRefGoogle Scholar
  26. Hayasaka D, Korenaga T, Suzuki K, Sánchez-Bayo F, Goka K (2012c) Differences in susceptibility of five cladoceran species to two systemic insecticides, imidacloprid and fipronil. Ecotoxicology 21:421–427CrossRefGoogle Scholar
  27. Hayasaka D, Suzuki K, Nomura T, Nishiyama M, Nagai T, Sánchez-Bayo F, Goka K (2013) Comparison of acute toxicity of two neonicotinoid insecticides, imidacloprid and clothianidin, to five cladoceran species. J Pestic Sci 38:44–47CrossRefGoogle Scholar
  28. Helanterä H, Strassmann JE, Carrillo J, Queller DC (2009) Unicolonial ants: where do they come from, what are they and where are they going? Trends Ecol Evol 24:341–349CrossRefGoogle Scholar
  29. Hickey CW (1989) Sensitivity of four New Zealand cladoceran species and Daphnia magna to aquatic toxicants. New Zeal J Mar Fresh Res 23:131–137CrossRefGoogle Scholar
  30. Hoang TC, Pryor RL, Rand GM, Frakes RA (2011) Use of butterflies as nontarget insect test species and the acute toxicity and hazard of mosquito control insecticides. Environ Toxicol Chem 30:997–1005CrossRefGoogle Scholar
  31. Holway DA (1999) Competitive mechanisms underlying the displacement of native ants by the invasive Argentine ant. Ecology 80:238–251CrossRefGoogle Scholar
  32. Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233CrossRefGoogle Scholar
  33. Hooper-Bùi LM, Rust MK (2000) Oral toxicity of abamectin, boric acid, fipronil, and hydramethylnon to laboratory colonies of Argentine ants (Hymenoptera: Formicidae). J Econ Entomol 93:858–864CrossRefGoogle Scholar
  34. Hulme PE (2006) Beyond control: wider implications for the management of biological invasions. J Appl Ecol 43:835–847CrossRefGoogle Scholar
  35. Human KG, Gordon DM (1996) Exploitation and interference competition between the invasive Argentine ant, Linepithema humile, and native ant species. Oecologia 105:405–412CrossRefGoogle Scholar
  36. Inoue MN, Sunamura E, Suhr EL, Ito F, Tatsuki S, Goka K (2013) Recent range expansion of the Argentine ant in Japan. Divers Distrib 19:29–37CrossRefGoogle Scholar
  37. Inoue MN, Saito-Morooka F, Suzuki K, Nomura T, Hayasaka D, Kishimoto T, Sugimaru K, Sugiyama T, Goka K (2015) Ecological impacts on native ant and ground-dwelling animal communities through the Argentine ant (Linepithema humile) (Hymenoptera: Formicidae) management in Japan. Appl Entomol Zool. doi: 10.1007/s13355-015-0338-7 Google Scholar
  38. Jiang W, Soeprono A, Rust MK, Gan J (2013) Ant control efficacy of pyrethroids and fipronil on outdoor concrete surfaces. Pest Manag Sci 70:271–277CrossRefGoogle Scholar
  39. Kiffney PM, Clements WH (1996) Size-dependent response of macroinvertebrates to metals in experimental streams. Environ Toxicol Chem 15:1352–1356CrossRefGoogle Scholar
  40. Klotz JK, Rust MK, Field HC, Greenberg L, Kupfer K (2009) Low impact directed sprays and liquid baits to control Argentine ants (Hymenoptera: Formicidae). Sociobiology 54:101–108Google Scholar
  41. Krushelnycky PD, Gillespie RG (2008) Compositional and functional stability of arthropod communities in the face of ant invasions. Ecol Appl 18:1547–1562CrossRefGoogle Scholar
  42. Lach L (2008) Argentine ants displace floral arthropods in a biodiversity hotspot. Divers Distrib 14:281–290CrossRefGoogle Scholar
  43. Lorente C, Causapé J, Glud RN, Hancke K, Merchán D, Muñiz S, Val J, Navarro E (2015) Impacts of agricultural irrigation on nearby freshwater ecosystems: the seasonal influence of triazine herbicides in benthic algal communities. Sci Total Environ 503:151–158CrossRefGoogle Scholar
  44. Lowe S, Browne M, Boudjelas S (2000) 100 of the world’s worst invasive alien species. Aliens 12:1–12Google Scholar
  45. Ministry of the Environment, Japan (2013) Control manuals of Argentine ant (Revised version). Ministry of the Environment, Japan, TokyoGoogle Scholar
  46. Muyssen BTA, Bossuyt BTA, Janssen CR (2005) Inter- and intra-species variation in zinc tolerance of field-collected cladoceran populations. Chemosphere 61:1159–1167CrossRefGoogle Scholar
