Skip to main content
Log in

Lethal and parasitism effects of selected novel pesticides on the immature stages of Trichogramma chilonis (Trichogrammatidae: Hymenoptera)

  • Original Research Article
  • Published:
International Journal of Tropical Insect Science Aims and scope Submit manuscript

Abstract

Selectivity of pesticides to the natural enemies in an agroecosystem is required for more effective integrated pest management. Trichogramma chilonis (Ishii) is an important natural enemy of lepidopteran pests, and is often exposed to pesticides. Effects of selected pesticides on acute mortality and parasitism when applied to parasitoids in egg, larval and pupal stages in their hosts were evaluated at 1x (field dose in Pakistan), 2x (double field dose) and 0.5x (half of field dose) doses. The parasitized host eggs were dipped in formulated solutions of pesticides when parasitoids were in different life stages. Parasitoid emergence from hosts treated with acetamiprid, fipronil and abamectin in the egg treatment and with spinetoram in all immature treatments were ≤ 33.9%. Treatment with acetamiprid (≤ 83.1 and ≤ 60.9%), fipronil (≤ 42.3and ≤ 72.7%), and abamectin (≤ 17.2 and ≤ 52.6%) yielded emergence in larval and pupal stage treatments, respectively. Spirotetramat, chlorantraniliprole, spiromesifen, haloxyfop-p-methyl, bispyribac sodium, nicosulfuron, chlorothalonil + procymidone, myclobutanil, pyraclostrobin + metiram, and trifloxystrobin + tebuconazole produced parasitoid emergence ≥ 80.1%.

Parasitoids emerged from hosts treated with spirotetramat, chlorantraniliprole, spiromesifen, bispyribac sodium, pyraclostrobin + metiram and trifloxystrobin + tebuconazole (except at 2 × dose in egg treatment) produced ≥ 84% parasitism in all treatments. Myclobutanil treatment of egg, and nicosulfuron and haloxyfop-p-methyl treatments of larvae and pupae, yielded > 90% parasitism. Acetamiprid and fipronil treatment of larvae and pupae, and abamectin treatment of pupae produced ≤ 78.46% and ≤ 10.76% parasitism, respectively. Over half of the pesticides caused no significant mortality to immature stages or exhibited little to no adverse impacts on parasitism and are promising for integration with these parasitoids.

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
Fig. 6

Similar content being viewed by others

References

  • Akhtar ZR, Tariq K, Handler AM, Ali A, Ullah F, Ali F, Zang L-S, Gulza A, Ali S (2021) Toxicological risk assessment of some commonly used insecticides on Cotesia flavipes, a larval parasitoid of the spotted stem borer Chilo partellus. Ecotoxico 30(3):448–458

    CAS  Google Scholar 

  • Bale J, van Lenteren J, Bigler F (2008) Biological control and sustainable food production. Philos Trans R Soc Lond 363:761–776

    CAS  Google Scholar 

  • Ballal CR, Srinivasan R, Jalali SK (2009) Evaluation of an endosulfan tolerant strain of Trichogramma chilonis on cotton, BioContr l54: 723–732

  • Beasley TM, Zumbo DB (2009) Aligned rank tests for interactions in split-plot designs: Distributional assumptions and stochastic homogeneity. J Mod Appli Statist Meth 8:16–50

    Google Scholar 

  • Bellows T (2001) Restoring population balance through natural enemy introduction. Biol Cont 21:199–205

    Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Statisti Socie Seri B 57:289–300

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

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

    CAS  PubMed  Google Scholar 

  • Biondi A, Zappala` 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

  • Bompard A, Amat I, Fauvergue X, Spataro T (2013) Host-parasitoid dynamics and the success of biological control when parasitoids are prone to allee effects. PLoS ONE 8(10):e76768. https://doi.org/10.1371/journal.pone.0076768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brar KS, Varma GC, Shenhmar M (1991) Effect of insecticides on Trichogramma chilonis Ishii (hymenoptera: Trichogrammatidae), an egg parasitoid of sugarcane borers and cotton bollworms. J Entomon 16:43–48

    CAS  Google Scholar 

  • Brück E, Elbert A, Fischer R, Krueger S, Kühnhold J, Klueken AM, Nauen R, Niebes J-F, Reckmann U, Schnorbach H-J, Steffens R, van Waetermeulen X (2009) Movento®, an innovative ambimobile insecticide for sucking insect pest control in agriculture: Biological profile and field performance. Crop Prot 28:838–844

