Skip to main content
SpringerLink
Log in

Side-effects of pesticides used in irrigated rice areas on Telenomus podisi Ashmead (Hymenoptera: Platygastridae)

  • Published:
Ecotoxicology Aims and scope Submit manuscript

Abstract

Telenomus podisi Ashmead (Hymenoptera: Platygastridae) is an important agent for the biological control of stink bug eggs in irrigated rice areas and the best strategy for its preservation is the use of selective pesticides. The aim of this study was to know the side-effects of pesticides used in Brazilian irrigated rice areas on egg parasitoid T. podisi. We evaluated, under laboratory conditions, 13 insecticides, 11 fungicides, 11 herbicides, and a control (distilled water) in choice and no-choice tests. In the no-choice tests, the pesticides were sprayed at pre and post-parasitism stages (egg and larval stages of T. podisi). In the choice tests, sprays were conducted only at pre-parasitism stages. For all tests, we prepared cards with 25 eggs of the alternative host Euschistus heros (Fabricius) (Hemiptera: Pentatomidae) non-parasitized (pre-parasitism) and parasitized (post-parasitism), which were subjected to pesticide sprays. The parasitism and emergence rates of T. podisi were determined classifying the pesticides in terms of the reduction of parasitism or emergence rates compared to the control. The neurotoxic insecticide cypermethrin, lambda-cyhalothrin, zeta-cypermethrin, etofenprox, thiamethoxam, thiamethoxam + lambda-cyhalothrin, acetamiprid + alpha-cypermethrin, and bifenthrin + alpha-cypermethrin + carbosulfan were more harmful to T. podisi and, therefore, are less suitable for the integrated management of insect pests in irrigated rice areas.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • AGROFIT. 2015. Sistema de agrotóxicos fitossanitários. http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. Accessed 13 June 2015

  • Agüero MAF, Neves PMOJ (2014) Seletividade de Metarhizium anisopliae a Telenomus podisi (Hymenoptera: Platygastridae). Investig Agrar 16:21–28

    Google Scholar 

  • Andres A, Concenço G, Melo PTBS, Schmidt M, Resende RG (2007) Detecção da resistência de capim-arroz (Echinochloa sp.) ao herbicida quinclorac em regiões orizícolas do Sul do Brasil. Planta Daninha 25:221–226. doi:10.1590/S0100-83582007000100025

    Article  Google Scholar 

  • Antigo MR, Oliveira HNde, Carvalho GA, Pereira FF (2013) Repelência de produtos fitossanitários usados na cana-de-açúcar e seus efeitos na emergência de Trichogramma galloi. Rev Ciênc Agron 44:910–916

    Article  Google Scholar 

  • Bayram A, Salermo G, Onofri A, Conti E (2010) Lethal and sublethal effects of preimaginal treatments with two pyrethroids on the life history of the egg parasitoid Telenomus busseolae. BioControl 55:697–710. doi:10.1007/s10526-010-9288-8

    Article  CAS  Google Scholar 

  • Beserra EB, Parra JRP (2005) Seletividade de lambdacialotrina a Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae). Acta Sci Agron 27:321–326. doi:10.4025/actasciagron.v27i2.1852

    Article  CAS  Google Scholar 

  • 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 87:803–812. doi:10.1016/j.chemosphere.2011.12.082

    Article  CAS  Google Scholar 

  • Biondi A, Campolo O, Desneux N, Siscaro G, Palmeri V, Zappalà L (2015) Life stage-dependent susceptibility of Aphytis melinus DeBach (Hymenoptera: Aphelinidae) to two pesticides commonly used in citrus orchards. Chemosphere 128:142–7. doi:10.1016/j.chemosphere.2015.01.034

    Article  CAS  Google Scholar 

  • Bordin LC, Casa RT, Marcuzzo LL, Bogo A, Zancan RL (2016) Efeito da aplicação de fungicidas no controle de doenças foliares de arroz irrigado e sua relação com o rendimento industrial. Summa Phytopathol 42:85–88. doi:10.1590/0100-5405/2012

