Skip to main content
SpringerLink
Log in

Sublethal and transgenerational effects of short-term and chronic exposures to the neonicotinoid nitenpyram on the cotton aphid Aphis gossypii

  • Original Paper
  • Published:
Journal of Pest Science Aims and scope Submit manuscript

Abstract

Aphis gossypii Glover (Hemiptera: Aphididae) is a polyphagous pest worldwide. Neonicotinoid insecticides, such as nitenpyram, are widely used for its control in cotton crops. Sublethal or low exposure to these insecticides can cause contrasting effects on arthropod pest populations. Through laboratory experiments, we assessed the impact of low nitenpyram concentrations on the exposed A. gossypii generation (F0) and on its progeny (F1). Nitenpyram caused sublethal effects on reproduction and longevity in the aphids directly exposed (F0) to low doses. However, the estimated demographic indexes of the progeny (F1) of those individuals exposed for 72 h were higher than those of the control population. This is the first laboratory evidence of a transgenerational hormesis owing to low lethal and sublethal nitenpyram concentrations. Although these findings must be validated in real cropping conditions, it could be expected that, in addition to the acute effects that usually occur at high (label) doses, sublethal effects and hormesis can occur on the pest populations over time among insecticide applications in the field.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

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 temperature on the parasitoid Bracon nigricans. PLoS ONE 10:e0138411

    Article  PubMed  PubMed Central  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 

  • Ayyanath MM, Cutler GC, Scott-Dupree CD, Sibley PK (2013) Transgenerational shifts in reproduction hormesis in green peach aphid exposed to low concentrations of imidacloprid. PLoS ONE 8:e74532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azzam S, Wang F, Wu JC, Shen J, Wang LP, Yang GQ, Guo YR (2009) Comparisons of stimulatory effects of a series of concentrations of four insecticides on reproduction in the rice brown planthopper Nilaparvata lugens (Stål) (Hemiptera: delphacidae). Int J Pest Manag 55:347–358

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Biondi A, Desneux N, Amiens-Desneux E, Siscaro G, Zappalà L (2013b) Biology and developmental strategies of the Palaearctic parasitoid Bracon nigricans (Hymenoptera: Braconidae) on the Neotropical moth Tuta absoluta (Lepidoptera: Gelechiidae). J Econ Entomol 106:1638–1647

    Article  PubMed  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  PubMed  Google Scholar 

  • Blackman RL, Eastop VF (1984) Aphids on the World’s Crops: an identification and information guide. Wiley, New York

    Google Scholar 

  • Calabrese EJ, Baldwin LA (1998) Hormesis as a biological hypothesis. Environ Health Perspect 106:357–362

    Article  PubMed  PubMed Central  Google Scholar 

  • Campolo O, Chiera E, Malacrinò A, Laudani F, Fontana A, Albanese GR, Palmeri V (2014) Acquisition and transmission of selected CTV isolates by Aphis gossypii. J Asia Pac Entomol 17:493–498

    Article  Google Scholar 

  • Cordeiro EMG, De Moura ILT, Fadini MAM, Guedes RNC (2013) Beyond selectivity: are behavioral avoidance and hormesis likely causes of pyrethroid-induced outbreaks of the southern red mite Oligonychus ilicis? Chemosphere 93:1111–1116

    Article  CAS  PubMed  Google Scholar 

  • Cutler GC, Ramanaidu K, Astatkie T, Isman MB (2009) Green peach aphid, Myzus persicae (Hemiptera: Aphididae), reproduction during exposure to sublethal concentrations of imidacloprid and azadirachtin. Pest Manag Sci 65:205–209

    Article  CAS  Google Scholar 

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

    Article  CAS  PubMed  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, Fauvergue X, Dechaume-Moncharmont FX, Kerhoas L, Ballanger Y, Kaiser L (2005) Diaeretiella rapae limits Myzus persicae populations after applications of deltamethrin in oilseed rape. J Econ Entomol 98:9–17

    Article  PubMed  Google Scholar 

  • Desneux N, Denoyelle R, Kaiser L (2006a) A multi-step bioassay to assess the effect of the deltamethrin on the parasitic wasp Aphidius ervi. Chemosphere 65:1697–1706

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Elbert A, Haas M, Springer B, Thielert W, Nauen R (2008) Applied aspects of neonicotinoid uses in crop protection. Pest Manag Sci 64:1099–1105

    Article  CAS  PubMed  Google Scholar 

  • Finney DJ (1971) Statistical logic in monitoring of reactions to therapeutic drugs. Methods Inf Med 10:237

    CAS  PubMed  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, Cutler GC (2014) Insecticide-induced hormesis and arthropod pest management. Pest Manag Sci 70:690–697