    Google Scholar 

  • Brown RA (1989) Pesticides and non-target terrestrial invertebrates: an industrial approach. In: Jepson PC (ed) Pesticides and nontarget invertebrates. Intercept Ltd, Wimborne 19–42

  • Bueno A. de F, Bueno RCO de F, Parra JRP, Vieira SS (2008) Effects of pesticides used in soybean crops to the egg parasitoid Trichogramma pretiosum. Ciência Rural. Santa Maria 38(6):1495–1503

  • Bull DL, Coleman RJ (1985) Effects of pesticides on Trichogramma spp. Southwest Entomol (supplement) 8:156–168

    CAS  Google Scholar 

  • Calvo B, Stantafe G (2016) Scmamp: An R software package for statistical comparison of multiple algorithms in multiple problems. https://www.rdocumentation.org/packages/scmamp/versions/0.2.55 Version 0.2.55

  • Carmo EL, Bueno AF, Bueno RCOF (2010) Pesticide selectivity for the insect egg parasitoid Telenomus remus. BioCont 55:455–464

  • Carvalho GA, Reis PR, Rocha LCD, Moraes JC, Fuini LC, Ecole CC (2003) Side-effects of insecticides used in tomato fields on Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). Maringa 25(2):275–279

    CAS  Google Scholar 

  • Chang SC, Hu NT, Hsin CY, Sun CN (2001) Characterization of differences between two Trichogramma wasps by molecular markers. Biol Cont 21:75–78

    CAS  Google Scholar 

  • Cheng S, Lin R, Wang L, Qiu Q, Qu M, Ren X, Zong F, Jiang H, Yu C (2018) Comparative susceptibility of thirteen selected pesticides to three different insect egg parasitoid Trichogramma species. Ecotoxic Environm Safety 166:86–91

    CAS  Google Scholar 

  • Consoli FL, Parra JRP, Hassan SA (1998) Side-effects of insecticides used in tomato fields on the egg parasitoid Trichogramma pretiosum Riley (Hym., Trichogrammatidae), a natural enemy of Tuta absoluta (Meyrick) (Lep., Gelechiidae). J Appl Entomol 122:43–47

    CAS  Google Scholar 

  • Croft BA (1990) Arthropod biological control agents and pesticides. John Wiley and Sons, New York 

  • de Mendiburu F (2020) Agricolae: An R software package for statistical procedures for agricultural research. https://tarwi.lamolina.edu.pe/~fmendiburu/ Version 1.2–8

  • de Paiva ACR, Beloti VH, Yamamoto PT (2018) Sublethal effects of insecticides used in soybean on the parasitoid Trichogramma pretiosum. Ecotoxico 27(4):448–456

    Google Scholar 

  • de Paiva ACR, Filho FHI, Parro EA, Barbosa DPL, Yamamoto PT (2020) Do Ready-Mix Insecticides Cause Lethal and Sublethal Effects on Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) Pupa?. J Eco Entomol XX(XX) 1–7

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

    CAS  PubMed  Google Scholar 

  • Desneux N, Pham-Dele`gue MH, Kaiser L (2004) Effects of sub-lethal and lethal doses of lambda-cyhalothrin on oviposition experience and host-searching behaviour of a parasitic wasp, Aphidius ervi. Pest Manag Sci 60:381–389

    CAS  PubMed  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

    CAS  PubMed  Google Scholar 

  • Engindeniz S, Engindeniz DY (2006) Economic analysis of pesticide use on greenhouse cucumber growing: A case 493 study for Turkey. J Plant Dis Prot 113:193–198

    Google Scholar 

  • Firake DM, Thubru DP, Behere GT (2017) Eco-toxicological risk and impact of pesticides on important parasitoids of cabbage butterflies in cruciferous ecosystem. Chemosph 168:372–383

    CAS  Google Scholar 

  • Fishel FM (2013) The EPA conventional reduced risk pesticide program. PI-224. University of Florida Institute of Food and Agricultural Sciences, Gainesville

  • Ghorbani M, Saber M, Bagheri M, Vaez N (2016) Effects of diazinon and fipronil on different developmental stages of Trichogramma brassicae Bezdenko (Hym.; Trichogrammatidae). J Agric Sci Technol 18:1267–1278

