Abstract
The chive maggot, Bradysia odoriphaga (Yang and Zhang) is an economically important insect pest, affecting many key vegetables, including Chinese chive, especially in northern China. Chlorfenapyr, a halogenated pyrrole insecticide that interferes with mitochondrial oxidative phosphorylation is widely used against B. odoriphaga. In this study, we evaluated selection-induced resistance to chlorfenapyr and fitness costs in B. odoriphaga. The results showed that B. odoriphaga developed 43.32-fold resistance after continuous exposure to chlorfenapyr for over 10 consecutive generations. The life-history traits of chlorfenapyr-resistant and susceptible strains were compared using age-stage, two-sex life table approach. No significant effects were observed on the longevity and pre-adult period. However, reduction in the total pre-oviposition period (TPOP) and fecundity (eggs/female) were observed in the resistant strain. Moreover, the demographic parameters such as intrinsic rate of increase (r), net reproductive rate (R0) and finite rate of increase (λ) were also decreased significantly in the resistant strain compared to the susceptible strain. These results showed the potential of B. odoriphaga to develop resistance against chlorfenapyr under continuous selection pressure. Furthermore, there was a fitness cost linked with chlorfenapyr resistance in B. odoriphaga. We conclude that a better knowlegde on the trade-off at play between resistance degree and fitness cost could be crucial for developing further management of B. odoriphaga in China.
Similar content being viewed by others
References
Abbas N, Shad SA, Razaq M (2012) Fitness cost, cross resistance and realized heritability of resistance to imidacloprid in Spodoptera litura (Lepidoptera: Noctuidae). Pestic Biochem Physiol 103(3):181–188
Abbas N, Shah RM, Shad SA, Azher F (2016) Dominant fitness costs of resistance to fipronil in Musca domestica Linnaeus (Diptera: Muscidae). Vet Parasitol 226:78–82
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
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
Black BC, Hollingworth RM, Ahammadsahib KI, Kukel CD, Donovan S (1994) Insecticidal action and mitochondrial uncoupling activity of AC-303,630 and related halogenated pyrroles. Pestic Biochem Physiol 50(2):115–128
Cao G, Feng H, Guo F, Wu K, Li X, Liang G, Desneux N (2014) Quantitative analysis of fitness costs associated with the development of resistance to the Bt Toxin Cry1Ac in Helicoverpa armigera. Scientific Reports 4(1):5629. https://doi.org/10.1038/srep05629
Cao G, Han Z (2006) Tebufenozide resistance selected in Plutella xylostella and its cross‐resistance and fitness cost. Pest Manag Sci 62(8):746–751
Carriere Y, Deland J-P, Roff D, Vincent C (1994) Life-history costs associated with the evolution of insecticide resistance. Proceedings of the Royal Society of London Series B, Biological Sciences 258 (1351):35–40
Carrière Y, Ellers-Kirk C, Biggs R, Higginson DM, Dennehy TJ, Tabashnik BE (2004) Effects of gossypol on fitness costs associated with resistance to Bt cotton in pink bollworm. J Econ Entomol 97(5):1710–1718
Chen C, Liu Y, Shi X, Desneux N, Han P, Gao X (2017a) Elevated carboxylesterase activity contributes to the lambda-cyhalothrin insensitivity in quercetin fed Helicoverpa armigera (Hübner). PLoS ONE 12(8):e0183111. https://doi.org/10.1371/journal.pone.0183111
Chen C, Shan T, Liu Y, Shi X, Gao X (2018a) Identification of a novel cytochrome P450 CYP3356A1 linked with insecticide detoxification in Bradysia odoriphaga. Pest Manag Sci 75:1006–1013
Chen C, Shi X, Desneux N, Han P, Gao X (2017b) Detection of insecticide resistance in Bradysia odoriphaga Yang et Zhang (Diptera: Sciaridae) in China. Ecotoxicology 26(7):868–875
Chen C, Wang C, Liu Y, Shi X, Gao X (2018b) Transcriptome analysis and identification of P450 genes relevant to imidacloprid detoxification in Bradysia odoriphaga. Sci Rep 8(1):2564
