Skip to main content
Log in

Sublethal effects of imidacloprid on the predatory seven-spot ladybird beetle Coccinella septempunctata

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

The seven-spot ladybird beetle, Coccinella septempunctata, is a major natural enemy of aphids in the field and in greenhouses in China and is part of integrated pest management (IPM). Imidacloprid, a highly efficient insecticide that not only kills aphids at lethal concentrations, but also can cause various sublethal effects in nontarget organisms. To strengthen IPM and its sustainability, it is important assessing possible side effects on natural enemies. When the effects of sublethal concentrations (LC5 and 10%LC5) of imidacloprid on C. septempunctata were evaluated, the adult longevity was shortened by 23.97 and 28.68 %, and the fecundity reduced by 52.81 and 56.09 % compared to control population. In the F1 generation (i.e., the progeny of the exposed individuals), the juvenile development was slower by 1.44 days and 0.66 days, and the oviposition period was shortened by 10 and 13 days, respectively. The fecundity of the F1 generation decreased by 17.88, 44.03 and 51.69 % when exposed to 1%LC5, 10%LC5, and LC5, respectively. The results of demographical growth estimates showed that the intrinsic rate of increase (r m ) and net reproductive rate (R 0 ) were lower in C. septempunctata populations that had been exposed to sublethal concentrations of imidacloprid. The results emphasize the importance of assessing side effects of low imidacloprid concentrations on such predator species, even at the transgenerational level.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Abbes K, Biondi A, Kurtulus A, Ricupero M, Russo A, Siscaro G, Chermiti B, Zappalà L (2015) Combined non-target effects of insecticide and high temperatures on the parasitoid Bracon nigricans. PLoS One 10(9):e0138411

    Article  Google Scholar 

  • Abbott WS (1925) A method for computing the effectiveness of an insecticide. J Econ Entomol 18:265–267

    Article  CAS  Google Scholar 

  • Ali A, Ahmad F, Biondi A, Wang Y, Desneux N (2012) Potential for using Datura alba leaf extracts against two major stored grain pests, the khapra beetle Trogoderma granarium and the rice weevil Sitophillus oryzae. J Pest Sci 85:359–366

    Article  Google Scholar 

  • Ahmad M, Ossiewatsch HR, Basedow T (2003) Effects of neem treated aphids as food/hosts on their predators and parasitoids. J Appl Entomol 127:458–464

    Article  CAS  Google Scholar 

  • Baas J, Jager T, Kooijman B (2010) A review of DEB theory in assessing toxic effects of mixtures. Sci Total Environ 408:3740–3745

    Article  CAS  Google Scholar 

  • Bengochea P, Budia F, Viñuela E, Medina P (2014) Are kaolin and copper treatments safe to the olive fruit fly parasitoid Psyttalia concolor? J Pest Sci 87:351–359

    Article  Google Scholar 

  • Biondi A, Desneux N, Siscaro G, Zappalà L (2012a) Using organic-certified rather than synthetic pesticides may not be safer for biological control agents: selectivity and side effects of 14 pesticides on the predator Orius laevigatus. Chemosphere 87:803–812

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Biondi A, Zappalà L, Stark JD, Desneux N (2013) Do biopesticides affect the demographic traits of a parasitoid wasp and its biocontrol services through sublethal effects? PLoS One 8:e76548

    Article  CAS  Google Scholar 

  • Biondi A, Campolo O, Desneux N, Siscaro G, Palmeri V, Zappalà L (2015) Life stage-dependent susceptibility of Aphytis melinus DeBach (Hymenoptera: Aphelinidae) to two pesticides commonly used in citrus orchards. Chemosphere 128:142–147

    Article  CAS  Google Scholar 

  • Biondi A, Zappalà L, Di Mauro A, Tropea Garzia G, Russo A, Desneux N, Siscaro G (2016) Can alternative host plant and prey affect phytophagy and biological control by the zoophytophagous mirid Nesidiocoris tenuis?. BioControl 61:79–90

    Article  Google Scholar 

  • Bompard A, Jaworski CC, Bearez P, Desneux N (2013) Sharing a predator: can an invasive alien pest affect the predation on a local pest? Pop Ecol 55:433–440

