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Sublethal and transgenerational effects of insecticides in developing Trichogramma galloi (Hymenoptera: Trichogrammatidae)

Toxicity of insecticides to Trichogramma galloi

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Abstract

This study assessed the transgenerational effects of insecticides in developing Trichogramma galloi (Hymenoptera: Trichogrammatidae). Laboratory bioassays were performed in which five insecticides were sprayed on egg-larval, pre-pupal and pupal stages of the parasitoid. The interaction between insecticides and development stages of the parasitoid was not significant for the rate of F0 emergence. All insecticides significantly reduced the emergence of wasps, with the lowest emergence observed when they were applied to the pupal stage. For the sex ratio, only spinosad applied to the pre-pupal stage and triflumuron applied on the egg-larval and pre-pupal stages did not differ from the controls. Triflumuron applied to pre-pupae did not lead to any difference in the parasitism rate of the treated generation (F0) when compared to the control. There were no significant differences among survival curves for females of F0 when all insecticides were sprayed on the egg-larval stage. Both concentrations of lambda-cyhalothrin + thiamethoxam reduced female pre-pupal survival, and all treatments reduced female pupal survival. In addition, we observed a transgenerational effect of the insecticides on emergence and sex ratio of next generation (F1). Lambda-cyhalothrin + thiamethoxam (Min) applied to the pre-pupae and pupae, the maximum rate of the same insecticides applied to the egg-larvae and pre-pupae, and spinosad applied to pre-pupae all significantly reduced the adults emergence of T. galloi F1 generation. Only triflumuron did not alter the F1 sex ratio. These bioassays provide a basis for better understanding the effects of insecticide use on beneficial parasitoids.

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References

  • Ali A, Ahmad F, Biondi A, Wang Y, Desneux N (2012) Potential for using Datura alba leaf extracts against two major stored grain pests, the khapra beetle Trogoderma granarium and the rice weevil Sitophillus oryzae. J Pest Sci 85:359–366

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Biondi A, Desneux N, Siscaro G, Zappalà L (2012b) 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 87:803–812

    Article  CAS  Google Scholar 

  • Biondi A, Zappalà 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

    Article  CAS  Google Scholar 

  • Carvalho GA, Reis PR, Moraes JC, Fuini LC, Rocha LCD, Goussain MM (2002) Efeitos de alguns inseticidas utilizados na cultura do tomateiro (Lycopersicon esculentum Mill.) a Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae). Ciênc Agrotec 26:1160–1166

    CAS  Google Scholar 

  • Carvalho GA, Godoy MS, Parreira DS, Rezende DT (2010) Effect of chemical insecticides used in tomato crops on immature Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). Rev Colomb Entomol 36:10–15

    CAS  Google Scholar 

  • Chailleux A, Desneux N, Seguret J, Khanh HDT, Maignet P, Tabone E (2012) Assessing European egg parasitoids as a mean of controlling the invasive South American tomato pinworm Tuta absoluta. PLoS ONE 7:e48068

    Article  CAS  Google Scholar 

  • Chailleux A, Bearez P, Pizzol J, Amiens-Desneux E, Ramirez-Romero R, Desneux N (2013) Potential for combining indigenous natural enemies for biological control of the key invasive tomato pest, Tuta absoluta, in Afro-Eurasia. J Pest Sci 86:533–541

    Article  Google Scholar 

  • Cohen E (2010) Chitin biochemistry: synthesis, hydrolysis and inhibition. In: Jérôme C, Stephens JS (eds) Advances in insect physiology. Academic, London, pp 5–74

    Google Scholar 

  • Cônsoli FL, Rossi MM, Parra JRP (1999) Development time and characteristics of the immature stages of Trichogramma galloi and T. pretiosum (Hymenoptera, Trichogrammatidae). Rev Bras Entomol 43:271–275

    Google Scholar 

  • Cônsoli FL, Botelho PSM, Parra JRP (2001) Selectivity of insecticides to the egg parasitoid Trichogramma galloi Zucchi, 1988, (Hym., Trichogrammatidae). J Appl Entomol 125:37–43

