Abstract
Bradysia odoriphaga is a major insect pest that infests Chinese chive in northern China. Clothianidin is a second-generation neonicotinoid insecticide that is commonly used against B. odoriphaga. In this study, the effect of sublethal clothianidin concentrations (LC5 and LC10) on key biological characteristics of B. odoriphaga was investigated using an age-stage, two-sex life table method. Bioassays results showed that clothianidin exhibited high toxicity against B. odoriphaga with LC50 of 1.898 mg L−1 following 24 h exposure. The developmental duration of larvae was significantly increased when exposed to the LC5 (0.209 mg L−1) and LC10 (0.340 mg L−1) of clothianidin. No significant effects were observed on the pupal stage, adult pre-oviposition period (APOP), total pre-oviposition period (TPOP), and mean longevities of male and female. The oviposition period and fecundity of B. odoriphaga were reduced in clothianidin-treated groups. Moreover, key demographic parameters, including the intrinsic rate of increase (r), finite rate of increase (λ), and net reproductive rate (R0), were significantly decreased by the LC5 and LC10 of clothianidin, while no effects were noted on mean generation time (T). Overall, this study showed that sublethal concentrations of clothianidin have a detrimental effect on B. odoriphaga developmental period, fecundity, and life table parameters. Therefore, clothianidin has the potential to suppress the population of B. odoriphaga even at sublethal concentrations.
Similar content being viewed by others
Data availability
All data analyzed during this study are included in this published article.
References
Akca I, Ayvaz T, Yazici E, Smith CL, Chi H (2015) Demography and population projection of Aphis fabae (Hemiptera: Aphididae): with additional comments on life table research criteria. J Econ Entomol 108(4):1466–1478
Armstrong JS, Peairs FB, Pilcher SD, Russell CC (1993) The effect of planting time insecticides and liquid fertilizer on the Russian wheat aphid (Homoptera: Aphididae) and the lesion nematode (Pratylenchus thornei) on winter wheat. J Kans Entomol Soc 66: 69–74
Arrington AE, Kennedy GG, Abney MR (2016) Applying insecticides through drip irrigation to reduce wireworm (Coleoptera: Elateridae) feeding damage in sweet potato. Pest Manag Sci 72(6):1133–1140
Biondi A, Desneux N, Siscaro G, Zappalà L (2012) 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(7):803–812
Chen C, Zhao Y, Li H, Zhang P, Mu W, Liu F (2014) Biological activity of benzothiazole against Bradysia odoriphaga (Diptera: Sciaridae) at different developmental stages. Acta Entomol Sin 57(1):45–51
Chen G-M, Chi H, Wang R-C, Wang Y-P, Xu Y-Y, Li X-D, Yin P, Zheng F-Q (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(5):2143–2152
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(4):741–751
Chi H (1988) Life-table analysis incorporating both sexes and variable development rates among individuals. Environ Entomol 17(1):26–34
Chi H (2018) TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. http://140.120.197.173/Ecology/Download/Twosex-MSChart-exe-B200000.rar
Chi H (2020) TWOSEX-MSChart: a computer program for the age-stage, two-sex life table analysis. http://140.120.197.173/ecology/Download/TWOSEX-MSChart-B100000.rar
Chi H, Liu H (1985) Two new methods for the study of insect population ecology. Bull Inst Zool Acad Sin 24(2):225–240
Chi H, Su H-Y (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(1):10–21
Chi H, Yang T-C (2003) Two-sex life table and predation rate of Propylaea japonica Thunberg (Coleoptera: Coccinellidae) fed on Myzus persicae (Sulzer)(Homoptera: Aphididae). Environ Entomol 32(2):327–333
