Skip to main content
SpringerLink
Log in

Flupyradifurone induces transgenerational hormesis effects in the cowpea aphid, Aphis craccivora

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

With low-dose stimulation and high-dose inhibition, insecticide-induced hormesis, a biphasic phenomenon, can contribute to pest resurgence. The cowpea aphid, Aphis craccivora (Koch) (Homoptera: Aphididae), is a vital insect that infests legume crops. Its hormesis of flupyradifurone has not been previously established. Age-stage two-sex life analysis is used to investigate the sublethal and transgenerational effects of flupyradifurone on two successive generations of A. craccivora. A leaf-dip bioassay method revealed high toxicity of flupyradifurone against A. craccivora, with lethal concentration 50% value (LC50) of 1.82 mg L−1 after 48 h exposure. Treatment of parent generation (F0) with LC10 and LC25 of flupyradifurone significantly increased the longevity and fecundity of the directly exposed adults. The results of transgenerational effects showed that the treatment of (F0) with LC25 induced significant hormetic effects in progeny generation (F1). Furthermore, flupyradifurone at LC25 significantly enhanced the biological traits, such as intrinsic rate of increase (r), finite rate of increase (λ), and net reproductive rate (R0) compared with the control. Similarly, both LC10 and LC25 induced a significant increase in the mean generation time T (d). Conversely, both treatments caused a significant decrease in the doubling time (DT). Data in the present study demonstrate that the exposure of (F0) to flupyradifurone at LC10 and LC25 enhanced longevity and fecundity in the directly exposed adults of A. craccivora, and induced transgenerational hormesis across the subsequent (F1) generation. These results should be taken into consideration when using flupyradifurone for controlling cowpea aphid.

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
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

All data generated during this study are included in this published article.

References

  • Agathokleous E, Brown PH, Calabrese EJ (2021) A gift from parent to offspring: transgenerational hormesis. Trends Plant Sci xx:2–4. https://doi.org/10.1016/j.tplants.2021.08.006

    Article  CAS  Google Scholar 

  • Atta B, Rizwan M, Sabir AM et al. (2021) Lethal and sublethal effects of clothianidin, imidacloprid and sulfoxaflor on the wheat aphid, Schizaphis graminum (Hemiptera: Aphididae) and its coccinellid predator, Coccinella septempunctata. Int J Trop Insect Sci 41:345–358. https://doi.org/10.1007/s42690-020-00212-w

    Article  Google Scholar 

  • Ayyanath M-M, 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  Google Scholar 

  • Bao H, Liu S, Gu J et al. (2009) Sublethal effects of four insecticides on the reproduction and wing formation of brown planthopper, Nilaparvata lugens. Pest Manag Sci 65:170–174. https://doi.org/10.1002/ps.1664

    Article  CAS  Google Scholar 

  • Bass C, Denholm I, Williamson MS, Nauen R (2015) The global status of insect resistance to neonicotinoid insecticides. Pestic Biochem Physiol 121:78–87

    Article  CAS  Google Scholar 

  • Blackman RL, Eastop VF (2006) Aphids on the world’s herbaceous plants and shrubs. 1. Host lists and keys. Wiley

  • Calabrese EJ (2005) Paradigm lost, paradigm found: the re-emergence of hormesis as a fundamental dose response model in the toxicological sciences. Environ Pollut 138:378–411

    Article  CAS  Google Scholar 

  • Calabrese EJ, Baldwin LA (1997) The dose determines the stimulation (and poison): development of a chemical hormesis database. Int J Toxicol 16:545–559

    Article  CAS  Google Scholar 

  • Chen GM, Chi H, Wang RC et al. (2018) Demography and uncertainty of population growth of conogethes punctiferalis (Lepidoptera: Crambidae) reared on five host plants with discussion on some life history statistics. J Econ Entomol 111:2143–2152. https://doi.org/10.1093/jee/toy202