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
Chi H (2018) TWOSEX-MS chart: 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, You MS, Atlihan R, Smith CL, Kavousi A, Ozgokçe MS, Guncan A, Tuan SJ, Fu JW, Xu YY, Zheng FQ, Ye BH, Chu D, Yu Y, Gharekhani G, Saska P, Gotoh T, Schneider MI, Bussaman P, Gokçe A, Liu TX (2020) Age-stage, two-sex life table: an introduction to theory, data analysis, and application. Entomol Gen. https://doi.org/10.1127/entomologia/2020/0936
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
Dang Z, Dong J, Gao Z, Jia H, Zhang K, Pan W (2001) Biology and injury of Bradysia odoriphaga on leek in different types of cultivation. J Agric Univ Hebei 24:65–68
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(2):117–126
Desneux N, Decourtye A, Delpuech J-M (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106
Ejaz M, Afzal MBS, Shabbir G, Serrão JE, Shad SA, Muhammad W (2017) Laboratory selection of chlorpyrifos resistance in an Invasive Pest, Phenacoccus solenopsis (Homoptera: Pseudococcidae): Cross-resistance, stability and fitness cost. Pestic Biochem Physiol 137:8–14
Ejaz M, Ali Shad S (2017) Spirotetramat resistance selected in the Phenacoccus solenopsis (Homoptera: Pseudococcidae): cross-resistance patterns, stability, and fitness costs analysis. J Econ Entomol 110(3):1226–1234
Fan Y, Kang Z, Wang Z, Campos M, Desneux N, Shi X (2018) Quercetin and paraoxon induction of hydrolase activity in Helicoverpa armigera and malathion-susceptible and resistant Musca domestica. Entomol Gen 38(2):157–171
Feng H, Zheng F (1987) Studies of the occurrence and control of Bradysia odoriphaga Yang et Zhang. J Shandong Agric Univ 18:71–80
Finney D (1971) Probit analysis. Cambridge University Press, London, p 333
Fu B, Li Q, Qiu H, Tang L, Zeng D, Liu K, Gao Y (2018) Resistance development, stability, cross‐resistance potential, biological fitness and biochemical mechanisms of spinetoram resistance in Thrips hawaiiensis (Thysanoptera: Thripidae). Pest Manag Sci 74(7):1564–1574
Gao H, Zhai Y, Wang W, Chen H, Zhou X, Zhuang Q, Yu Y, Li R (2016) Transcriptome analysis and discovery of genes relevant to development in Bradysia odoriphaga at three developmental stages. PLoS ONE 11(2):e0146812
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, Liu S, Jan S, Ali B, Shahid M, Fernández-Grandon GM, Nawaz M, Ahmad A, Wang M (2018) Gossypol-induced fitness gain and increased resistance to deltamethrin in beet armyworm, Spodoptera exigua (Hübner). Pest Manag Sci 75:683–693
Hoffmann A, French B, Hellmich R, Lauter N, Gassmann AJ (2015) Fitness costs of resistance to Cry3Bb1 maize by western corn rootworm. J Appl Entomol 139(6):403–415
Hollingworth RM, Gadelhak GG (1998) Mechanisms of action and toxicity of new pesticides that disrupt oxidative phosphorylation. Rev Toxicol 2(1):253–266
Imahori Y, Suzuki Y, Uemura K, Kishioka I, Fujiwara H, Ueda Y, Chachin K (2004) Physiological and quality responses of Chinese chive leaves to low oxygen atmosphere. Postharvest Biol Technol 31(3):295–303
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
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
Zheng JQ (2004) Handbook of contemporary vegetable pests and diseases: identification and management. China Agriculture Press, Beijing, China
Jin T, Lin Y-Y, Jin Q-A, Wen H-B, Peng Z-Q (2015) Population susceptibility to insecticides and the development of resistance in Bactrocera cucurbitae (Diptera: Tephritidae). J Econ Entomol 109(2):837–846
Khan HAA, Shad SA, Akram W (2012) Effect of livestock manures on the fitness of house fly, Musca domestica L. (Diptera: Muscidae). Parasitol Res 111(3):1165–1171
Kliot A, Ghanim M (2012) Fitness costs associated with insecticide resistance. Pest Manag Sci 68(11):1431–1437
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 H, Zhu F, Zhou X-M, Li N, Lei C-L (2007) Bionomics and control of the root maggot, Bradysia odoriphaga, infested on the watermelon. Entomol Knowl 44(6):834–836