    Article  Google Scholar 

  • Blacquiere T, Smagghe G, Van Gestel CA, Mommaerts V (2012) Neonicotinoids in bees: a review on concentrations, side-effects and risk assessment. Ecotoxicology 21:973–992

    Article  CAS  Google Scholar 

  • Bozsik A (2006) Susceptibility of adult Coccinella septempunctata (Coleoptera: Coccinellidae) to insecticides with different modes of action. Pest Manag Sci 62:651–654

    Article  CAS  Google Scholar 

  • Cabral S, Soares AO, Garcia P (2011) Voracity of Coccinella undecimpunctata: effects of insecticides when foraging in a prey/plant system. J Pest Sci 84:373–379

    Article  Google Scholar 

  • Chen Z, Qu Y, Xiao D, Song L, Zhang S, Gao X, Desneux N, Song D (2015) Lethal and social-mediated effects of ten insecticides on the subterranean termite Reticulitermes speratus. J Pest Sci 88:741–751

    Article  Google Scholar 

  • Chi H (1988) Life-table analysis incorporating both sexes and variable development rates among individuals. Environ Entomol 17:26–31

    Article  Google Scholar 

  • Chi H (2012) TWOSEX-MS Chart: a computer program for the age-stage, two-sex life table analysis. National Chung Hsing University, Taichung Taiwan

    Google Scholar 

  • Chi H, Liu H (1985) Two new methods for the study of insect population ecology. Bull Inst Zool 24:225–240

    Google Scholar 

  • Chi H, Su HY (2006) Age-stage, two-sex life tables of Aphidius gifuensis (Ashmead) (Hymenoptera: Braconidae) and its host Myzus persicae (Sulzer) (Homoptera: Aphididae) with mathematical proof of the relationship between female fecundity and the net reproductive rate. Environ Entomol 35:10–21

    Article  Google Scholar 

  • Cresswell JE, Desneux N, vanEngelsdorp D (2012) Dietary traces of neonicotinoid pesticides as a cause of population declines in honey bees: an evaluation by Hill’s epidemiological criteria. Pest Manag Sci 68:819–827

    Article  CAS  Google Scholar 

  • Desneux N, Wajnberg E, Fauvergue X, Privet S, Kaiser L (2004) Oviposition behaviour and patch‐time allocation in two aphid parasitoids exposed to deltamethrin residues. Entomol Exp Appl 112:227–235

    Article  CAS  Google Scholar 

  • Desneux N, Ramirez‐Romero R, Kaiser L (2006) Multistep bioassay to predict recolonization potential of emerging parasitoids after a pesticide treatment. Environ Toxicol Chem 25:2675–2682

    Article  CAS  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  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Eisenback BM, Salom SM, Kok LT, Lagalante AF (2010) Lethal and sublethal effects of imidacloprid on Hemlock woolly Adelgid (Hemiptera: Adelgidae) and two introduced predator species. J Econ Entomol 103:1222–1234

    Article  CAS  Google Scholar 

  • Finney DJ (1971) Probit analysis. Cambridge University Press, Cambridge

    Google Scholar 

  • Fogel MN, Schneider MI, Desneux N, Gonzalez B, Ronco AE (2013) Impact of the neonicotinoid acetamiprid on immature stages of the predator Eriopis connexa (Coleoptera: Coccinellidae). Ecotoxicology 22:1063–1071

    Article  CAS  Google Scholar 

  • Gao SK, Yang ZQ (2015) Application of life table in pest biological control. Chinese. J Biol Control 31:256–263

    Google Scholar 

  • Grafton-Cardwell EE, Gu P (2003) Conserving vedalia beetle, Rodolia cardinalis (Mulsant) (Coleoptera: Coccinellidae), in citrus: a continuing challenge as new insecticides gain registration. J Econ Entomol 96:1388–1398

    Article  CAS  Google Scholar 

  • Gerami S, Jahromi KT, Ashouri A, Rasoulian G, Heidari A (2005) Sublethal effects of imidacloprid and pymetrozine on the life table parameters of Aphis gossypii Glover (Homoptera: Aphididae). Comm Appl Biol Sci 70:779–785

    CAS  Google Scholar 

  • Gontijo PC, Moscardini VF, Michaud JP, Carvalho GA (2014) Non-target effects of chlorantraniliprole and thiamethoxam on Chrysoperla carnea when employed as sunflower seed treatments. J Pest Sci 87:711–719