    Article  Google Scholar 

  • Chen X, Ma K, Li F et al. (2016) Sublethal and transgenerational effects of sulfoxaflor on the biological traits of the cotton aphid, Aphis gossypii Glover (Hemiptera: Aphididae). Ecotoxicology 25:1841–1848. https://doi.org/10.1007/s10646-016-1732-9

    Article  CAS  Google Scholar 

  • Chi H (2020a) Probit-MSChart: a computer program for probit analysis. Available on: http://140.120.197.173/Ecology/products.htm

  • Chi H (2020b) TWOSEX-MS Chart: a computer program for the age-stage, two-sex life table analysis. Available on: http://140.120.197.173/Ecology/prod02.htm

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

    Google Scholar 

  • Chi H, Su H (2006) -stage, two-sex life tables of Aphidius gifuensis (Ashmead)(Hymenoptera: Braconidae) and its host Myzus persicae (Sulzer)(Homoptera: Aphididae) with mathematical. Environ Entomol 10–21. 0046-225X/06/0010Ð0021$04.00/0

  • Chi H, You M, Atlıhan R et al. (2020) Age-stage, two-sex life table: an introduction to theory, data analysis, and application. Entomol Gen 40:103–124. https://doi.org/10.1127/entomologia/2020/0936

    Article  Google Scholar 

  • Cho S-R, Koo H-N, Yoon C, Kim G-H (2011) Sublethal effects of flonicamid and thiamethoxam on green peach aphid, Myzus persicae and feeding behavior analysis. J Korean Soc Appl Biol Chem. https://doi.org/10.1007/bf03253177

  • Colares F, Michaud JP, Bain CL, Torres JB (2017) Relative toxicity of two aphicides to Hippodamia convergens (Coleoptera: Coccinellidae): implications for integrated management of sugarcane aphid, Melanaphis sacchari (Hemiptera: Aphididae). J Econ Entomol 110:52–58

    CAS  Google Scholar 

  • Coy MR, Bin L, Stelinski LL (2016) Reversal of insecticide resistance in Florida populations of Diaphorina citri (Hemiptera: Liviidae). Florida Entomol 99:26–32

    Article  Google Scholar 

  • Cui L, Yuan H, Wang Q et al. (2018) Sublethal effects of the novel cis-nitromethylene neonicotinoid cycloxaprid on the cotton aphid Aphis gossypii Glover (Hemiptera: Aphididae). Sci Rep 8:1–9. https://doi.org/10.1038/s41598-018-27035-7

    Article  CAS  Google Scholar 

  • Cutler GC (2013) Insects, insecticides and hormesis: evidence and considerations for study. Dose-Response 11:dose–response

  • Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106

    Article  CAS  Google Scholar 

  • Duke SO (2014) Hormesis with pesticides. Pest Manag Sci 70:10–1002

    Google Scholar 

  • Foster SP, Denholm I, Thompson R (2003) Variation in response to neonicotinoid insecticides in peach-potato aphids, Myzus persicae (Hemiptera: Aphididae). Pest Manag Sci Former Pestic Sci 59:166–173

    Article  CAS  Google Scholar 

  • Goodman D (1982) Optimal life histories, optimal notation, and the value of reproductive value. Am Nat 119:803–823

    Article  Google Scholar 

  • Hassan SA, de Veire M (2004) Compatibility of pesticides with biological control agents. Biocontrol Prot Cult 1:129–148

    Google Scholar 

  • Hullé M, Chaubet B, Turpeau E, Simon JC (2020) Encyclop’aphid: a website on aphids and their natural enemies. Entomol Gen 40:97–101. https://doi.org/10.1127/entomologia/2019/0867

    Article  Google Scholar 

  • Janmaat A, Borrow E, Matteoni J, Jones G (2011) Response of a red clone of Myzus persicae (Hemiptera: Aphididae) to sublethal concentrations of imidacloprid in the laboratory and greenhouse. Pest Manag Sci 67:719–724. https://doi.org/10.1002/ps.2113