    Article  Google Scholar 

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

    Google Scholar 

  • Daam MA, Van den Brink PJ (2010) Implications of differences between temperate and tropical freshwater ecosystems for the ecological risk assessment of pesticides. Ecotoxicology 19:24–37

    Article  CAS  Google Scholar 

  • Delpuech JM, Meyet J (2003) Reduction in the sex ratio of the progeny of a parasitoid wasp (Trichogramma brassicae) surviving the insecticide chlorpyrifos. Arch Environ Contam Toxicol 45:203–208

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Dias-Pini NS, Broglio SMF, Costa SS, Santos JN, Guzzo EC (2012) Biological characteristics of Telenomus alecto and Trichogramma galloi reared on eggs of the sugarcane borer Diatraea flavipennella. Rev Bras Entomol 56:515–518

    Article  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

    Article  CAS  Google Scholar 

  • Guo L, Desneux N, Sonoda S, Liang P, Han P, Gao XW (2013) Sublethal and transgenerational effects of chlorantraniliprole on biological traits of the diamondback moth Plutella xylostella. Crop Prot 48:29–34

    Article  CAS  Google Scholar 

  • Hassan SA (1998) Guidelines for the evaluation of side effects of plant protection products on Trichogramma cacoeciae Marchal (Hym., Trichogrammatida). IOBC/WPRS Bull 21:119–128

    Google Scholar 

  • 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 Entomol 122:569–573

    Article  CAS  Google Scholar 

  • Hoffmann EJ, Middleton SM, Wise JC (2008) Ovicidal activity of organophosphate, oxadiazine, neonicotinoid and insect growth regulator chemistries on northern strain plum curculio, Conotrachelus nenuphar. J Insect Sci 8:1–6

    Article  Google Scholar 

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

    Google Scholar 

  • IRAC Insecticide Resistance Action Committee (2012) Mode of action classification: insecticide resistance management. http://www.irac-online.org/content/uploads/MoA-Brochure_ed-3.5_21Feb12.pdf. Accessed 20 March 2013

  • James DG (2002) Selectivity of the acaricide, bifenazate, and aphicide, pymetrozine, to spider mite predators in Washington hops. Int J Acarol 28:175–179

    Article  Google Scholar 

  • Johnson MW, Tabashnik BE (1999) Enhanced biological control through pesticide selectivity. In: Fisher T, Bellows TS, Caltagirone LE, Dahlsten DL, Huffaker C, Gordh G (eds) Handbook of biological control. Academic, San Diego, pp 297–317

    Chapter  Google Scholar 

  • Kim SW, Kwak J, An YJ (2013) Multigenerational study of gold nanoparticles in Caenorhabditis elegans: transgenerational effect of maternal exposure. Environ Sci Technol 47:5393–5399

    Article  CAS  Google Scholar 

  • Liu TX, Zhang Y (2012) Side effects of two reduced-risk insecticides, indoxacarb and spinosad, on two species of Trichogramma (Hymenoptera: Trichogrammatidae) on cabbage. Ecotoxicology 21:2254–2263

    Article  CAS  Google Scholar 

  • Maia JB, Carvalho GA, Leite MIS, Oliveira RL, Makyama L (2010) Selectivity of insecticides used in corn crops to adult Trichogramma atopovirilia (Hymenoptera: Trichogrammatidae). Rev Colomb Entomol 36:202–206

    CAS  Google Scholar 

  • Marini RP (2003) Approaches to analyzing experiments with factorial arrangements of treatments plus other treatments. Hort Science 38:117–120

    Google Scholar 

  • Merzendorfer H (2013) Chitin synthesis inhibitors: old molecules and new developments. Insect Sci 20:121–138

    Article  CAS  Google Scholar 

  • Mills N (2010) Egg parasitoids in biological control and integrated pest management. In: Cônsoli FL, Parra JRP, Zucchi RA (eds) Egg parasitoids in agroecosystems with emphasis on Trichogramma, 1st edn. Springer, Dordrecht, pp 389–411

