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

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Abstract

Integration of chemical and biological controls is an important tactic of integrated pest management. Trichogramma chilonis (Ishii) is an important natural enemy of lepidopteran pests. However, the minute parasitoids are adversely affected by most pesticides. Effects of acute mortality and parasitism of selected novel pesticides on adults of T. chilonis exposed to the dried residues of field doses for 24 h on glass surface were evaluated. Acetamiprid, spinetoram and fipronil induced mortality of > 95%, followed by abamectin (ranged 71.3–83.5%) in four residual-age treatments. Spiromesifen, haloxyfop-p-methyl, mixture of pyraclostrobin + metiram and mixture of trifloxystrobin + tebuconazole revealed mortality of ≤ 36.4% in all treatments (when female parasitoids were exposed to 1 day, 5 days, 10 days and 15 days after treatments). Bispyribac sodium induced mortality of ranged 51.1–54.9% in 1- and 5-day treatments, and approximately ≤ 10% in others (10-day and 15-day treatment). Eggs of Sitotroga cerealella in acetamiprid, spinetoram, fipronil and abamectin treatments showed ≤ 36% parasitism relative to controls in all treatments. Spirotetramat, bispyribac sodium, nicosulfuron, trifloxystrobin + tebuconazole and pyraclostrobin + metiram resulted in parasitism rates of 49.2–71.2% and 81.5–93.8% in 1-day and 15-day treatment, respectively. Helicoverpa armigera nucleopolyhedrovirus, chlorantraniprole, spiromesifen haloxyfop-p-methyl, chlorothalonil + procymidone and myclobutanil showed ≥ 80.6% parasitism in all treatments. Thus, acetamiprid, spinetoram, fipronil and abamectin were the most harmful among the pesticides used for both emergence and parasitism, while remaining pesticides demonstrated relatively compatibility with the emergence as well as parasitism by the minute parasitoids, and can be integrated with the minute parasitoid in agroecosystem.

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References

  • Abbott WS (1925) A method of computing the effectiveness of an insecticide. J Econ Entomol 18(2):265–267

    CAS  Google Scholar 

  • Abdollahzadeh G, Sharifzadeh MS, Damalas CA (2015) Perceptions of the beneficial and harmful effects of pesticides among Iranian rice farmers influence the adoption of biological control. Crop Prot 75:124–131

    Google Scholar 

  • Amano H, Haseeb M (2001) Recently-proposed methods and concepts of testing the effects of pesticides on the beneficial mite and insect species: study limitations and implications in IPM. Appl Entomol Zool 36(1):1–11

    Google Scholar 

  • Ananthakrishnan TN, Senrayan R, Murugesan S, Annadurai RS (1991) Kairomones of Heliothis armigera and Corcyra cephalonica and their influence on the parasitic potential of Trichogramma chilonis (Trichogrammatidae: Hymenoptera). J Biosci 16(3):111–119

    Google Scholar 

  • Arbogast RT, Mullen MA (1987) Dynamics of Sitotroga cerealella (Olivier) (Lepidoptera: Gelechiidae) and Sitophilus zeamais motschulsky (Coleoptera: Curculionidae) populations in a small bulk of stored corn. Res Popul Ecol 29(1):1–15

    Google Scholar 

  • Athey KJ, Ruberson JR, Olson DM, Harwood JD (2019) Predation on stink bugs (Hemiptera: Pentatomidae) in cotton and soybean agroecosystems. PLoS ONE 14(3):1–14

    Google Scholar 

  • Barney RJ, Weston PA (1996) Movement of Angoumois grain moth (Lepidoptera: Gelechiidae) in a small-farm ecosystem. Environ Entomol 25(2):261–267

    Google Scholar 

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

    CAS  Google Scholar 

  • Bull DL, House VS (1983) Effects of different insecticides on parasitism of host eggs by Trichogramma pretiosum Riley. Southwest Entomol 8:46–53

    CAS  Google Scholar 

  • Cônsoli 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

    Google Scholar 

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

    Google Scholar 

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

    PubMed  CAS  Google Scholar 

  • Ebrahimi E (2004) Investigation and Identification of species of Trichogramma Westwood in Iran. In: Azema M, Mirabzadeh A (eds) Issues on different aspects of applying natural enemies for biological control of insect pests. Nashre Markaz, Tehran, pp 1–71