    Article  CAS  Google Scholar 

  • Kerns DL, Stewart SD (2000) Sublethal effects of insecticides on the intrinsic rate of increase of cotton aphid. Entomol Exp Appl 94:41–49. https://doi.org/10.1023/A:1003972510397

    Article  CAS  Google Scholar 

  • Liang PZ, Ma KS, Chen XW et al. (2018) Toxicity and sublethal effects of flupyradifurone, a novel butenolide insecticide, on the development and fecundity of Aphis gossypii (Hemiptera: Aphididae). J Econ Entomol 112:852–858. https://doi.org/10.1093/jee/toy381

    Article  CAS  Google Scholar 

  • Lu Y-H, Zheng X-S, Gao X-W (2016) Sublethal effects of imidacloprid on the fecundity, longevity, and enzyme activity of Sitobion avenae (Fabricius) and Rhopalosiphum padi (Linnaeus). Bull Entomol Res 106:551–559

    Article  CAS  Google Scholar 

  • Maggi VL, Leigh TF (1983) Fecundity response of the twospotted spider mite to cotton treated with methyl parathion or phosphoric acid1. J Econ Entomol 76:20–25. https://doi.org/10.1093/jee/76.1.20

    Article  CAS  Google Scholar 

  • Mokbel E-S, Huesien A (2020) Sublethal effects of emamectin benzoate on life table parameters of the cotton leafworm, Spodoptera littoralis (Boisd.). Bull Natl Res Cent 44: https://doi.org/10.1186/s42269-020-00412-x

  • Mokbel EMS, Hussain HBH, Rasha AZ (2020) Sublethal effects of malathion on biology and population growth of Khapra Beetle, Trogoderma granarium everts (Coleoptera: Dermestidae). Egypt Acad J Biol Sci 13:57–72. https://eajbsa.journals.ekb.eg/article_102086.html

  • Moores GD, Gao X, 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 

  • Morse JG, Zareh N (1991) Pesticide-induced hormoligosis of citrus thrips (Thysanoptera: Thripidae) fecundity. J Econ Entomol 84:1169–1174

    Article  CAS  Google Scholar 

  • Nauen R, Jeschke P, Velten R et al. (2015) Flupyradifurone: a brief profile of a new butenolide insecticide. Pest Manag Sci 71:850–862

    Article  CAS  Google Scholar 

  • Qu Y, Ullah F, Luo C et al. (2020) Sublethal effects of beta-cypermethrin modulate interspecific interactions between specialist and generalist aphid species on soybean. Ecotoxicol Environ Saf 206:111302. https://doi.org/10.1016/j.ecoenv.2020.111302

    Article  CAS  Google Scholar 

  • Qu Y, Xiao D, Li J et al. (2015) Sublethal and hormesis effects of imidacloprid on the soybean aphid Aphis glycines. Ecotoxicology 24:479–487

    Article  CAS  Google Scholar 

  • Qu Y, Xiao D, Liu J et al. (2017) Sublethal and hormesis effects of beta-cypermethrin on the biology, life table parameters and reproductive potential of soybean aphid Aphis glycines. Ecotoxicology 1002–1009. https://doi.org/10.1007/s10646-017-1828-x

  • Radha R (2013) Comparative studies on the Effectiveness of Pesticides for Aphid control in Cowpea. Res J Agric For Sci ISSN 2320:6063

  • Ricupero M, Desneux N, Zappalà L, Biondi A (2020) Target and non-target impact of systemic insecticides on a polyphagous aphid pest and its parasitoid. Chemosphere 247:. https://doi.org/10.1016/j.chemosphere.2019.125728

  • Rix RR, Ayyanath MM, Christopher Cutler G (2016) Sublethal concentrations of imidacloprid increase reproduction, alter expression of detoxification genes, and prime Myzus persicae for subsequent stress. J Pest Sci (2004) 89:581–589. https://doi.org/10.1007/s10340-015-0716-5