Chi H, You M, Atlıhan R, Smith CL, Kavousi A, Özgökçe MS, Güncan A, Tuan S-J, Fu J-W, Xu Y-Y, Zheng F-Q, Ye B-H, Chu D, Yu Y, Gharekhani G, Saska P, Gotoh T, Schneider MI, Bussaman P, Gökçe A, Liu T-X (2020) Age-stage, two-sex life table: an introduction to theory, data analysis, and application. Entomol Gen 40(2):102–123. https://doi.org/10.1127/entomologia/2020/0936
Cutler GC (2013) Insects, insecticides and hormesis: evidence and considerations for study. Dose-Response 11(2). https://doi.org/10.2203/dose-response.12-008.Cutler
Decourtye A, Henry M, Desneux N (2013) Overhaul pesticide testing on bees. Nature 497(7448):188–188. https://doi.org/10.1038/497188a
Deligeorgidis NP, Kavallieratos NG, Malesios C, Sidiropoulos G, Deligeorgidis PN, Benelli G, Papanikolaou NE (2019) Evaluation of combined treatment with mineral oil, fenoxycarb and chlorpyrifos against Cydia pomonella, Phyllonorycter blancardella and Synanthedon myopaeformis in apple orchards. Entomol Gen 39:117–126
Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106
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
Desneux N, Fauvergue X, Dechaume-Moncharmont F-X, Kerhoas L, Ballanger Y, Kaiser L (2005) Diaeretiella rapae limits Myzus persicae populations after applications of deltamethrin in oilseed rape. J Econ Entomol 98(1):9–17
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
Ding Q, Xu X, Wang X, Ullah F, Gao X, Song D (2021) Characterization and functional analysis of two acetylcholinesterase genes in Bradysia odoriphaga Yang et Zhang (Diptera: Sciaridae). Pestic Biochem Physiol 104807
Efron B, Tibshirani R (1993) An introduction to the Bootstrap. Chapman and Hall. Inc, New York, NY, p 914
Feng H, Zheng F (1987) Studies of the occurrence and control of Bradysia odoriphaga Yang et Zhang. J Shandong Agric Univ 18:71–80
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). Ecotoxicol 22:1063–1071
Gong Y, Shi X, Desneux N, Gao X (2016) Effects of spirotetramat treatments on fecundity and carboxylesterase expression of Aphis gossypii Glover. Ecotoxicology 25(4):655–663
Goodman D (1982) Optimal life histories, optimal notation, and the value of reproductive value. Am Nat 119(6):803–823
Guedes R, Smagghe G, Stark J, Desneux N (2016) Pesticide-induced stress in arthropod pests for optimized integrated pest management programs. Annu Rev Entomol 61:43–62
Gul H, Ullah F, Biondi A, Desneux N, Qian D, Gao X, Song D (2019) Resistance against clothianidin and associated fitness costs in the chive maggot, Bradysia odoriphaga. Entomol Gen 39(2):81–92. https://doi.org/10.1127/entomologia/2019/0861
Guo L, Desneux N, Sonoda S, Liang P, Han P, Gao X-W (2013) Sublethal and transgenerational effects of chlorantraniliprole on biological traits of the diamondback moth, Plutella xylostella L. Crop Prot 48:29–34
Hafeez M, Jan S, Nawaz M, Ali E, Ali B, Qasim M, Fernández-Grandon GM, Shahid M, Wang M (2019) Sub-lethal effects of lufenuron exposure on spotted bollworm Earias vittella (Fab): key biological traits and detoxification enzymes activity. Environ Sci Pollut Res 26(14):14300–14312
Haddi K, Turchen LM, Viteri Jumbo LO, Guedes RN, Pereira EJ, Aguiar RW, Oliveira EE (2020) Rethinking biorational insecticides for pest management: unintended effects and consequences. Pest Manag Sci 76(7):2286–2293
Huang Y-B, Chi H (2011) The age-stage, two-sex life table with an offspring sex ratio dependent on female age. J Agric For 60:337–345
Jam NA, Saber M (2018) Sublethal effects of imidacloprid and pymetrozine on the functional response of the aphid parasitoid, Lysiphlebus fabarum. Entomol Gen 38(2):173–190