  47. Myers JH, Savoie A, van Randen E (1998) Eradication and pest management. Annu Rev Entomol 43:471–491CrossRefGoogle Scholar
  48. Nagai T, Yokoyama A (2012) Comparison of ecological risks of insecticides for nursery-box application using species sensitivity distribution. J Pestic Sci 37:233–239CrossRefGoogle Scholar
  49. OECD (1995) Guidance document for aquatic effects assessment. Organization for Economic Co-operation and DevelopmentGoogle Scholar
  50. OECD (1998) OECD guidelines for the testing of chemicals TG 213: honeybees, acute oral toxicity test. Organization for Economic Co-operation and DevelopmentGoogle Scholar
  51. Okaue M, Yamamoto K, Touyama Y, Kameyama T, Terayama M, Sugiyama T, Murakami K, Ito F (2007) Distribution of the Argentine ant, Linepithema humile, along the Seto Island Sea, western Japan: result of surveys in 2003-2005. Entomol Sci 10:337–342CrossRefGoogle Scholar
  52. Pino FG, Jove M (2005) Comparatibility of entomopathogenic nematodes with fipronil. J Helminthol 79:333–337CrossRefGoogle Scholar
  53. Posthuma L, Suter GW II, Traas TP (2001) Species sensitivity distributions in ecotoxicology. Lewis Publishers, Boca RatonCrossRefGoogle Scholar
  54. R-Development-Core-Team (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna (
  55. Rico A, Geber-Corrêa R, Campos PS, Garcia MVB, Waichman AV, van den Brink PJ (2010) Effects of parathion-methyl on Amazonian fish and freshwater invertebrates: a comparison of sensitivity with temperate data. Arch Environ Contam Toxicol 58:765–771CrossRefGoogle Scholar
  56. Ritz C (2010) Toward a unified approach to dose-response modeling in ecotoxicology. Environ Toxicol Chem 29:220–229CrossRefGoogle Scholar
  57. Ritz C, Streibig JC (2005) Bioassay analysis using R. J Stat Softw 12:1–22Google Scholar
  58. RIVM (2001) Guidance document on deriving environmental risk limits. National Institute of Public Health and the Environment, BilthovenGoogle Scholar
  59. Rouco M, López-Rodas V, González R, Huertas IE, García-Sánchez MJ, Flores-Moya A, Costas E (2014) The limit of the genetic adaptation to copper in freshwater phytoplankton. Oecologia 175:1179–1188CrossRefGoogle Scholar
  60. Roura-Pascual N, Hui C, Ikeda T, Leday G, Richardson DM, Carpintero S, Espadaler X, Gómez C, Guénard B, Hartley S, Krushelnycky P, Lester PJ, McGeoch MA, Menke SB, Pedersen JS, Pitt JPW, Reyes J, Sanders NJ, Suarez AV, Touyama Y, Ward D, Ward PS, Worner SP (2011) Relative roles of climatic suitability and anthropogenic influence in determining the pattern of spread in a global invader. Proc Natl Acad Sci USA 108:220–225CrossRefGoogle Scholar
  61. Rust MK, Reierson DA, Klotz JH (2003) Pest management of Argentine ants (Hymenoptera: Formicidae). J Entomol Sci 38:159–169Google Scholar
  62. 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 97:1017–1024CrossRefGoogle Scholar
  63. Sánchez-Bayo F (2012) Insecticides mode of action in relation to their toxicity to non-target organisms. J Environ Anal Toxicol S4:S4-002Google Scholar
  64. Scharf ME, Ratliff CR, Bennett GW (2004) Impacts of residual insecticide barriers on perimeter-invading ants, with particular reference to the odorous house ant, Tapinoma sessile. J Econ Entomol 97:601–605CrossRefGoogle Scholar
  65. Schlueter MA, Guttman SI, Oris JT, Bailer AJ (1995) Survival of copper-exposed juvenile fathead minnows (Pimephales promelas) differs among allozyme genotypes. Environ Toxicol Chem 14:1727–1734CrossRefGoogle Scholar
  66. Silverman J, Brightwell RJ (2008) The Argentine ant: challenges in managing an invasive unicolonial pest. Annu Rev Entomol 53:231–252CrossRefGoogle Scholar
  67. Simberloff D, Parker IM, Windle PN (2005) Introduced species policy, management, and future research needs. Front Ecol Environ 3:12–20CrossRefGoogle Scholar
  68. Soeprono AM, Rust MK (2004) Strategies for controlling argentine ants (Hymenoptera: Formicidae). Sociobiology 44:669–682Google Scholar