    Article  CAS  PubMed  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  PubMed  Google Scholar 

  • Guo L, Desneux N, Sonoda S, Liang P, Han P, Gao XW (2013) Sublethal and transgenerational effects of chlorantraniliprole on biological traits of the diamondback moth, Plutella xylostella L. Crop Prot 48:29–34

    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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He YX, Zhao JW, Zheng Y, 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  PubMed  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  PubMed  PubMed Central  Google Scholar 

  • Hui JJ, Liu CZ, Meng YF, Chen J (2009) Sublethal effects of imidacloprid to Acyrthosiphon pisum. Plant Prot 35:86–88

    CAS  Google Scholar 

  • Kidd PW, Rummel DR (1997) Effect of insect predators and a pyrethroid insecticide on cotton aphid, Aphis gossypii Glover population density. Southwest Entomol 22:381–393

    Google Scholar 

  • Kidd PW, Rummel DR, Thorvilson HG (1996) Effect of cyhalothrin on field populations of the cotton aphid, Aphis gossypii Glover, in the Texas High Plains. Southwest Entomol 21:293–301

    CAS  Google Scholar 

  • Kindlmann P, Dixon AFG (1989) Developmental constraints in the evolution of reproductive strategies: telescoping of generations in parthenogenetic aphids. Funct Ecol 3:531–537

    Article  Google Scholar 

  • Lashkari MR, Sahragard A, Ghadamyari M (2007) Sublethal effects of imidacloprid and pymetrozine on population growth parameters of cabbage aphid, Brevicoryne brassicae on rapeseed, Brassica napus L. Insect Sci 14:207–212

    Article  CAS  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  PubMed  Google Scholar 

  • Lu CH, Liu XG, Dong FS, Xu J, Wang X, Zheng YQ (2010) Residue and degradation of nitenpyram in cotton and soil. Environ Chem 29:614–618

    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  PubMed  Google Scholar 

  • Magalhaes LC, Hunt TE, Siegfried BD (2009) Efficacy of neonicotinoid seed treatments to reduce soybean aphid populations under field and controlled conditions in Nebraska. J Econ Entomol 102:187–195

    Article  CAS  PubMed  Google Scholar 

  • Marshall KL, Collins D, Wilson LJ, Herron G (2014) Efficacy of two thiamethoxam pre-germination seed treatments and a phorate side-dressing against neonicotinoid and pirimicarb resistant cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae). Austral Entomology 54:351–357

    Article  Google Scholar 

  • Meyer JS, Ingersoll CG, McDonald LL, Boyce MS (1986) Estimating uncertainty in population growth rates: jackknife vs. bootstrap techniques. Ecology 67:1156–1166

    Article  Google Scholar 

  • Minamida I, Iwanaga K, Tabuchi T, Uneme H, Danstuji H, Okauchi T (1993) Synthesis and insecticidal activity of acyclic nitroethylene compounds containing a 3-pyridylmethylamino group. J Pestic Sci 18:31–40

    Article  Google Scholar 

  • Mollá O, Biondi A, Alonso-Valiente M, Urbaneja A (2014) A comparative life history study of two mirid bugs preying on Tuta absoluta and Ephestia kuehniella eggs on tomato crops: implications for biological control. Biocontrol 59:175–183

    Article  Google Scholar 

  • Moores GD, Gao XW, Denholm I, Devonshire AL (1996) Characterisation of insensitive acetylcholinesterase in insecticide resistant cotton aphids, Aphis gossypii Glover (Homoptera: Aphididae). Pestic Biochem Physiol 56:102–110

    Article  CAS  Google Scholar 

  • Nauen R, Jeschke P, Copping L (2008) In focus: neonicotinoid insecticides. Pest Manag Sci 64:1081

    Article  CAS  PubMed  Google Scholar 

  • Obana H, Okihashi M, Akutsu K, Kitagawa Y, Hori S (2003) Determination of neonicotinoid pesticide residues in vegetables and fruits with solid phase extraction and liquid chromatography mass spectrometry. J Agric Food Chem 51:2501–2505

    Article  CAS  PubMed  Google Scholar 

  • Pan H, Liu Y, Liu B, Lu Y, Xu 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 

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

    Article  CAS  PubMed  Google Scholar 

  • Rondeau G, Sanchez-Bayo F, Tennekes HA, Decourtye A, Ramirez-Romero R, Desneux N (2014) Delayed and time-cumulative toxicity of imidacloprid in bees, ants and termites. Sci Rep 4:srep05566