    Google Scholar 

  • Gardner J, Hoffmann MP, Pitcher SA, Harper JK (2011) Integrating insecticides and Trichogramma ostriniae to control European corn borer in sweet corn: economic analysis. Biol Control 56:9–16

    CAS  Google Scholar 

  • Gentz MC, Murdoch G, King GF (2010) Tandem use of selective insecticides and natural enemies for effective, reduced-risk pest management. Biol Control 52:208–215

    Google Scholar 

  • 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 

  • Gould F, Kennedy GG, Johnson MT (1991) Effects of natural enemies on the rate of herbivore adaptation to resistant host plants. Entomol Exp Appl 58:1–15

    Google Scholar 

  • Hassan SA (1988) Selection of suitable Trichogramma strains to control the codling moth Cydia pomonella and the two summer fruit tortrix moths Adoxophyes orana, Pandemis heparana (Lep: Tortricidae). Entomophaga 33(4):19–27

    Google Scholar 

  • Hassan SA (1989) Testing methodology and the concept of the IOBC/WPRS working group. In: Jepson PC (ed) Pesticides and non-target invertebrate. Intercept, Hants, pp 1–18

    Google Scholar 

  • Hassan SA, Bigler F, Bogenschütz H, Boller E, Brun J, Calis JNM, Coremans- Pelseneer J, Duso C, Grove A, Heimbach U, Hokkanen H, Helyer N, Lewis G, Mansour F, Moreth L, Polgar L, Samsoe-Petersen L, Sauphanor B, Stäubli A, Sterk G, Vainio A, van de Veire M, Viggiani G, Vogt H (1994) Results of the sixth joint pesticide testing programme of the IOBC/WPRS-working group ‘pesticides and beneficial organisms’. Entomophaga 39:107–119

    Google Scholar 

  • Hong-xing X, Ya-jun Y, Yan-hui L, Xu-song Z, Jun-ce T, Feng-xiang L, Qiang F, Zhong-xian L (2017) Sustainable management of rice insect pests by non-chemical insecticide technologies in china. Rice Sci 24(2):61–72

    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 

  • Jepsen SJ, Rosenheim JA, Matthews CE (2007) The impact of sulfur on the reproductive success of Anagrus spp. parasitoids in the field. BioControl 52(5):599–612

    CAS  Google Scholar 

  • 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 Control 134:32–37

    CAS  Google Scholar 

  • Kang Z-W, Liu F-H, Pang R-P, Tian H-G, Liu T-X (2018) Effect of sublethal doses of imidacloprid on the biological performance of aphid endoparasitoid Aphidius gifuensis (Hymenoptera: Aphidiidae) and influence on its related gene expression. Front Physiol. https://doi.org/10.3389/fphys.2018.01729

    Article  PubMed  PubMed Central  Google Scholar 

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

    PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Li L-Y (1994) Worldwide use of Trichogramma for biological control on different crops: a survey. In: Wajnberg E, Hassan SA (eds) Biological control with egg parasitoids. CAB International, Wallingford, pp 37–54

    Google Scholar 

  • Manjunath ΤΜ, Bhatnagar VS, Pawar CS, Sithanantham S (1985) Economic importance of Heliothis spp. in India and an assessment of their natural enemies and host plants. In: Proceedings of the workshop on biological control of Heliothis. New Delhi, India, pp 197–228

  • 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

    Google Scholar 

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

    CAS  Google Scholar 

  • Naranjo SE (2011) Impacts of Bt transgenic cotton on integrated pest management. J Agric Food Chem 59(11):5842–5851

    PubMed  CAS  Google Scholar 

  • 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 

  • Parreiraa DS, Alcántara-de la Cruzb R, Dimatéb FAR, Batistac LD, Ribeirod RC, Ferreirae GAR, Zanunciob JC (2019) Bioactivity of ten essential oils on the biological parameters of Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) adults. Ind Crops Prod 127:11–15

    Google Scholar 

  • Preetha G, Stanley J, Suresh S, Kuttalam S, Samiyappan R (2009) Toxicity of selected insecticides to Trichogramma chilonis: assessing their safety in the rice ecosystem. Phytoparasitica 37:209–215