    Google Scholar 

  • Gill HK, Garg H (2014) Pesticide: Environmental Impacts and Management Strategies. Pesticides-Toxic Effects. Intech. Rijeka, Croatia, 187–230

  • Goulart RM, Volpe HX, Vacari AM, Thuler RT, De Bortoli SA (2011) Insecticide selectivity to two species of Trichogramma in three different hosts, as determined by IOBC/WPRS methodology. Pest Manag Sci 68(2):240–244

  • Guedes RN, Lima JOG, Zanuncio JC (1992) Seletividade dos inseticidas deltametrina, fenvalerato e fenitrotion para Podisus connexivus Bergroth, 1891 (Heteroptera: Pentatomidae). An Soc Entomol Bras 21:339–346

    CAS  Google Scholar 

  • Gurr GM, Wratten SD, Barbosa P (2000) Success in conservation biological control of arthropods. In: Gurr G, Wratten S (eds) Biological control: measures of success. Springer, Dordrecht, pp 105–132

    Google Scholar 

  • Hagley EAC, Laing JE (1989) Effect of pesticides on parasitism of artificially distributed eggs of the codling moth Cydia pomonella (Lepidoptera: Tortricidae) by Trichogramma sp. (Hymenoptera: Trichogrammatidae). Proc Entomol Soc Ont 120:25–33

    Google Scholar 

  • Hassan SA (1977) Standardized techniques for testing side-effects of pesticides on beneficial arthropods in the laboratory. J Plant Dis Prot 84:158–163

    CAS  Google Scholar 

  • Hassan SA (1989) Testing methodology and the concept of the IOBC/WPRS Working Group, in Pesticides and Non-Target Invertebrates, ed. By Jepson PC. Intercept, Andover, 1–18

  • Hassan SA (1992) Guideline of the side effects of plant protection products on Trichogramma chilonis. In guideline for testing the effects of pesticides on beneficial organisms: description of test method. Bull IOBC/WPRS 15:18–39

    Google Scholar 

  • Hassan SA (1993) The mass rearing and utilization of Trichogramma to control lepidopterous pests: achievements and outlook. Pestic Sci 37(4):387–391

    Google Scholar 

  • Hassan SA (1994) Strategies to select Trichogramma species for use in biological control. In: Wajnberg E, Hassan SA (eds) Biological Control With Egg Parasitoids. CAB International, Oxon, 55–71

  • Hassan SA (1997) Seleção de espécies de Trichogramma para uso em programas controle biológico. In: Parra JRP, Zucchi RA (eds) Trichogramma e o controle biológico aplicado. pp. 183–206

  • Hassan SA, Abdelgader H (2001) A sequential testing program to assess the side effects of pesticides on Trichogramma cacoeciae Marchal (Hym.Trichogrammatidae). IOBC/WPRS Bull 24:71–81

    Google Scholar 

  • Hassan SA, Biglert H, Bogenschutz H, Boller E, Brun J, Callis JNM, CPelseneer J, Duso C, Grove A, Heimbach U, Helyer N, Hokkanen H, Lewis GB, Mansour F, Moreth L, Polgar L, S-Petersen L, Suphanor B, Staubli A, Stern G, Vainio A, Veire VDM, Viggiani G, Vogt H (1994) Results of the sixth joint pesticide testing programme of the IOBC/WPRS-working group “Pesticides and Beneficial Organisms.” Entomopha 39(1):107–119

  • Hassan SA, Hafes B, Degrande PE, Herai K (1998) The side-effects of pesticides on the egg parasitoid Trichogramma cacoeciae Marchal (Hym., Trichogrammatidae), acute dose response and persistence tests. J Appl Ent 122(1–5):569–57

  • Hewa-Kapuge S, Mcdougall S, Hoffmann AA (2003) Effects of methoxyfenozide, indoxacarb, and other insecticides on the beneficial egg parasitoid Trichogramma nr. Brassicae (Hymenoptera: Trichogrammatidae) under laboratory and field conditions. J Econ Entomol 96:1083–1090

    CAS  PubMed  Google Scholar 

  • Higgins JJ, Tashtoush S (1994) An aligned rank transform test for interaction. Nonline Wor 1:201–211

    Google Scholar 

  • Hussain D, Akram M, Iqbal Z, Ali A, Saleem M (2010) Effect of insecticides on Trichogramma chilonis Ishii (Hymenoptera: Trichogrammatidae) immature and adult survival. J Agric Res 48:531–537