    Article  Google Scholar 

  • Borges M, Laumann RA, Silva CCAda, Moraes MCB, Santos HMdos, Ribeiro TR (2006) Metodologias de criação e manejo de colônias de percevejos da soja (Hemiptera - Pentatomidae) para estudos de comportamento e ecologia química. Embrapa Recursos Genéticos e Biotecnologia, Brasília, p 18, http://www.embrapa.br/documents/1355163/2022525/doc182.pdf/25c8a999-816b-4050-b0c7-611c24e60700 Documentos/Embrapa Recursos Genéticos e Biotecnologia, 182Accessed 13 April 2016

    Google Scholar 

  • Brugger KE, Cole PG, Newman IC, Parker N, Scholz B, Suvagia P, Walker G, Hammond TG (2010) Selectivity of chlorantraniliprole to parasitoid wasps. Pest Manag Sci 66:1075–1081. doi:10.1002/ps.1977

    Article  CAS  Google Scholar 

  • Bueno AdeF, Bueno RCOde, Parra JRP, Vieira SS (2008) Effects of pesticides used in soybean crops to the egg parasitoid Trichogramma pretiosum. Cienc Rural 38:1495–1503. doi:10.1590/S0103-84782008000600001

    Article  CAS  Google Scholar 

  • Carmo ELdo, Bueno AdeF, Bueno RCOde, Vieira SS, Gobbi AL, Vasco FR (2009) Seletividade de diferentes agrotóxicos usados na cultura da soja ao parasitoide de ovos Telenomus remus. Cienc Rural 39:2293–2300. doi:10.1590/S0103-84782009005000188

    Article  Google Scholar 

  • Carmo ELdo, Bueno AdeF, Bueno RCOde (2010) Pesticide selectivity for the insect egg parasitoid Telenomus remus. BioControl 55:455–464. doi:10.1007/s10526-010-9269-y

    Article  CAS  Google Scholar 

  • Carvalho GAde, Parra JRP, Baptista GCde (2001) Impacto de produtos fitossanitários utilizados na cultura do tomateiro na fase adulta de duas linhagens de Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae). Cienc Agrotec 25:560–568

    Google Scholar 

  • Castro AAde, Côrrea AS, Legaspi JC, Guedes RNC, Serrão JE, Zanuncio JC (2013) Survival and behavior of the insecticide-exposed predators Podisus nigrispinus and Supputius cincticeps (Heteroptera: Pentatomidae). Chemosphere 93:1043–1050. doi:10.1016/j.chemosphere.2013.05.075

    Article  Google Scholar 

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

    Google Scholar 

  • Counce PA, Keisling TC, Mitchell AJ (2000) A uniform, objective, and adaptative system for expressing rice development. Crop Sci 40:436–443. doi:10.2135/cropsci2000.402436x

    Article  Google Scholar 

  • Desneux N, Fauvergue X, Dechaume-Moncharmont FX, Kerhoas L, Ballanger Y, Kaiser L (2005) Diaeretiella rapae limits Myzus persicae populations after applications of deltamethrin in oilseed rape. J Econ Entomol 98:9–17. doi:10.1603/0022-0493-98.1.9

    Article  Google Scholar 

  • Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106. doi:10.1146/annurev.ento.52.110405.091440

    Article  CAS  Google Scholar 

  • Farias PMde, Klein JT, Sant’Ana J, Redaelli LR, Grazia J (2012) First records of Glyphepomis adroguensis (Hemiptera, Pentatomidae) and its parasitoid, Telenomus podisi (Hymenoptera, Platygastridae), on irrigated rice fields in Rio Grande do Sul, Brazil. Rev Bras Entomol 56:383–384

    Article  Google Scholar 

  • Garjan AS, Talebi K, Pourmirza AA (2005) Effect of some pyrethroid and organphosphorous insecticides on developmental stages of Trissolcus grandis (Thom.) (Hymenoptera: Platygastridae). J Sci Tech Agr Nat Res 8:157–165

    Google Scholar 

  • Godoy KB, Galli JC, Ávila CJ (2005) Parasitismo em ovos de percevejos da soja Euschistus heros (Fabricius) e Piezodorus guildinii (Westwood) (Hemiptera: Pentatomidae) em São Gabriel do Oeste, MS. Cienc Rural 35:455–458. doi:10.1590/S0103-84782005000200034