    CAS  Google Scholar 

  • Rasool B, Arif J, Hamed M, Nadeem S (2002) Field performance of Trichogramma chilonis against Helicoverpa armigera under varying sowing time and varieties of cotton. Int J Biol Agric 4:113–114

    Google Scholar 

  • 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 

  • Shojai M, Ostovan H, Khodaman AR, Hosseini M, Daniali M, Seddighfar M, Nasrollahi AA, Labbafi Y, Ghavam F, Honarbakhsh S (1998) An investigation on beneficial species of Trichogramma spp. (Hym., Trichogrammatidae), active in apple orchards, and providing optimum conditions for mass production in laboratory cultures. J Agric Sci Islam Azad Univ 16:5–39

    Google Scholar 

  • Singh SP (2001) Augmentative biocontrol in India. In: Singh SP, Murphy ST, Ballal CR (eds) Augmentative biocontrol—proceedings of the ICAR-CABI workshop, 29th June to July 1st, 2001. Project Directorate of Biological Control, Bangalore, pp 1–20

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

    PubMed  CAS  Google Scholar 

  • Sorokina AP (1999) Trophic links of species of the genus Trichogramma West. (Hym. Trichogrammatidae) of the world fauna. Entomol Rev 79:125–132

    Google Scholar 

  • Stapel JO, Cortesero AM, Lewis WJ (2000) Disruptive sublethal effects of insecticides on biological control: altered foraging ability and life span of a parasitoid after feeding on extrafloral nectar of cotton treated with systemic insecticides. Biol Control 17:243–249

    CAS  Google Scholar 

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

    PubMed  Google Scholar 

  • Stavrinides MC, Mills NJ (2009) Demographic effects of pesticides on biological control of Pacific spider mite (Tetranychus pacificus) by the western predatory mite (Galendromus occidentalis). Biol Control 48:267–273

    CAS  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 MV, 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

    CAS  Google Scholar 

  • Suh CPC, Orr DB, Duyn JWV (2000) Effect of insecticides on Trichogramma exiguum (Trichogrammatidae: Hymenoptera) pre-imaginal development and adult survival. J Econ Entomol 93:577–583

    PubMed  CAS  Google Scholar 

  • Tilman D, Cassman KG, Matson PA, Naylor R, Polasky S (2002) Agricultural sustainability and intensive production practices. Nature 418:671–677

    PubMed  CAS  Google Scholar 

  • Unmole L (2010) Study of the biology of Trichogramma chilonis Ishii (Hymenoptera: Trichogrammatidae) in Mauritius. Univ Maurit Res J 16:84–99

    Google Scholar 

  • Van Driesche RG, Bellows TS Jr (1996) Biological control. Chapman and Hall Press, New York

    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

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Wang D, Lü L, He Y (2017b) Effects of two conventional insecticides on male-specific sex pheromone discrimination and mate choice in Trichogramma chilonis (Hymenoptera: Trichogrammatidae). Environ Entomol 46(2):328–334

    PubMed  CAS  Google Scholar 

  • WHO (2009) Guidelines for efficacy testing of insecticides for indoor and outdoor ground-applied space spray applications: control of neglected tropical diseases. WHO Pesticide Evaluation Scheme

Download references

Acknowledgements

I am very much grateful to the Higher Education Commission of Pakistan for the financial support to my research. I also wish to acknowledge the Nuclear Institute of Food and Agriculture (NIFA), Tarnab, Peshawar, for the provision of laboratory. I am also thankful to Dr. John R Ruberson, Head, Department of Entomology, University of Nebraska, Lincoln, USA, for revised and corrected the English language used in this manuscript. I am also very grateful to Jos Feys, senior research fellow and faculty member of movement and rehabilitation sciences 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 indigenous 5000 PhD fellowship program batch IV with research Grant Number 074-3591-Bm4-011.

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  1. Department of Environmental Sciences, University of Peshawar, Peshawar, Pakistan

    Muhammad Ashraf Khan

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Khan, M.A. Lethal and parasitism effects of selected novel pesticides on adult Trichogramma chilonis (Hymenoptera: Trichogrammatidae). J Plant Dis Prot 127, 81–90 (2020). https://doi.org/10.1007/s41348-019-00280-2

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