    Google Scholar 

  • Hussain D, Ali A, M-ul-Hassan M, Ali S, Saleem M, Nadeem S (2012) Evaluation of Toxicity of Some New Insecticides against Egg Parasitoid Trichogramma chilonis (Ishii) (Hymenoptera: Trichogrammatidae). Pakistan J Zool 44(4):1123–1127

    CAS  Google Scholar 

  • Hutchison WD, Flood B, Wyman JA (2004) Advances in United States sweet corn and snap bean insect pest management. In: Insect pest management Springer, Berlin, Heidelberg, pp. 247–278

  • Jacas J, Urbaneja A (2009) Origen de las plagas e historia del control Biológico. Control Biológico De. Plagas Agric. Phytoma, Esp. 3–13

  • Jalali SK, Singh SP (1993) Susceptibility of various stages of Trichogrammatoidea armigera Nagaraja to some pesticides and effect of residues on survival and parasitizing ability. Biocont Sci Technol 3:21–27

    Google Scholar 

  • Jepson PC (1989) Pesticides and non-target invertebrates. (ed.) Intercept. Wimborne. Dorset, U.K

  • Jiang J, Liu X, Zhang Z, Liu F, Mu W (2019) Lethal and sublethal impact of sulfoxaflor on three species of Trichogramma parasitoid wasps (Hymenoptera: Trichogrammatidae). Biol Cont 134:32–37

    CAS  Google Scholar 

  • Jiang J, Ma D, Zhang Z, Yu C, Liu F, Mu W (2018) Favorable compatibility of nitenpyram with the aphid predator, Coccinella septempunctata L. (Coleoptera: Coccinellidae). Envir Sci Pollu Res, 25(27):27393–27401

  • Kay M, Wobbrock JO (2015) ARTool: An R software package for the aligned rank transform for nonparametric factorial ANOVAs. https://cran.r-project.org/web/packages/ARTool Version 0.9.5

  • Khan MA (2017) Effect of selected baculoviruses on oviposition preference by Trichogramma chilonis (Trichogrammatidae: Hymenoptera). J King Saud Univ–Sci 29:214–220

  • Khan MA (2020) Lethal and parasitism effects of selected novel pesticides on adult Trichogramma chilonis (Hymenoptera: Trichogrammatidae). J Plant Dis Prot 127:81–90 

    Article  Google Scholar 

  • Khan MA, Khan H, Farid A (2014) Assessment of the lethal and parasitism effects of Helicoverpa armigera Nucleopolyhedrovirus (HaNPV) on Trichogramma chilonis (Ishii) (Hymenoptera: Trichogrammatidae). Sar J Agric 30(4):425–432

    Google Scholar 

  • Khan MA, Khan H, Farid A, Ali A (2015a) Evaluation of Toxicity of some Novel Pesticides to Parasitism by Trichogramma chilonis (Hymenoptera: Trichogramm-atidae). J Agric Res 53(1):63–73

    Google Scholar 

  • Khan MA, Khan H, Ruberson JR (2015b) Lethal and behavioral effects of selectednovel pesticides on adults of Trichogrammapretiosum (Hymenoptera: Trichogrammatidae). Pest Manag Sci 71:1640–1648

    CAS  PubMed  Google Scholar 

  • Khan MA, Ruberson JR (2017) Lethal effects of selected novel pesticides on immature stages of Trichogrammapretiosum (Hymenoptera:Trichogrammatidae). Pest Manag Sci 73(12):2465–2472

    CAS  PubMed  Google Scholar 

  • Landis DA, Wratten SD, Gurr GM (2000) Habitat management to conserve natural enemies of arthropod pests in agriculture. Ann Rev Ento 45:175–201

    CAS  Google Scholar 

  • Leite GLD, de Paulo PD, Zanuncio JC, Tavares WD-S, Alvarenga AC, Dourado LR, Bispo EP, Soares MA (2017) Herbicide toxicity, selectivity and hormesis of nicosulfuron on 10 Trichogrammatidae (Hymenoptera) species parasitizing Anagasta ( = Ephestia) kuehniella(Lepidoptera: Pyralidae) eggs. J Environ Sci Health B 2:52(1):70–76

  • Lingathurai S PM, Raveen R, Priyatharsini PV, Sathikumaran R, Narayanan PCS (2015) Ecotoxicological performances and biochemical effect of selected pesticides on Trichogramma chilonis (Ishii) (Hymenoptera: Trichogrammatid- ae). J Entom Zool Stud 3(1):109–114