    Article  Google Scholar 

  • Golin V (2014) Incidência natural, biologia, seletividade e efeito de liberações inoculativas de parasitoides de ovos (Hymenoptera: Platygastridae) no controle de Euschistus heros (Fabricius) (Hemiptera: Pentatomidae) no Mato Grosso. PhD. Thesis, Universidade Federal do Paraná

  • Goulart RM, Bortoli SAde, Thuler RT, Pratissoli D, Viana CLTP, Volpe HXL (2008) Avaliação da seletividade de inseticidas a Trichogramma spp. (Hymenoptera: Trichogrammatidae) em diferentes hospedeiros. Arq Inst Biol 75:69–77

    Google Scholar 

  • Hassan SA, Halsall N, Gray AP, Kuehner C, Moll M, Bakker FM, Roembke J, Yousef A, Nasr F, Abdelgader HÁ (2000) A laboratory method to evaluate the side effects of plant protection products on Trichogramma cacoeciae Marchal (Hym., Trichogrammatidae). In: Candolfi MP, Blümel S, Forster R, Bakker FM, Grimm C, Hassan SA, Heimbach U, Mead-Briggs MA, Reber B, Schmuck R, Vogt H (eds) Guidelines to evaluate side-effects of plant protection products to non-target arthropods. IOBC/WPRS, Reinheim, p 107–119

    Google Scholar 

  • Idalgo TDN, Sant’Ana J, Redaelli LR, Pires PDdaS (2013) Parasitismo de ovos de Tibraca limbativentris Stal (Hemiptera: Pentatomidae) em lavoura de arroz irrigado, Eldorado do Sul, RS. Arq Inst Biol 80:453–456. doi:10.1590/S1808-16572013000400014

    Article  Google Scholar 

  • IRRI (International Rice Research Institute). (1985) Illustrated guide to integrated pest management in rice in tropical Asia. Los Baños.

  • Jansen JP (1999) Effects of wheat foliar fungicides on the aphid endoparasitoid Aphidius rhopalosiphi DeStefani-Perez (Hym., Aphididae) on glass plates and on plants. J Appl Ent 123:217–224. doi:10.1046/j.1439-0418.1999.00339.x

    Article  CAS  Google Scholar 

  • Khan ZR, James DG, Midega CAO, Pickett JA (2008) Chemical ecology and conservation biological control. Biol Control 45:210–224. doi:10.1016/j.biocontrol.2007.11.009

    Article  CAS  Google Scholar 

  • Koppel AL, Herbert Jr DA, Kuhar TP, Malone S, Arrington M (2011) Efficacy of selected insecticides against eggs of Euschistus servus and Acrosternum hilare (Hemiptera: Pentatomidae) and the egg parasitoid Telenomus podisi (Hymenoptera: Platygastridae). J Econ Entomol 104:137–142. doi:10.1603/EC10222

    Article  CAS  Google Scholar 

  • Lou YG, Zhang GR, Zhang WQ, Hu Y, Zhang J (2013) Biological control of rice insect pests in China. Biol Control 6:8–20. doi:10.1016/j.biocontrol.2013.06.011

    Article  Google Scholar 

  • Magano DA, Krolow IRC, Grützmacher AD, Panozzo LE, Armas FSde, Zimmer M (2013) Efeitos secundários de herbicidas aplicados em soja sobre Trichogramma pretiosum. Pesq Agrop Gaúcha 19:49–56

    Google Scholar 

  • Magano DA, Grützmacher AD, Armas FSde, Paulus LF, Panozzo LE, Mentnech KJ, Zotti MJ (2015) Evaluating the selectivity of registered fungicides for soybean against Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae). Afr J Agric Res 10:3825–3831. doi: 0.5897/AJAR2014.9083

    Article  Google Scholar 

  • Manzoni CG, Grützmacher AD, Giolo FP, Lima CABde, Nörnberg SD, Härter WdaR, Müller C (2006) Seletividade de agrotóxicos recomendados na produção integrada da maçã a Trichogramma pretiosum Riley, 1879 (Hym.: Trichogrammatidae) em condições de laboratório. Rev Bras Frutic 28:254–257. doi:10.1590/S0100-29452006000200022