Liang P, Tian Y-A, Biondi A, Desneux N, Gao X-W (2012) Short-term and transgenerational effects of the neonicotinoid nitenpyram on susceptibility to insecticides in two whitefly species. Ecotoxicology 21(7):1889–1898
Liu Z, Han Z (2006) Fitness costs of laboratory-selected imidacloprid resistance in the brown planthopper, Nilaparvata lugens Stål. Pest Manag Sci 62(3):279–282
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
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
Ma K, Tang Q, Xia J, Lv N, Gao X (2019) Fitness costs of sulfoxaflor resistance in the cotton aphid, Aphis gossypii Glover. Pestic Biochem Physiol 158:40–46
Mau J-L, Chen C-P, Hsieh P-C (2001) Antimicrobial effect of extracts from Chinese chive, cinnamon, and corni fructus. J Agri Food Chem 49(1):183–188
Mei Z, Wu Q, Zhang Y, Hua L (2004) Life tables of the laboratory population of Bradysia odoriphaga Yang & Zhang (Diptera: Mycetophilidae) at different temperatures. Acta Entomol Sin 47(2):219–222
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
Mu W, Liu F, Jia Z, He M, Xiang G (2003) A simple and convenient rearing technique for Bradysia odoriphaga. Entomol J East China 12(2):87–89
N’guessan R, Boko P, Odjo A, Akogbeto M, Yates A, Rowland M (2007) Chlorfenapyr: a pyrrole insecticide for the control of pyrethroid or DDT resistant Anopheles gambiae (Diptera: Culicidae) mosquitoes. Acta Trop 102(1):69–78
Oliver S, Kaiser M, Wood O, Coetzee M, Rowland M, Brooke B (2010) Evaluation of the pyrrole insecticide chlorfenapyr against pyrethroid resistant and susceptible Anopheles funestus (Diptera: Culicidae). Trop Med Int Health 15(1):127–131
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
Petzold‐Maxwell J, Siegfried BD, Hellmich R, Abel C, Coates B, Spencer TA, Horikoshi R, Gassmann AJ (2017) Fitness costs associated with Cry1F resistance in the European corn borer. J Appl Entomol 141(1–2):67–79
Qu W-M, Tai S-L, Zhang C-H, Wang L, Li L-L, Chu D, Yu Y (2018) Dispersal pattern of Bradysia odoriphaga populations in Shandong, China as revealed by microsatellite markers: implications of human activities. Entomol Gen 37(2):115–127. https://doi.org/10.1127/entomologia/2018/0528
Raghavendra K, Barik T, Bhatt R, Srivastava H, Sreehari U, Dash A (2011) Evaluation of the pyrrole insecticide chlorfenapyr for the control of Culex quinquefasciatus Say. Acta Trop 118(1):50–55
Rand GM (2004) Fate and effects of the insecticide–miticide chlorfenapyr in outdoor aquatic microcosms. Ecotoxicol Environ Saf 58(1):50–60
Saeed R, Sayyed AH, Shad SA, Zaka SM (2010) Effect of different host plants on the fitness of diamond-back moth, Plutella xylostella (Lepidoptera: Plutellidae). Crop Prot 29(2):178–182
Sayyed AH, Ahmad M, Crickmore N (2008a) Fitness costs limit the development of resistance to indoxacarb and deltamethrin in Heliothis virescens (Lepidoptera: Noctuidae). J Econ Entomol 101(6):1927–1933
Sayyed AH, Saeed S, Noor-Ul-Ane M, Crickmore N (2008b) Genetic, biochemical, and physiological characterization of spinosad resistance in Plutella xylostella (Lepidoptera: Plutellidae). J Econ Entomol 101(5):1658–1666
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
Scott JG, Georghiou GP (1985) Rapid development of high-level permethrin resistance in a field-collected strain of the house fly (Diptera: Muscidae) under laboratory selection. J Econ Entomol 78(2):316–319
Steinbach D, Moritz G, Nauen R (2017) Fitness costs and life table parameters of highly insecticide-resistant strains of Plutella xylostella (L.) (Lepidoptera: Plutellidae) at different temperatures. Pest Manag Sci 73(9):1789–1797
Tan W-L, Wang Z-M, Li C-X, Chu H-L, Xu Y, Dong Y-D, Wang Z-c, Chen D-Y, Liu H, Liu D-P (2012) First report on co-occurrence knockdown resistance mutations and susceptibility to beta-cypermethrin in Anopheles sinensis from Jiangsu Province, China. PLoS ONE 7(1):e29242