    Google Scholar 

  • Lou YG, Zhang GR, Zhang WQ, Huc Y, Zhang J (2013) Biological control of rice insect pests in China. Biol Cont 67:8–12

    Google Scholar 

  • Mahankuda B, Sawai HR, Gawande RW, Neharkar PS, Nagdeote VG (2019) Effect of insecticide residues on the adult survival rate of Trichogramma chilonis under laboratory condition. J Entomol Zool Stud 7(2):1349–1351

  • Manzoni CG, Grutzmacher AD, Giolo FP, Harter WDR, Castilhos RV, Paschoal MDF (2007) Side-effects of pesticides used in integrated production of apples to parasitoids of Trichogramma pretiosum Riley and Trichogramma atopovirilia Oatman & Platner (Hymenoptera: Trichogrammatidae). BioAssay 2:1–11

  • Martinson T, Williams L III, English-Loeb G (2001) Compatibility of chemical disease and insect management practices used in New York vineyards with biological control by Anagrus spp Mymaridae Hymenoptera parasitoids of Erthroneura leafhoppers. Biol Cont 22:227–234

  • Moens J, Tirry L, Clercq PD (2012) Susceptibility of cocooned pupae and adults of the parasitoid Microplitis mediator to selected insecticides. Phytopara 40:5–9

    Google Scholar 

  • Moura AP, Carvalho GA, Pereira AE, Rocha LCD (2006) Selectivity evaluation of insecticides used to control tomato pests to Trichogramma pretiosum. BioCont 51:769–778

    CAS  Google Scholar 

  • Nascimento PT, Fadini MAM, Valicente FH, Ribeiro PEA (2018) Does Bacillus thuringiensis have adverse effects on the host egg location by parasitoid wasps? Revis Brasil De Entomol 62:260–266

    Google Scholar 

  • Parra JRP, Zucchi RA (1997) Trichogramma e o Controle Biol´ogico Aplicado. FEALQ, Piracicaba, Brazil, pp. 324

  • Parreira DS, Cruz RA, Zanuncio JC, Lemes PG, Rolim GS, Barbosa LR, Leite GLD, Serrão JE (2018) Essential oils cause detrimental effects on biological parameters of Trichogramma galloi immatures, J Pest Sci 91(2):887–895

    Google Scholar 

  • Peterson LS (1993) Effects of 45 insecticides, acaricides and molluscicides on the rove beetle Aleochara bilineata (col.: staphylinidae) in the laboratory. Entomopha 38 (3):371–382

  • Peterson LS (1995) Effects of 37 fungicides on the rove beetle Aleochara bilineata (coleop: staphylinidae) in the laboratory. Entomophaga 40(2):145–152

    Google Scholar 

  • Pinto JD (2006) A review of the New World genera of Trichogrammatidae (Hymenoptera). J Hymen 15:38–163

    Google Scholar 

  • Pinto JD, Stouthamer R (1994) Systematics of the Trichogrammatidae with emphasis on Trichogramma. In: Wajnberg E, Hassan SA (eds) Biological control with egg parasitoids. CAB International, Wallingford, pp. 1–36

    Google Scholar 

  • Polaszek A (2010) Species diversity and host associations of Trichogramma in Eurasia. In: Cônsoli FL, Parra JR, Zucchi RA (eds) Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma. Springer, Dordrecht, pp. 237–266

  • Pontes JP, Leite GLD, Bispo EPR, Tavares W de S, Menezes CWG de,Wilcken CF, Zanuncio JC (2020) A glyphosate‑based herbicide in a free-choice test on parasitism, emergence, and female‑biased sex ratio of 10 Trichogrammatidae. J Plant Dis Prot 127:73–79

  • R Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/

  • Ruberson JR, Nemoto H, Hirose Y (1998) Pesticides and conservation of natural enemies in pest management. In: Barbosa P (ed) Conservation biological control. Academic Press, New York, pp 207–220

    Google Scholar 

  • Sagheer M, Ashfaq M, M-ul H, Rana SA (2008) Integration of Some Biopesticides and Trichogramma chilonis for the Sustainable Management of Rice Leaf Folder Cnaphalocrocis medinalis (Guenee) (Lepidoptera: Pyralidae). Pak J Agri Sci 45(1):69–74