Jeschke P, Moriya K, Lantzsch R, Seifert H, Lindner W, Jelich K, Gohrt A, Beck M, Etzel W (2001) Thiacloprid (Bay YRC 2894)—a new member of the chloronicotinyl insecticide (CNI) family. Pflanzenschutz Nachrichten-Bayer 54:147–160
Jeschke P, Nauen R (2008) Neonicotinoids—from zero to hero in insecticide chemistry. Pest Manag Sci 64(11):1084–1098
Jiang J, Cao H, Zhang R, Zhang M, Li S (2004) Effect of organophosphorous insecticides on Chinese chive insect pests and their degradation by pesticide-degrading bacterium. J Appl Ecol 15(8):1459–1462
Kumar U, Berliner J, Adak T, Rath PC, Dey A, Pokhare SS, Jambhulkar NN, Panneerselvam P, Kumar A, Mohapatra SD (2017) Non-target effect of continuous application of chlorpyrifos on soil microbes, nematodes and its persistence under sub-humid tropical rice-rice cropping system. Ecotoxicol Environ Saf 135:225–235
Li H-J, He X-K, Zeng A-J, Liu Y-J, Jiang S-R (2007) Bradysia odoriphaga copulatory behavior and evidence of a female sex pheromone. J Agric Urban Entomol 24(1):27–35
Li W, Lu Z, Li L, Yu Y, Dong S, Men X, Ye B (2018) Sublethal effects of imidacloprid on the performance of the bird cherry-oat aphid Rhopalosiphum padi. PLoS ONE 13(9):e0204097
Lu Q, Zhang W, Guo W, Zhang Y (2006) A preliminary study on distributing phase and sampling methods of Bradysia odoriphaga larva in Chinese chive field. Acta Agric Boreali-Occident Sin 15(2):75–77
Lu Y, Wu K, Jiang Y, Guo Y, Desneux N (2012) Widespread adoption of Bt cotton and insecticide decrease promotes biocontrol services. Nature 487(7407):362
Luo C, Li D, Qu Y, Zhao H, Hu Z (2018) Indirect effects of chemical hybridization agent SQ-1 on clones of the wheat aphid Sitobion avenae. Entomol Gen 38(1):61–71
Ma J, Chen S, Moens M, Han R, De Clercq P (2013) Efficacy of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) against the chive gnat, Bradysia odoriphaga. J Pest Sci 86(3):551–561
Magalhaes LC, French BW, Hunt TE, Siegfried BD (2007) Baseline susceptibility of western corn rootworm (Coleoptera: Chrysomelidae) to clothianidin. J Appl Entomol 131(4):251–255
Mei ZX (2003) Studies on biological characteristics and cold hardiness of Bradysia ordoriphaga. Master, Northwest Ace-tech University of Agriculture and Forestry
Mohammed AAA, Desneux N, Fan Y, Han P, Ali A, Song D, Gao X-W (2018) Impact of imidacloprid and natural enemies on cereal aphids: integration or ecosystem service disruption? Entomol Gen 37(1):47–61
Pan H, Liu Y, Liu B, Lu Y, Xu X, Qian X, Wu K, Desneux N (2014) Lethal and sublethal effects of cycloxaprid, a novel cis-nitromethylene neonicotinoid insecticide, on the mirid bug Apolygus lucorum. J Pest Sci 87(4):731–738
Passos LC, Soares MA, Collares LJ, Malagoli I, Desneux N, Carvalho GA (2018) Lethal, sublethal and transgenerational effects of insecticides on Macrolophus basicornis, predator of Tuta absoluta. Entomol Gen 38:127–143
Qu Y, Xiao D, Liu J, Chen Z, Song L, Desneux N, Benelli G, Gao X, Song D (2017) Sublethal and hormesis effects of beta-cypermethrin on the biology, life table parameters and reproductive potential of soybean aphid Aphis glycines. Ecotoxicol 26:1002–1009
Qu Y, Xiao D, Li J, Chen Z, Biondi A, Desneux N, Gao X, Song D (2015) Sublethal and hormesis effects of imidacloprid on the soybean aphid Aphis glycines. Ecotoxicol 24(3):479–487
Rahman T, Broughton S (2016) Evaluation of thiacloprid and clothianidin (neonicotinoids) as alternative to fenthion (organophosphate) for control of Mediterranean fruit fly (Diptera: Tephritidae) in deciduous fruit orchards. Crop Prot 90:170–176