    Article  Google Scholar 

  • Martins JF, da S, Botton M, Carbonari JJ, Quintela ED (2004) Eficiência de Metarhizium anisopliae no controle do Percevejo-do-colmo Tibraca limbativentris (Heteroptera: Pentatomidae) em lavoura de arroz irrigado. Cienc Rural 34:1681–1688. doi:10.1590/S0103-84782004000600003

    Article  Google Scholar 

  • Maruyama WI, Pinto AdeS, Gravena S (2002) Parasitóides de ovos de percevejos (Hemiptera: Heteroptera) em plantas daninhas. Ceres 49:453–459

    Google Scholar 

  • Moscardini VF, Moura APde, 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. doi:10.4025/actasciagron.v30i2.1723

    Google Scholar 

  • Moura APde, Carvalho GA, Rigitano RLde (2004) Efeito residual de novos inseticidas utilizados na cultura do tomateiro sobre Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae). Acta Sci Agron 26:231–237. doi:10.4025/actasciagron.v26i2.1888

    Article  CAS  Google Scholar 

  • Nörnberg SD, Grützmacher AD, Giolo FP, Stefanello Júnior G, Lima CAB, Grützmacher DD (2008) Seletividade de formulações de glyphosate aplicado nos estádios imaturos de Trichogramma pretiosum. Planta Daninha 26:611–617. doi:10.1590/S0100-83582008000300017

    Article  Google Scholar 

  • Pacheco DJP, Corrêa-Ferreira BS (2000) Parasitismo de Telenomus podisi Ashmead (Hymenoptera: Platygastridae) em populações de percevejos pragas da soja. An Soc Entomol Bras 29:295–302. doi:10.1590/S0301-80592000000200011

    Article  Google Scholar 

  • Pazini JdeB, Grützmacher AD, Martins JFdaS, Pasini RA, Rakes M (2016) Selectivity of pesticides used in rice crop on Telenomus podisi and Trichogramma pretiosum. Pesq Agropec Trop 46:327–335. doi:10.1590/1983-40632016v4640844

    Article  Google Scholar 

  • Peres WAA, Corrêa-Ferreira BS (2004) Methodology of mass multiplication of Telenomus podisi Ash. and Trissolcus basalis (Woll.) (Hymenoptera: Platygastridae) on eggs of Euschistus heros (Fab.) (Hemiptera: Pentatomidae). Neotrop Entomol 33:457–462. doi:10.1590/S1519-566X2004000400010

    Article  Google Scholar 

  • Pratissoli D, Milanez AM, Barbosa WF, Celestino FN, Andrade GS, Polanczyk RA (2010) Side effects of fungicides used in cucurbitaceous crop on Trichogramma atopovirilia Oatman & Platner (Hymenoptera: Trichogrammatidae). Chil J Agr Res 70:323–327

    Article  Google Scholar 

  • R Development Core Team (2015) R - A language and environment for statistical computing. rev. 3.2.0. R Foundation for Statistical Computing, Vienna, Austria, http://r-project.org Accessed 10 August 2015

    Google Scholar 

  • Riffel CT, Prando HF, Boff MIC (2010) Primeiro relato de ocorrência de Telenomus podisi (Ashmead) e Trissolcus urichi (Crawford) (Hymenoptera : Platygastridae) como parasitóides de ovos do percevejo-do-colmo-do-arroz, Tibraca limbativentris (Stål) (Hemiptera: Pentatomidae), em Santa Catarina. Neotrop Entomol 39:447–448. doi:10.1590/S1519-566X2010000300021

    Article  Google Scholar 

  • Saber M, Hejazi MJ, Kamali K, Moharramipour S (2005) Lethal and sublethal effects of fenitrothion and deltamethrin residues on the egg parasitoid Trissolcus grandis (Hymenoptera: Platygastridae). J Econ Entomol 98:35–40

    Article  CAS  Google Scholar 

  • Settle WH, Ariawan H, Astuti ET, Cahyana W, Hakim AL, Hindayana D, Lestari AS (1996) Managing tropical rice pests through conservation of generalist natural enemies and alternative prey. Ecology 77:1975–1988. doi:10.2307/2265694