    Google Scholar 

  • Sattar S, Ullah F, Saljoqi AUR, Arif M, Qazi JI (2011) Toxicity of some new insecticides against Trichogramma chilonis (Hymenoptera: Trichogrammatidae) under laboratory and extended laboratory conditions. Pak J Zool 43:1117–1125

    CAS  Google Scholar 

  • Schuld M, Schmuck UR (2000) Effects of Thiacloprid, a New Chloronicotinyl Insecticide, on the Egg Parasitoid Trichogramma cacoeciaev. Ecotoxicolo 9:197–205

    CAS  Google Scholar 

  • Sheng S, Wang J, Zhang X-rui, Liu Z-xiang, Yan M-wen, Shao Y, Zhou J-cheng, Wu Fu-an, Wang J (2021) Evaluation of Sensitivity to Phoxim and Cypermethrin in an Endoparasitoid, Meteorus pulchricornis (Wesmael) (Hymenoptera: Braconidae), and Its Parasitization Efficiency Under Insecticide Stress. J Insec Sci 21(1):10; 1–8

  • Singh PP, Varma GC (1986) Comparative toxicities of some pesticides to Chrysoperla carnea (Chrysopidae: Neuroptera) and Trichogrammabrasiliensis (Hymenoptera: Trichogrammatidae), two arthropod natural enemies of cotton pests. Agric Ecosyst Environ 15:23–30

    CAS  Google Scholar 

  • Smith SM (1996) Biological control with Trichogramma: advances, successes, and potential of their use. Annu Rev Entomol 41:375–406

    CAS  PubMed  Google Scholar 

  • Snyder WE (2019) Give predators a complement: conserving natural enemy biodiversity to improve biocontrol. Biol Cont 135:73–82

    Google Scholar 

  • Stark JD, Banken JO (1999) Importance of population structure at the time of toxicant exposure. Ecotox Environ Safety 42:282–287

    CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Steiner H (1977) Standardized field test to measure side-effects of pesticides in the tree level. J Plant Dise Prot 84(3):164–166

    Google Scholar 

  • Sterk G, Hassan SA, Baillod M, Bakker F, Bigler F, Blümel S, Bogenschütz H, Boller E, Bromand, B, Brun J, Calis JNM, Coremans-Pelseneer J, Duso C, Garrido A, Grove A, Heimbach U, Hokkanen H, Jacas J, Lewis G, Moreth L, Polgar L, Rovesti L, Samsoe-Peterson L, Sauphanor B, Schaub L, Stäubli A, Tuset JJ, Vainio A, de Veire M.V, Viggiani G, Viñuela E, Vogt H (1999) Results of the seventh joint pesticide testing programme carried out by the IOBC/WPRS-Working Group ‘‘Pesticides and Beneficial Organisms’’. BioControl 44:99–117

  • Suinaga FA, Picanc¸o M, Zanuncio JC, Bastos CS (1996) Seletividade fisiólogica de inseticidas a Podisus nigrispinus (Dallas, 1851) (Heteroptera: Pentatomidae) predador de lagartas desfolhadoras de eucalipto. Rev Árvore 20:407–414

  • Tabebordbara F, Shishehbora P, Ziaeea M, Sohrabi F (2020) Lethal and sublethal effects of two new insecticides spirotetramat and flupyradifurone in comparison to conventional insecticide deltamethrin on Trichogramma evanescens (Hymenoptera: Trichogrammatidae). J Asia-Pacif Entom 23:1114–1119

    Google Scholar 

  • Thomson LJ, Hoffmann AA (2010) Natural enemies responses and pest control importance of local vegetation. Biol Cont 52:160–166

    Google Scholar 

  • Torres JB, Bueno A de F (2018) Conservation biological control using selective insecticides – A valuable tool for IPM. Bio Cont 126:53–64

  • You Y, Lin T, Wei H, Zeng Z, Fu J, Liu X, Lin R, Zhang Y (2016) Laboratory evaluation of the sublethal effects of four selective pesticides on the predatory mite Neoseiulus cucumeris (Oudemans). Syst Appl Acarol 21(11):1506–1514

    Google Scholar 

  • Yu SJ (1998) Selectivity of insecticides to the spined soldier bug (Heteroptera: Pentatomidae) and its lepidopterous prey. J Econ Entomol 81:119–122

    Google Scholar 

  • van den Bosch R, Stern VM (1962) The integration of chemical and biological control of arthropods pests. Annu Rev Ent 7:367–386