    Google Scholar 

  • Ministério da Agricultura, Pecuária e Abastecimento (2013) AGROFIT: sistema de agrotóxicos fitossanitários. Coordenação Geral de Agrotóxicos e Afins/DFIA/DAS, Brasília, Brazil. http://extrant.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. Accessed 17 March 2013

  • Moscardini VF, Moura AP, Carvalho GA, Lasmar O (2008) Efeito residual de inseticidas sintéticos sobre Trichogramma pretiosum Riley (Hym., Trichogrammatidae) em diferentes gerações. Acta Sci Agron 30:177–182

    Google Scholar 

  • Moscardini VF, Gontijo PC, Carvalho GA, Oliveira RL, Maia JB, Silva FF (2013) Toxicity and sublethal effects of seven insecticides to eggs of the flower bug Orius insidiosus (Say) (Hemiptera: Anthocoridae). Chemosphere 92:490–496

    Article  CAS  Google Scholar 

  • Narahashi T, Zhao X, Ikeda T, Nagata N, Yeh JZ (2007) Differential actions of insecticides on target sites: basis for selective toxicity. Hum Exp Toxicol 26:361–366

    Article  CAS  Google Scholar 

  • Oliveira CM, Auad AM, Mendes SM, Frizzas MR (2014) Crop losses and the economic impact of insect pests on Brazilian agriculture. Crop Prot 56:50–54

    Article  Google Scholar 

  • Parra JRP (2010) Mass rearing of egg parasitoids for biological control programs. In: Cônsoli FL, Parra JRP, Zucchi RA (eds) Egg parasitoids in agroecosystems with emphasis on Trichogramma, 1st edn. Springer, Dordrecht, pp 267–292

    Google Scholar 

  • Parra JRP, Zucchi RA (2004) Trichogramma in Brazil: feasibility of use after twenty years of research. Neotrop Entomol 33:271–281

    Article  Google Scholar 

  • Pinto JD (2006) A review of the new world genera of Trichogrammatidae (Hymenoptera). J Hymenopt Res 15:38–163

    Google Scholar 

  • Querino RB, Zucchi RA, Pinto JD (2010) Systematics of the trichogrammatidae (Hymenoptera: Chalcidoidea) with a focus on the genera attacking Lepidoptera. In: Cônsoli FL, Parra JRP, Zucchi RA (eds) Egg parasitoids in agroecosystems with emphasis on Trichogramma, 1st edn. Springer, Dordrecht, pp 191–218

    Google Scholar 

  • Rodriguez JR, Pintureau B, Galan M (1994) Determinants of the color of host eggs parasitized by Trichogramma fuentesi. Entomol Exp Appl 70:121–128

    Article  Google Scholar 

  • Saber M, Abedi Z (2013) Effects of methoxyfenozide and pyridalyl on the larval ectoparasitoid Habrobracon hebetor. J Pest Sci 86:685–693

    Article  Google Scholar 

  • SAS Institute (2008) SAS/STAT User’s Guide, v. 8. Cary: SAS Institute

  • Scott AJ, Knott MA (1974) Cluster analysis method for grouping means in the analysis of variance. Biometrics 30:507–512

    Article  Google Scholar 

  • Sechser B, Reber B, Bourgeois F (2002) Pymetrozine: selectivity spectrum to beneficial arthropods and fitness for integrated pest management. J Pest Sci 75:72–77

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Souza JR, Carvalho GA, Moura AP, Couto MHG, Maia JB (2013) Impact of insecticides used to control Spodoptera frugiperda (J. E. Smith) in corn on survival, sex ratio, and reproduction of Trichogramma pretiosum Riley offspring. Chil J Agric Res 73:122–127

    Article  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

    Article  Google Scholar 

  • Sterk G, Hassan SA, Baillod M et al (1999) Results of the seventh joint pesticide testing programme carried out by the IOBC/WPRSWorking Group “Pesticides and beneficial organisms”. Biocontrol 44:99–117

    Article  CAS  Google Scholar 

  • Stock D, Holloway PJ (1993) Possible mechanisms for surfactant-induced foliar uptake of agrochemicals. Pest Sci 38:165–177