Sâmia RR, Gontijo PC, Oliveira RL, Carvalho GA (2019) Sublethal and transgenerational effects of thiamethoxam applied to cotton seed on Chrysoperla externa and Harmonia axyridis. Pest Manag Sci 75(3):694–701
Schneider M, 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(10):1451–1455
Shahout HA, Xu J-X, Qiao J, Jia Q-d (2011) Sublethal effects of methoxyfenozide, in comparison to chlorfluazuron and beta-cypermethrin, on the reproductive characteristics of common cutworm Spodoptera litura (Fabricius)(Lepidoptera: Noctuidae). J Entomol Res Soc 13(3):53–63
Soares MA, Passos LC, Campos MR, Collares LJ, Desneux N, Carvalho GA (2019) Side effects of insecticides commonly used against Tuta absoluta on the predator Macrolophus basicornis. J Pest Sci 92:1447–1456
Stark JD, Banks JE (2003) Population-level effects of pesticides and other toxicants on arthropods. Annu Rev Entomol 48(1):505–519
Taning CNT, Vanommeslaeghe A, Smagghe G (2019) With or without foraging for food, field-realistic concentrations of sulfoxaflor are equally toxic to bumblebees (Bombus terrestris). Entomol Gen 39(2):151–155. https://doi.org/10.1127/entomologia/2019/0784
Tomizawa M, Casida JE (2005) Neonicotinoid insecticide toxicology: mechanisms of selective action. Annu Rev Pharmacol Toxicol 45:247–268
Tuan SJ, Lee CC, Chi H (2014) 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 Sci 70(5):805–813
Ullah F, Gul H, Desneux N, Gao X, Song D (2019a) Imidacloprid-induced hormesis effects on demographic traits of the melon aphid, Aphis gossypii. Entomol Gen 39(3–4):325–337. https://doi.org/10.1127/entomologia/2019/0892
Ullah F, Gul H, Desneux N, Qu Y, Xiao X, Khattak AM, Gao X, Song D (2019b) Acetamiprid-induced hormetic effects and vitellogenin gene (Vg) expression in the melon aphid, Aphis gossypii. Entomol Gen 39(3–4):259–270. https://doi.org/10.1127/entomologia/2019/0887
Ullah F, Gul H, Desneux N, Said F, Gao X, Song D (2020a) Fitness costs in chlorfenapyr-resistant populations of the chive maggot, Bradysia odoriphaga. Ecotoxicology 29(4):407–416. https://doi.org/10.1007/s10646-020-02183-7
Ullah F, Gul H, Desneux N, Tariq K, Ali A, Gao X, Song D (2019c) Clothianidin-induced sublethal effects and expression changes of vitellogenin and ecdysone receptors genes in the melon aphid, Aphis gossypii. Entomol Gen 39(2):137–149. https://doi.org/10.1127/entomologia/2019/0865
Ullah F, Gul H, Tariq K, Desneux N, Gao X, Song D (2020b) Acetamiprid resistance and fitness costs of melon aphid, Aphis gossypii: an age-stage, two-sex life table study. Pestic Biochem Physiol 104729. https://doi.org/10.1016/j.pestbp.2020.104729
Ullah F, Gul H, Tariq K, Desneux N, Gao X, Song D (2020c) 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
Van Herk W, Vernon R, Tolman J, Ortiz Saavedra H (2008) Mortality of a wireworm, Agriotes obscurus (Coleoptera: Elateridae), after topical application of various insecticides. J Econ Entomol 101(2):375–383
Varikou K, Garantonakis N, Birouraki A (2019) Exposure of Bombus terrestris L. to three different active ingredients and two application methods for olive pest control. Entomol Gen 39:53–60
Wang C, Liu J, Liu Z, Xue M (2014) Occurrence characteristics and control measures of Bradysia odoriphaga on leek in winter facilities and open field cultivation. North Hortic 22:113–117
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 on the cotton aphid Aphis gossypii. J Pest Sci 90:389–396
Yu X, Rao G, Liao H, Li X (2003) Insecticidal activities of several botanical secondary metabolites against larvae of Bradysia odoriphaga Yang et Zhang. Jiangsu J Agric Sci 19:228–232