    Article  Google Scholar 

  • Guedes RNC, Smagghe G, Stark JD, Desneux N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu Rev Entomol 61:43–62

    Article  CAS  Google Scholar 

  • Han P, Niu CY, Lei CL, Cui JJ, Desneux N (2010) Quantification of toxins in a Cry1Ac+CpTI cotton cultivar and its potential effects on the honey bee Apis mellifera L. Ecotoxicology 19:1452–1459

  • Han P, Niu CY, Biondi A, Desneux N (2012) Does transgenic Cry1Ac+CpTI cotton pollen affect hypopharyngeal gland development and midgut proteolytic enzyme activity in the honey bee Apis mellifera L. (Hymenoptera, Apidae)? Ecotoxicology 21:2214–2221

    Article  CAS  Google Scholar 

  • He YX, Zhao J, Zheng Y, Zhan Z, Desneux N, Wu KM (2012) Lethal effect of imidacloprid on the coccinellid predator Serangium japonicum and sublethal effects on predator voracity and on functional response to the whitefly Bemisia tabaci. Ecotoxicology 21:1291–1300

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Jager T, Zimmer EI (2012) Simplified dynamic energy budget model for analysing ecotoxicity data. Ecol Model 225:74–81

    Article  CAS  Google Scholar 

  • Ji LL, Dong YK, Li ZH (2011) The indoor toxicity effect of four pesticides to the adult of Coccinella septempunctata. Shangdong Agric Sci 5:74–75. (in Chinese)

    Google Scholar 

  • Liang P, Tian YA, Biondi A, Desneux N, Gao XW (2012) Short-term and transgenerational effects of the neonicotinoid nitenpyram on susceptibility to insecticides in two whitefly species. Ecotoxicology 21:1889–1898

    Article  CAS  Google Scholar 

  • Lu YH, Wu KM, Jiang YY, Guo YY, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487:362–365

    Article  CAS  Google Scholar 

  • Lucas E, Giroux S, Demougeo S, Duchesne RM, Coderre D (2004) Compatibility of a natural enemy, Coleomegilla maculata lengi (Col.,Coccinellidae) and four insecticides used against the Colorado potato beetle (Col.,Chrysomelidae). J Appl Entomol 128:233–239

    Article  Google Scholar 

  • Malaquias JB, Ramalho FS, Omoto C, Godoy WAC, Silveira RF (2013) Imidacloprid affects the functional response of predator Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) to strains of Spodoptera frugiperda (JE Smith) on Bt cotton. Ecotoxicology 23:192–200

    Article  Google Scholar 

  • Mirande L, Desneux N, Haramboure M, Schneider MI (2015) Intraguild predation between an exotic and a native coccinellid in Argentina: the role of prey density. J Pest Sci 88:155–162

    Article  Google Scholar 

  • Moscardini VF, Gontijo PC, Michaud JP, Carvalho GA (2015) Sublethal effects of insecticide seed treatments on two nearctic lady beetles (Coleoptera: Coccinellidae). Ecotoxicology 5:1152–1161

    Article  Google Scholar 

  • Moser SE, Obrycki JJ (2009) Non-target effects of neonicotinoid seed treatments: mortality of coccinellid larvae related to zoophytophagy. Biol Control 51:487–492

    Article  Google Scholar 

  • Nauen R, Koob B, Elbert A (1998) Antifeedant effects of sublethal dosages of imidacloprid on Bemisia tabaci. Entomol Exp Appl 88:287–293

    Article  CAS  Google Scholar 

  • Palumbo JC, Horowitz AR, Prabhaker N (2001) Insecticidal control and resistance management for Bemisia tabaci. Crop Prot 20:739–765

    Article  CAS  Google Scholar 

  • Pan H, Liu Y, Liu B, Lu Y, Xu X, Qian X et al. (2014) Lethal and sublethal effects of cycloxaprid, a novel cis-nitromethylene neonicotinoid insecticide, on the mirid bug Apolygus lucorum. J Pest Sci 87:731–738

    Article  Google Scholar 

  • Papachristos DP, Milonas PG (2008) Adverse effects of soil applied insecticides on the predatory coccinellid Hippodamia undecimnotata (Coleoptera: Coccinellidae). Biol Control 47:77–81