    Article  CAS  Google Scholar 

  • Tabone E, Bardon C, Desneux N, Wajnberg E (2010) Parasitism of different Trichogramma species and strains on Plutella xylostella L. on greenhouse cauliflower. J Pest Sci 83:251–256

    Article  Google Scholar 

  • Tan Y, Biondi A, Desneux N, Gao XW (2012) Assessment of physiological sublethal effects of imidacloprid on the mirid bug Apolygus lucorum (Meyer-Dür). Ecotoxicology 21:1989–1997

    Article  CAS  Google Scholar 

  • Vanaclocha P, Vidal-Quist C, Oheix S, Montón H, Planes L, Catalán J, Tena A, Verdú MJ, Urbaneja A (2013) Acute toxicity in laboratory tests of fresh and aged residues of pesticides used in citrus on the parasitoid Aphytis melinus. J Pest Sci 86:329–336

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wang Y, Chen L, Yu R, Zhao X, Wu C, Cang T, Wang Q (2012b) Insecticide toxic effects on Trichogramma ostriniae (Hymenoptera: Trichogrammatidae). Pest Manag Sci 68:1564–1571

    Article  CAS  Google Scholar 

  • Wang Y, Yu R, Zhao X, Chen L, Wu C, Cang T, Wang Q (2012c) Susceptibility of adult Trichogramma nubilale (Hymenoptera: Trichogrammatidae) to selected insecticides with different modes of action. Crop Prot 34:76–82

    Article  Google Scholar 

  • Wang Y, Chen L, An X, Jiang J, Wang Q, Cai L, Zhao X (2013) Susceptibility to selected insecticides and risk assessment in the insect egg parasitoid Trichogramma confusum (Hymenoptera: Trichogrammatidae). J Econ Entomol 106:142–149

    Article  CAS  Google Scholar 

  • Wiesner P, Kayser H (2000) Characterization of nicotinic acetylcholine receptors from the insects Aphis craccivora, Myzus persicae, and Locusta migratoria by radioligand binding assays: relation to thiamethoxam action. J Biochem Mol Toxicol 14:221–230

    Article  CAS  Google Scholar 

  • Zappalà L, Biondi A, Alma A et al (2013) Natural enemies of the South American moth, Tuta absoluta, in Europe, North Africa and Middle-East, and their potential use in pest control strategies. J Pest Sci 86:635–647

    Article  Google Scholar 

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Acknowledgments

We would like to thank the National Council of Scientific and Technological Development (CNPq), the CAPES Foundation (Brazilian Ministry of Education), and the Minas Gerais State Foundation for Research Aid (FAPEMIG) for the financial support provided. We would also like to thank Dr. J. P. Michaud, Kansas State University, for his comments and corrections.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical standards

All study participants provided informed consent, and the study design was approved by the appropriate ethics review boards.

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Authors and Affiliations

  1. Laboratory of Selectivity Studies, Department of Entomology, Federal University of Lavras, P.O. Box 3037, Lavras, MG, 37200-000, Brazil

    Mariana Abreu Costa, Valéria Fonseca Moscardini, Pablo da Costa Gontijo, Geraldo Andrade Carvalho & Rodrigo Lopes de Oliveira

  2. EMBRAPA/CPAO, P.O. Box 449, Dourados, MS, 79804-970, Brazil

    Harley Nonato de Oliveira

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  1. Mariana Abreu Costa
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  2. Valéria Fonseca Moscardini
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  3. Pablo da Costa Gontijo
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  4. Geraldo Andrade Carvalho
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  5. Rodrigo Lopes de Oliveira
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  6. Harley Nonato de Oliveira
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Correspondence to Pablo da Costa Gontijo.

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Costa, M.A., Moscardini, V.F., da Costa Gontijo, P. et al. Sublethal and transgenerational effects of insecticides in developing Trichogramma galloi (Hymenoptera: Trichogrammatidae). Ecotoxicology 23, 1399–1408 (2014). https://doi.org/10.1007/s10646-014-1282-y

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