    Article  Google Scholar 

  • Rix RR, Cutler GC (2018) Does multigenerational exposure to hormetic concentrations of imidacloprid precondition aphids for increased insecticide tolerance? Pest Manag Sci 74:314–322. https://doi.org/10.1002/ps.4731

    Article  CAS  Google Scholar 

  • Shang J, Yao Y, Zhu X et al. (2021) Evaluation of sublethal and transgenerational effects of sulfoxaflor on Aphis gossypii via life table parameters and 16S rRNA sequencing. Pest Manag Sci. https://doi.org/10.1002/ps.6385

  • Sial MU, Zhao Z, Zhang L et al. (2018) Evaluation of Insecticides induced hormesis on the demographic parameters of Myzus persicae and expression changes of metabolic resistance detoxification genes. Sci Rep 8: https://doi.org/10.1038/s41598-018-35076-1

  • Siviter H, Muth F (2020) Do novel insecticides pose a threat to beneficial insects? Proc R Soc B Biol Sci 287: https://doi.org/10.1098/rspb.2020.1265

  • Smith HA, Giurcanu MC (2013) Residual effects of new insecticides on egg and nymph densities of Bemisia tabaci (Hemiptera: Aleyrodidae). Florida Entomol 504–511

  • Smith HA, Nagle CA, MacVean CA, McKenzie CL (2016) Susceptibility of Bemisia tabaci MEAM1 (Hemiptera: Aleyrodidae) to imidacloprid, thiamethoxam, dinotefuran and flupyradifurone in South Florida. Insects 7:57. https://doi.org/10.3390/insects7040057

    Article  Google Scholar 

  • Suárez-López YA, Hatem AE, Aldebis HK, Vargas-Osuna E (2020) Lethal and sublethal effects of lufenuron on the predator Chrysoperla carnea (Stephens) (Neuroptera: Chrysopidae). Crop Prot 135: https://doi.org/10.1016/j.cropro.2020.105217

  • Tan Y, Biondi A, Desneux N, Gao XW (2012) Assessment of physiological sublethal effects of imidacloprid on the mirid bug Apolygus lucorum (Meyer-Dü r). Ecotoxicology 21:1989–1997. https://doi.org/10.1007/s10646-012-0933-0

    Article  CAS  Google Scholar 

  • Tan Y, Jia B, Foster SP et al. (2021) Sublethal and transgenerational effects of lambda-cyhalothrin on the mirid bugs Lygus pratensis Linnaeus and Polymerus cognatus Fieber. Crop Prot 139:105354. https://doi.org/10.1016/j.cropro.2020.105354

    Article  CAS  Google Scholar 

  • Tang Q, Ma K, Chi H et al. (2019) Transgenerational hormetic effects of sublethal dose of flupyradifurone on the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). PLoS One 14:1–16. https://doi.org/10.1371/journal.pone.0208058

    Article  CAS  Google Scholar 

  • Tang Q, Xiang M, Hu H et al. (2015) Evaluation of sublethal effects of Sulfoxaflor on the Green Peach Aphid (Hemiptera: Aphididae) Using Life Table Parameters. J Econ Entomol 108:2720–2728. https://doi.org/10.1093/jee/tov221

    Article  CAS  Google Scholar 

  • Tuan SJ, Lee CC, Chi H (2014a) Erratum to Population and damage projection of Spodoptera litura (F.) on peanuts (Arachis hypogaea L.) under different conditions using the age-stage, two-sex life table [Pest Manag Science, 70 (2014), 805-813, 10.1002/ps.3618] Pest Manag Sci 70:1936. https://doi.org/10.1002/ps.3920

    Article  CAS  Google Scholar 

  • Tuan SJ, Lee CC, Chi H (2014b) Population and damage projection of Spodoptera litura (F.) on peanuts (Arachishypogaea L.) under different conditions using the age-stage, two-sex life table. Pest Manag Sci 70:805–813. https://doi.org/10.1002/ps.3618