    Article  CAS  Google Scholar 

  • Pérez-Hedo M, Urbaneja A (2015) Prospects for predatory mirid bugs as biocontrol agents of aphids in sweet peppers. J Pest Sci 88:65–73

    Article  Google Scholar 

  • Qu YY, Xiao D, Li JY, Chen Z, Biondi A, Desneux N, Gao XW, Song DL (2015) Sublethal and hornesis effects of imidacloprid on the soybean aphid Aphis glycines. Ecotoxicology 24:479–487

    Article  CAS  Google Scholar 

  • Ragsdale DW, Landis DA, Brodeur J, Heimpel GE, Desneux N (2011) Ecology and management of the soybean aphid in North America. Annu Rev Entomol 56:375–399

  • Ramirez-Romero R, Desneux N, Decourtye A, Chaffiol A, Pham-Delègue MH (2008) Does Cry1Ab protein affect learning performances of the honeybee Apis mellifera L. Ecotoxicol Environ Saf 70:327–333

  • Saeed R, Razaq M, Hardy IC (2015) The importance of alternative host plants as reservoirs of the cotton leaf hopper, Amrasca devastans, and its natural enemies. J Pest Sci 88:517–531

    Article  Google Scholar 

  • Sanchez-Bayo F (2014) The trouble with neonicotinoids. Science 6211:806–807

    Article  Google Scholar 

  • Sanchez-Bayo F, Goulson D, Pennacchio F, Nazzi F, Goka K, Desneux N (2016) Are bee diseases linked to pesticides? – A brief review. Environ Int 89-90:7–11

  • Schneider MI, Sanchez N, Pineda S, Chi H, Ronco A (2009) Impact of glyphosate on the development, fertility and demography of Chrysoperla externa (Neuroptera: Chrysopidae): ecological approach. Chemosphere 76:1451–1455

    Article  CAS  Google Scholar 

  • Singh SR, Walters KFA, Port GR, Northing P (2004) Consumption rates and predatory activity of adult and forth instar larvae of the seven spot ladybird, Coccinella septempunctata (L.), following contact with dimethoate residue and contaminated prey in laboratory arenas. Biol Control 30:127–133

    Article  CAS  Google Scholar 

  • Smith SF, Krischik VA (1999) Effects of systemic imidacloprid on Coleomegilla maculata (Coleoptera: Coccinellidae). Biol control 28:1189–1195

    CAS  Google Scholar 

  • Sohrabi F, Shishehbor P, Saber M, Mosaddegh MS (2012) Lethal and sublethal effects of buprofezin and imidacloprid on the whitefly parasitoid Encarsia inaron (Hymenoptera: Aphelinidae). Crop Prot 32:83–89

    Article  CAS  Google Scholar 

  • Sohrabi F, Shishehbor P, Saber M, Mosaddegh MS (2013) Lethal and sublethal effects of imidcaloprid and buprofezin on the sweetpotato white parasitoid Eretmocerus mundus (Hymenoptera: Aphelinidae). Crop Prot 45:98–103

    Article  CAS  Google Scholar 

  • Stark JD, Banks JE (2003) Population-level effects of pesticides and other toxicants on arthropods. Annu Rev Entomol 48:505–519

    Article  CAS  Google Scholar 

  • Stark JD, Banks JE, Vargas R (2004) How risky is risk assessment: the role that life history strategies play in susceptibility of species to stress. Proc Natl Acad Sci USA 101:732–736

    Article  CAS  Google Scholar 

  • Stark JD, Vargas RI, Banks JE (2007) Incorporating ecologically relevant measures of pesticide effect for estimating the compatibility of pesticides and biocontrol agents. J Econ Entomol 100:1027–1032

    Article  Google Scholar 

  • Tan XL, Zhao J, Zhang F, Wang S (2014) Light dependency of life trails, reproduction, locomotion, and predaion in the polyphagous ladybird Hippodamia variegata. Entomol Exp Appl 152:200–208

    Article  Google Scholar 

  • Tan Y, Biondi A, Desneux N, Gao XW (2012) Assessment of physiological sublethal effects of imidacloprid on the mirid bug Apolygus lucorum (Meyer-Dür). Ecotoxicology 21:1989–1997

    Article  CAS  Google Scholar 

  • Tomizawa M, Casida JE (2001) Structure and diversity of insect nicotinic acetylcholine receptors. Pest Manag Sci 57:914–922