    Article  Google Scholar 

  • Santos MF, Santos RL, Tomé HVV, Barbosa WF, Martins GF, Guedes RNC, Oliveira EE (2016) Imidacloprid-mediated effects on survival and fertility of the Neotropical brown stink bug Euschistus heros. J Pest Sci 89:231–240

    Article  Google Scholar 

  • Satar S, Kersting U, Uygun N (1999) Development and fecundity of Aphis gossypii Glover (Homoptera: Aphididae) on three Malvaceae hosts. Turk J Agric For 23:637–643

    Google Scholar 

  • Shi XB, Jiang LL, Wang HY, Qiao K, Wang D, Wang KY (2011) Toxicities and sublethal effects of seven neonicotinoid insecticides on survival, growth and reproduction of imidacloprid-resistant cotton aphid, Aphis gossypii. Pest Manag Sci 67:1528–1533

    Article  CAS  PubMed  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-Dur). Ecotoxicology 21:1989–1997

    Article  CAS  PubMed  Google Scholar 

  • Tomizawa M, Casida JE (2003) Selective toxicity of neonicotinoids attributable to specificity of insect and mammalian nicotinic receptors. Annu Rev Entomol 48:339–364

    Article  CAS  PubMed  Google Scholar 

  • Tomizawa M, Latli B, Casida JE (1996) Novel neonicotinoid-agarose affinity column for Drosophila and Musca nicotinic acetylcholine receptors. J Neurochem 67:1669–1676

    Article  CAS  PubMed  Google Scholar 

  • Wang XY, Yang ZQ, Shen ZR, Lu J, Xu WB (2008) Sublethal effects of selected insecticides on fecundity and wing dimorphism of green peach aphid (Hom., Aphididae). J Appl Entomol 132:135–142

    Article  CAS  Google Scholar 

  • Wang HR, Wu JC, Yang F, Geng J, Wang F (2009) Life table parameters of imidacloprid resistant and susceptible populations of Nilaparvata lugens (Stål) (Hemiptera: Delphacidae) under sublethal doses of insecticides. Acta Ecologica Sinica 9:4753–4760

    Google Scholar 

  • Wu KM, Guo YY (2005) The evolution of cotton pest management practices in China. Ann Rev Entomol 50:31–52

    Article  CAS  Google Scholar 

  • Xiao D, Yang T, Desneux N, Han P, Gao XW (2015) Assessment of sublethal and transgenerational effects of pirimicarb on the wheat aphids Rhopalosiphum padi and Sitobion avenae. PLoS One 10:e0128936

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeng CX, Wang JJ (2010) Influence of exposure to imidacloprid on survivorship, reproduction and vitellin content of the carmine spider mite, Tetranychus cinnabarinus. J Insect Sci 10:1–9

    Article  Google Scholar 

  • Zeng CX, Wang JJ, Zeng ZP, Cao G (2006) Impact of Sublethal doses of imidacloprid on experimental population of Myzus persicae. Chin Agric Sci Bull 22:335–338

    Google Scholar 

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

    Google Scholar 

Download references

Acknowledgments

This study was supported by a Special Fund for Agro-scientific Research in the Public Interest “Integrative control technology program for organic chemicals pollution in farmland and agricultural products quality and safety” (201503107) from the Agricultural Ministry of China. AB was supported by the Italian Ministry of Education, University and Research (SIR project ENTOBIONANO, RBSI14I02A).

Author information

Authors and Affiliations

  1. Department of Entomology, China Agricultural University, 2 Yuanmingyuan West Road, Beijing, 100193, China

    SiYi Wang, YongFeng Qi, XueYan Shi & XiWu Gao

  2. INRA (French National Institute for Agricultural Research), UMR 1355-7254, Institute Sophia Agrobiotech, Univ. NiceSophia Antipolis, CNRS, 06903, Sophia Antipolis, France

    Nicolas Desneux

  3. Department of Agricultural, Food and Environment, University of Catania, Via Santa Sofia 100, 95123, Catania, Italy

    Antonio Biondi

Authors
  1. SiYi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. YongFeng Qi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Nicolas Desneux
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. XueYan Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Antonio Biondi
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. XiWu Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to XueYan Shi.

Ethics declarations

Conflicts of interest

The authors declared that they have no conflicts of interest to this work.

Ethics approval

No ethics approval was required for this research.

Additional information

Communicated by M. Traugott.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, S., Qi, Y., Desneux, N. et al. Sublethal and transgenerational effects of short-term and chronic exposures to the neonicotinoid nitenpyram on the cotton aphid Aphis gossypii . J Pest Sci 90, 389–396 (2017). https://doi.org/10.1007/s10340-016-0770-7

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10340-016-0770-7

Keywords

Search

Navigation