Tang Q, Ma K, Chi H, Hou Y, Gao X (2019) Transgenerational hormetic effects of sublethal dose of flupyradifurone on the green peach aphid, Myzus persicae (Sulzer) (Hemiptera: Aphididae). PLoS ONE 14(1):e0208058
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
Tariq K, Ali A, Davies TGE, Naz E, Naz L, Sohail S, Hou M, Ullah F (2019) RNA interference-mediated knockdown of voltage-gated sodium channel (MpNav) gene causes mortality in peach-potato aphid, Myzus persicae. Sci Rep 9(1):5291. https://doi.org/10.1038/s41598-019-41832-8
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, 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, Wang X, Ding Q, Said F, Gao X, Desneux N, Song D (2020) RNAi-mediated knockdown of chitin synthase 1 (CHS1) gene causes mortality and decreased longevity and fecundity in Aphis gossypii. Insects 11(1):22. https://doi.org/10.3390/insects11010022
Ullah F, Gul H, Yousaf HK, Xiu W, Qian D, Gao X, Tariq K, Han P, Desneux N, Song D (2019d) Impact of low lethal concentrations of buprofezin on biological traits and expression profile of chitin synthase 1 gene (CHS1) in melon aphid, Aphis gossypii. Sci Rep 9(1):12291. https://doi.org/10.1038/s41598-019-48199-w
Ullah S, Shah RM, Shad SA (2016) Genetics, realized heritability and possible mechanism of chlorfenapyr resistance in Oxycarenus hyalinipennis (Lygaeidae: Hemiptera). Pestic Biochem Physiol 133:91–96
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(1):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 D, Qiu X, Wang H, Qiao K, Wang K (2010) Reduced fitness associated with spinosad resistance in Helicoverpa armigera. Phytoparasitica 38(2):103–110
Wang Z-H, Gong Y-J, Chen J-C, Su X-C, Cao L-J, Hoffmann AA, Wei S-J (2018) Laboratory selection for resistance to sulfoxaflor and fitness costs in the green peach aphid Myzus persicae. J Asia-Pac Entomol 21(1):408–412
Yabuki Y, Mukaida Y, Saito Y, Oshima K, Takahashi T, Muroi E, Hashimoto K, Uda Y (2010) Characterisation of volatile sulphur-containing compounds generated in crushed leaves of Chinese chive (Allium tuberosum Rottler). Food Chem 120(2):343–348
Yang J, Zhang X (1985) Notes on the fragrant onion gnats with descriptions of two new species of Bradysia (Diptera: Sciaridae). Acta Agric Univ Pekin 11:153–156
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
Zewen L, Zhaojun H, Yinchang W, Lingchun Z, Hongwei Z, Chengjun L (2003) Selection for imidacloprid resistance in Nilaparvata lugens: cross-resistance patterns and possible mechanisms. Pest Manag Sci 59(12):1355–1359
Zhang H, Mallik A, Zeng RS (2013) Control of Panama disease of banana by rotating and intercropping with Chinese chive (Allium tuberosum Rottler): role of plant volatiles. J Chem Ecol 39(2):243–252
Zhang P, Liu F, Mu W, Wang Q, Li H, Chen C (2014) Life table study of the effects of sublethal concentrations of thiamethoxam on Bradysia odoriphaga Yang and Zhang. Pestic Biochem Physiol 111:31–37
Zhang W, Wang K, Niu F, Wang D, Ren X (2009) Induction of chlorfenapyr on endogenous protective and detoxifying enzymes in beet armyworm, Spodoptera exigua (Hübner). Acta Phytophylacica Sin 36(5):455–460
Zhang X, Mao K, Liao X, He B, Jin R, Tang T, Wan H, Li J (2018) Fitness cost of nitenpyram resistance in the brown planthopper Nilaparvata lugens. J Pest Sci 91(3):1145–1151
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(3-4):221–230. https://doi.org/10.1127/entomologia/2019/0816
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 Agri Food Chem 65(29):5908–5915
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
Acknowledgements
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
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
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
Ullah, F., Gul, H., Desneux, N. et al. Fitness costs in chlorfenapyr-resistant populations of the chive maggot, Bradysia odoriphaga. Ecotoxicology 29, 407–416 (2020). https://doi.org/10.1007/s10646-020-02183-7
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10646-020-02183-7