    Google Scholar 

  • Varma GC, Singh PP (1987) Effect of insecticides on the emergence of Trichogramma brasiliensis (Hymenoptera: Trichogrammatidae) from parasitized host eggs. Entomoph 32:443–448

    CAS  Google Scholar 

  • Vieira A, Oliveira L, Garcia P (2001) Effects of conventional pesticides on the pre-imaginal developmental stages and on adults of Trichogramma cordubensis (Hymenoptera: Trichogrammatidae). Biocont Sci Technol 11:527–534

    Google Scholar 

  • Wahengbam J, Raut AM, Mandal SK, Banu AN (2018) Efficacy of new generation insecticides against Trichogramma chilonis Ishii and Trichogramma pretiosum Riley. J Ent Zool Stud 6(1):1361–1365

    Google Scholar 

  • Wajnberg E, Hassan SA (1994) Biological Control with Egg Parasitoids.CAB International, Wallingford, Oxon, UK, pp. 286

  • Way MJ (1986) The role of biological control in integrated plant protection. In: Franz JM (ed) Biological Plant and Health Protection. Gustav Fischer Verlag, Stuttgart, pp 289–303

    Google Scholar 

  • Wang DS, He YR, Guo XL, Luo YL (2012) Acute toxicities and sublethal effects of some conventional insecticides on Trichogramma chilonis (Hymenoptera: Trichogrammatidae). J Econ Entomol 105(4):1157–1163

    CAS  PubMed  Google Scholar 

  • Wang D, Lü L, He Y, Shi Q, Wang G (2016) Effects of Insecticides on Oviposition and Host Discrimination Behavior in Trichogramma chilonis (Hymenoptera: Trichogrammatidae). J Econ Entomol 109(6):2380–2387

    CAS  PubMed  Google Scholar 

  • Wang D, Lü L, He Y (2017) Effects of insecticides on sex pheromone communication and mating behavior in Trichogramma chilonis. J Pest Sci 91(1):65–78

    Google Scholar 

  • Willow J, Silva A, Veromann E, Smagghe G (2019) Acute effect of low-dose thiacloprid exposure synergised by tebuconazole in a parasitoid wasp. PlosOne 14(2):e0212456. https://doi.org/10.1371/journal.pone.0212456

    Article  CAS  Google Scholar 

  • Wobbrock JO, Findlater L, Gergle D, Higgins J (2011) The aligned rank transform for nonparametric factorial analyses using only ANOVA procedures. In Proceedings of the ACM Conference on Human Factors in Computing Systems (CHI '11), 143–146. URL: https://depts.washington.edu/aimgroup/proj/art/

  • Zucchi RA, Querino RB, Monteiro RC (2010) Diversity and hosts of Trichogramma in the New World, with emphasis in South America. In: Cônsoli FL, Parra JR, Zucchi RA (eds) Egg Parasitoids in Agroecosystems with Emphasis on Trichogramma. Springer, Dordrecht, pp 219–236

    Google Scholar 

Download references

Acknowledgements

I gratefully acknowledged the Higher Education Commission (HEC) of Pakistan financial support under indigenous PhD fellowship. I also wish to offer special thanks to the administration of the Nuclear Institute of Food and Agriculture (NIFA), Tarnab, Peshawar (Pakistan) for permission and provision of laboratory facilities to conduct experiments. I am also very grateful to Dr John R Ruberson, Chairman Department of Entomology, University of Nebraska, Lincoln. Nebraska, USA for English editing of the manuscript. I am very thankful to Jos Feys, senior research fellow at the KU Leuven University (Catholic University of Leuven, Belgium) for statistical analysis of the data.

Funding

This study was funded by Higher Education Commission of Pakistan under the indigenous 5000 PhD fellowship program, Batch IV with research grant number (PIN) 074–3591-BM4-011.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Muhammad Ashraf Khan.

Ethics declarations

Conflict of interest

I am the sole author of the manuscript and declares no conflict of interest with any person, institution or organization.

Additional information

Publisher's Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khan, M.A. Lethal and parasitism effects of selected novel pesticides on the immature stages of Trichogramma chilonis (Trichogrammatidae: Hymenoptera). Int J Trop Insect Sci 42, 1077–1093 (2022). https://doi.org/10.1007/s42690-021-00580-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42690-021-00580-x

Keywords

Navigation