    Article  CAS  Google Scholar 

  • Torres JB, Ruberson JR (2004) Toxicity of thiamethoxam and imidacloprid to Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) nymphs associated to aphid and whitefly control in cotton. Neotrop Entomol 33:99–106

    Article  CAS  Google Scholar 

  • van Herk WG, Vernon RS, Vojtko B, Snow S, Fortier J, Fortin C (2015) Contact behaviour and mortality of wireworms exposed to six classes of insecticide applied to wheat seed. J Pest Sci 88:717–739

    Article  Google Scholar 

  • Vincent C, Ferran A, Guige L, Gambier J, Brun J (2000) Effects of imidacloprid on Harmonia axyridis (Coleoptera: Coccinellidae) larval biological and locomotorybehavior. Eur J Entomol 97:501–506

    Article  CAS  Google Scholar 

  • Wang S, Qi Y, Desneux N, Shi X, Biondi A, Gao X (2017) Sublethal and transgenerational effects of short-term and chronic exposures to the neonicotinoid nitenpyram in Aphis gossypii. J Pest Sci. doi: 10.1007/s10340-016-0770-7

  • Youn YN, Seo MJ, Shin JG, Jang C, Yub YM (2003) Toxicity of greenhouse pesticides to multicolored Asian ladybeetles, Harmonia axyridis (Coleoptera: Coccinellidae). Biol Control 28:164–170

    Article  CAS  Google Scholar 

  • Yu CH, Fu, MR, LinRH, ZhangY, LiuYQ, JiangH, Brock, T.CM (2014a) Toxic effects of hexaflumuron on the development of Coccinella septempunctata. Environ Sci Pollut Res. 21:1418–1424

  • Yu CH, Lin RH, Fu MR, Zhou YM, Zong FL, Jiang H, Lv N, Piao XY, Zhang J, Liu YQ, Brock TCM (2014b) Impact of imidacloprid on life-cycle development of Coccinella septempunctata in laboratory microcosms. Ecotoxicol Environ Safe 110:168–173

    Article  CAS  Google Scholar 

  • Zotti MJ, Grutzmacher AD, Lopes IH, Smagghe G (2013) Comparative effects of insecticides with different mechanisms of action on Chrysoperla externa (Neuroptera: Chrysopidae): Lethal, sublethal and dose-response effects. Insect Sci 20:743–752

    Article  CAS  Google Scholar 

  • Zhang DW, Dong M, Du XG (2011) Effects of organic management on predator densities of Myzus persicae (Sulzer) during transition to organic agriculture in peach fields in China. J Sustain Agri 35:826–839

    Article  Google Scholar 

  • Zhang X, Xu Q, Lu W, Liu F (2015) Sublethal effects of four synthetic insecticides on the generalist predator Cyrtorhinus lividipennis. J Pest Sci 88:383–392

    Article  Google Scholar 

  • Zhao J, Li S, Gao XW, Zhang F, Wang S (2015) Comparison of life tables of Cheilomenes sexmaculata (Coleoptera: Coccinellidae) under laboratory and greenhouse conditions. J Econ Entomol 108:1700–1707

    Article  Google Scholar 

Download references

Acknowledgements

This research was supported by the National Key Basic Research and Development Program (973 program 2013CB127605), the Special Fund for Agro-scientific Research in the Public Interest (201303108), and the Beijing Novo Program (z121105002512039). The authors are grateful to Professor Hsin Chi (Laboratory of Theoretical and Applied Ecology, Department of Entomology, National Chung Hsing University, Taiwan) for providing the age-stage two-sex life table software.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Su Wang.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Statement of Human and Animal Rights

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures performed in studies involving animals were in accordance with the ethical standards of the institution or practice at which the studies were conducted.

Informed consent

There were no human subjects, thus informed consent is not applicable for this study.

Additional information

Da Xiao and Jing Zhao contributed equally to the study

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xiao, D., Zhao, J., Guo, X. et al. Sublethal effects of imidacloprid on the predatory seven-spot ladybird beetle Coccinella septempunctata . Ecotoxicology 25, 1782–1793 (2016). https://doi.org/10.1007/s10646-016-1721-z

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-016-1721-z

Keywords

Navigation