  69. Suarez AV, Holway DA, Case TJ (2001) Patterns of spread in biological invasions dominated by long-distance jump dispersal: insights from Argentine ant. Proc Natl Acad Sci USA 98:1095–1100CrossRefGoogle Scholar
  70. Sugiyama T (2000) Invasion of Argentine ant Linepithema humile into Hiroshima Prefecture Japan. Jap J Appl Entomol Zool 44:127–129 (in Japanese with English abstract) CrossRefGoogle Scholar
  71. Sunamura E, Nishisue K, Terayama M, Tatsuki S (2007) Invasion of four Argentine ant supercolonies into Kobe Port, Japan: their distributions and effects on indigenous ants (Hymenoptera: Formicidae). Sociobiology 50:659–674Google Scholar
  72. Sunamura E, Hatsumi S, Karino S, Nishisue K, Terayama M, Kitade O, Tatsuki S (2009) Four mutually incompatible Argentine ant supercolonies in Japan: inferring invasion history of introduced Argentine ants from their social structure. Biol Invasions 11:2329–2339CrossRefGoogle Scholar
  73. Sunamura E, Suzuki S, Sakamoto H, Nishisue K, Terayama M, Tatsuki S (2012) Impacts, ecology and dispersal of the invasive Argentine ant. In: Hendriks BP (ed) Agricultural Research Updates, vol 2., Nova Science PublishersHauppauge, NY, pp 207–237Google Scholar
  74. Thomas ML, Payne-Makrisâ CM, Suarez AV, Tsutsui ND, Holway DA (2006) When supercolonies collide: territorial aggression in an invasive and unicolonial social insect. Mol Ecol 15:4303–4315CrossRefGoogle Scholar
  75. Tsutsui ND, Case TJ (2001) Population genetics and colony structure of the Argentine ant (Linepithema humile) in its native and introduced ranges. Evolution 55:976–985CrossRefGoogle Scholar
  76. USEPA (1985) Guidelines for deriving numerical national water quality criteria for the protection of aquatic organisms and their uses. U.S. Environmental Protection Agency, Washington, DCGoogle Scholar
  77. USEPA (1996) Fipronil Pesticide Fact Sheet. EPA737-F-96-005, Washington, DCGoogle Scholar
  78. Valles SM, Koehler PG, Brenner RJ (1997) Antagonism of fipronil toxicity by piperonyl butoxide and S, S, S,-tributyl phosphorotrithioate in the German cockroach (Dictyoptera: Blattellidae). J Econ Entomol 90:1254–1258CrossRefGoogle Scholar
  79. White GL (1998) Control of the leaf-cutting ants Acromyrmex octospinosus (Reich.) and Atta cephalotes (L.) (Formicidae, Attini) with a bait of citrus meal and fipronil. Int J Pest Manag 44:115–117CrossRefGoogle Scholar
  80. Wilson EO, Durlach NI, Roth LM (1958) Chemical releasers of necrophoric behavior in ants. Psyche 65:108–114CrossRefGoogle Scholar
  81. Wiltz BA, Suiter DR, Gardner WA (2009) Activity of bifenthrin, chlorfenapyr, fipronil, and thiamethoxam against Argentine ants (Hymenoptera: Formicidae). J Econ Entomol 102:2279–2288CrossRefGoogle Scholar
  82. Zhao X, Yeh JZ, Salgado VL, Narahashi T (2005) Sulfone metabolite of fipronil blocks γ-aminobutyric acid- and glutamate-activated chloride channels in mammalian and insect neurons. J Pharmacol Exp Ther 314:363–373CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Daisuke Hayasaka
    • 1
  • Naoki Kuwayama
    • 1
  • Azuma Takeo
    • 1
  • Takanobu Ishida
    • 1
  • Hiroyuki Mano
    • 2
  • Maki N. Inoue
    • 3
  • Takashi Nagai
    • 4
  • Francisco Sánchez-Bayo
    • 5
  • Koichi Goka
    • 6
  • Takuo Sawahata
    • 1
  1. 1.Faculty of AgricultureKINDAI UniversityNaraJapan
  2. 2.Water Environment Research GroupPublic Works Research Institute (PWRI)TsukubaJapan
  3. 3.Department of Applied Biological ScienceTokyo University of Agriculture and TechnologyTokyoJapan
  4. 4.Organochemicals DivisionNational Institute for Agro-Environmental Sciences (NIAES)TsukubaJapan
  5. 5.Faculty of Agriculture & EnvironmentThe University of SydneyEveleighAustralia
  6. 6.Center for Environmental Biology and Ecosystem StudiesNational Institute for Environmental Studies (NIES)TsukubaJapan

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