    Article  CAS  Google Scholar 

  • Ullah F, Gul H, Desneux N et al. (2019a) Imidacloprid-induced hormesis effects on demographic traits of the melon aphid, aphis gossypii. Entomol Gen 39:325–337. https://doi.org/10.1127/entomologia/2019/0892

    Article  Google Scholar 

  • Ullah F, Gul H, Desneux N et al. (2019b) Acetamiprid-induced hormetic effects and vitellogenin gene (Vg) expression in the melon aphid, aphis gossypii. Entomol Gen 39:259–270. https://doi.org/10.1127/entomologia/2019/0887

    Article  Google Scholar 

  • Ullah F, Gul H, Tariq K et al. (2020) Thiamethoxam induces transgenerational hormesis effects and alteration of genes expression in Aphis gossypii. Pestic Biochem Physiol 165:104557. https://doi.org/10.1016/j.pestbp.2020.104557

    Article  CAS  Google Scholar 

  • Wang SY, Qi YF, Desneux N et al. (2017) Sublethal and transgenerational effects of short-term and chronic exposures to the neonicotinoid nitenpyram on the cotton aphid Aphis gossypii. J Pest Sci (2004). https://doi.org/10.1007/s10340-016-0770-7

  • Wei X, Pan Y, Xin X et al. (2017) Cross-resistance pattern and basis of resistance in a thiamethoxam-resistant strain of Aphis gossypii Glover. Pestic. Biochem. Physiol. 138:91–96

    Article  CAS  Google Scholar 

  • Xin JJ, Yu WX, Yi XQ et al. (2019) Sublethal effects of sulfoxaflor on the fitness of two species of wheat aphids, Sitobion avenae (F.) and Rhopalosiphum padi (L.). J Integr Agric 18:1613–1623. https://doi.org/10.1016/S2095-3119(18)62094-5

    Article  CAS  Google Scholar 

  • Yuan HB, Li JH, Liu YQ et al. (2017) Lethal, sublethal and transgenerational effects of the novel chiral neonicotinoid pesticide cycloxaprid on demographic and behavioral traits of Aphis gossypii (Hemiptera: Aphididae). Insect Sci 24:743–752. https://doi.org/10.1111/1744-7917.12357

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors pay great thanks to Prof. Dr. Hsin Chi (Laboratory of Theoretical and Applied Ecology, Department of Entomology, National Chung Hsing University, Taichung, Taiwan, Republic of China) for his valuable comments and suggestions which helped us to improve the manuscript.

Author contributions:

EAF was involved in designing the study; investigation; methodology; and writing of the original draft. SANE contributed to the experimental work. EMSM was contributed to designing the study, conducting the experimental part, writing of the orginal draft, and analyzing the obtained data. All authors read and approved the final manuscript.

Author information

Authors and Affiliations

  1. Department of Bioassay, Central Agricultural Pesticides Laboratory, Agricultural Research Center, 12618, Giza, Egypt

    Eman A. Fouad & Sherifa A. N. El-Sherif

  2. Department of Standard Rearing, Central Agricultural Pesticides Laboratory, Agricultural Research Center, 12618, Giza, Egypt

    El-Sayed M. S. Mokbel

Authors
  1. Eman A. Fouad
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sherifa A. N. El-Sherif
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. El-Sayed M. S. Mokbel
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to El-Sayed M. S. Mokbel.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors. The authors agree with the publication of the manuscript in this form.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fouad, E.A., El-Sherif, S.A.N. & Mokbel, ES.M.S. Flupyradifurone induces transgenerational hormesis effects in the cowpea aphid, Aphis craccivora. Ecotoxicology 31, 909–918 (2022). https://doi.org/10.1007/s10646-022-02556-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-022-02556-0

Keywords

Search

Navigation