Zeng X, He Y, Wu J, Tang Y, Gu J, Ding W, Zhang Y (2016) Sublethal effects of cyantraniliprole and imidacloprid on feeding behavior and life table parameters of Myzus persicae (Hemiptera: Aphididae). J Econ Entomol 109(4):1595–1602
Zhang P, Chen C, Li H, Liu F, Mu W (2014a) Selective toxicity of seven neonicotinoid insecticides to Bradysia odoriphaga and Eisenia foetida. Acta Phytophylacica Sin 41:79–86
Zhang P, He M, Zhao Y, Ren Y, Wei Y, Mu W, Liu F (2016) Dissipation dynamics of clothianidin and its control efficacy against Bradysia odoriphaga Yang and Zhang in Chinese chive ecosystems. Pest Manag Sci 72(7):1396–1404
Zhang P, Liu F, Mu W, Wang Q, Li H, Chen C (2014b) Life table study of the effects of sublethal concentrations of thiamethoxam on Bradysia odoriphaga Yang and Zhang. Pestic Biochem Physiol 111:31–37
Zhang P, Zhang X, Zhao Y, Ren Y, Mu W, Liu F (2015a) Efficacy of granular applications of clothianidin and nitenpyram against Aphis gossypii (Glover) and Apolygus lucorum (Meyer-Dür) in cotton fields in China. Crop Prot 78:27–34
Zhang P, Zhao Y-H, Wang Q-H, Mu W, Liu F (2017) Lethal and sublethal effects of the chitin synthesis inhibitor chlorfluazuron on Bradysia odoriphaga Yang and Zhang (Diptera: Sciaridae). Pestic Biochem Physiol 136:80–88
Zhang P, Zhao Y, Han J, Zhai Y, Mu W, Liu F (2015b) Control effects of thiamethoxam and clothianidin against Bradysia odoriphaga with different application methods. J Plant Prot 42:645–650
Zhao Y, Wang Q, Ding J, Wang Y, Zhang Z, Liu F, Mu W (2018) Sublethal effects of chlorfenapyr on the life table parameters, nutritional physiology and enzymatic properties of Bradysia odoriphaga (Diptera: Sciaridae). Pestic Biochem Physiol 148:93–102
Zhao Y, Wang Q, Wang Y, Zhang Z, Wei Y, Liu F, Zhou C, Mu W (2017) Chlorfenapyr, a potent alternative insecticide of phoxim to control Bradysia odoriphaga (Diptera: Sciaridae). J Agric Food Chem 65(29):5908–5915
Zhang Y, Guo L, Atlihan R, Chi H, Chu D (2019) Demographic analysis of progeny fitness and timing of resurgence of Laodelphax striatellus after insecticides exposure. Entomol Gen 39:221–230
Zhao Y, Zhang P, Zhai Y, Chen C, Wang Q, Han J, Zhang Z, Liu F, Mu W (2016) Sublethal concentration of benzothiazole adversely affect development, reproduction and longevity of Bradysia odoriphaga (Diptera: Sciaridae). Phytoparasitica 44(1):115–124
Funding
Funding was provided by the National Key Research and Development Program of China (2016YFD0200500) and the National Natural Science Foundation of China (31272077).
Author information
Authors and Affiliations
Contributions
HG, FU, ND, and DS designed the experiment. HG and FU performed the experiments and analyzed the data. HG, FU, KT, MH, and ND wrote and reviewed the manuscript. DS and XG contributed to the reagents/materials. All authors read and approved the manuscript.
Corresponding authors
Ethics declarations
Conflict of interest
The authors declare no competing interests.
Ethical approval
This article does not describe any studies involving human participants performed by the authors. All applicable international, national and/or institutional guidelines for the care and use of animals were followed.
Additional information
Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Gul, H., Ullah, F., Hafeez, M. et al. Sublethal concentrations of clothianidin affect fecundity and key demographic parameters of the chive maggot, Bradysia odoriphaga. Ecotoxicology 30, 1150–1160 (2021). https://doi.org/10.1007/s10646-021-02446-x
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-021-02446-x