    Article  Google Scholar 

  • Shea K, Nisbet RM, Murdoch WW, Yoo HJS (1996) The effect of egg limitation on stability in insect host-parasitoid population models. J Anim Ecol 65:743–755. doi:10.2307/5673

    Article  Google Scholar 

  • Silva CC, Laumann RA, Blassioli MC, Pareja M, Borges M (2008) Euschistus heros mass rearing technique for the multiplication of Telenomus podisi. Pesq agropec bras 43:575–580. doi:10.1590/S0100-204X2008000500004

    Article  Google Scholar 

  • Smaniotto LF, Gouvea Ade, Potrich M, Silva ERLda, Silva Jda, Pegorini CS (2013) Seletividade de produtos alternativos a Telenomus podisi Ashmed (Hymenoptera: Platygastridae). Semina 34:3295–3306. doi:10.5433/1679-0359.2013v34n6Supl1p3295

    Google Scholar 

  • Stecca CS, Bueno AF, Pasini A, Silva DM, Andrade K, Filho DMZ (2016) Side-effects of glyphosate to the parasitoid Telenomus remus Nixon (Hymenoptera: Platygastridae). Neotrop Entomol 45:192–200. doi:10.1007/s13744-016-0363-4

    Article  CAS  Google Scholar 

  • Stefanello Júnior GJ, Grützmacher AD, Grützmacher DD, Lima CAB, Dalmozo DOV, Paschoal MDF (2008) Seletividade de herbicidas registrados para a cultura do milho a adultos de Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). Planta Daninha 26:343–351. doi:10.1590/S0100-83582008000200010

    Article  Google Scholar 

  • Stefanello Júnior GJ, Grützmacher AD, Spagnol D, Pasini RA, Bonez C, Moreira DC (2012) Persistência de agrotóxicos utilizados na cultura do milho ao parasitoide Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae). Cienc Rural 42:17–23. doi:10.1590/S0103-84782012000100004

    Article  Google Scholar 

  • Turchen LM, Golin V, Butnariu AR, Guedes RN, Pereira MJ (2014) Selectivity of Annona (Annonaceae) extract on egg parasitoid Trissolcus urichi Crawford, 1913 (Hymenoptera: Platygastridae). Rev Colomb Entomol 40:176–180

    Google Scholar 

  • Turchen LM, Butnariu AR, Guedes RNC, Pereira MJB (2015) Lethal and sublethal effects of insecticides on the egg parasitoid Telenomus podisi (Hymenoptera: Platygastridae). J Econ Entomol 109:84–92. doi:10.1093/jee/tov273

    Article  Google Scholar 

  • Vinson SB (1997) Comportamento de seleção hospedeira de parasitóides de ovos, com ênfase na família Trichogrammatidae. In: Parra JRP, Zucchi RA (eds) Trichogramma e o controle biológico aplicado. FEALQ, Piracicaba, p 67–120

    Google Scholar 

  • Zachrisson B, Costa V, Bernal J (2014) Incidencia natural de parasitoides de huevos de Oebalus insularis Stal (Heteroptera: Pentatomidae) en Panamá. Idesia 32:119–121. doi:10.4067/S0718-34292014000200016

    Article  Google Scholar 

Download references

Acknowledgements

We thank to Dr. Mariane D’avila Rosenthal (Agronomic Engineer - UFPel/FAEM) for full assistance in mass rearing of insects in laboratory.

Funding

This work was financial supported by the Brazilian Federal Agency for the Support and Evaluation of Graduate Education (CAPES) and the National Council for Scientific and Technological Development (CNPq - Grant Number 308769/2013-9).

Author information

Authors and Affiliations

  1. Departamento de Fitossanidade, Universidade Federal de Pelotas (UFPel), Caixa Postal 354, CEP 96010-900, Capão-do-Leão, RS, Brazil

    Juliano de Bastos Pazini, Rafael Antonio Pasini, Matheus Rakes & Anderson Dionei Grützmacher

  2. Departamento de Estatística, Cidade Universitária, Universidade Federal de Santa Maria (UFSM), Bairro Camobi, CEP 97105-900, Santa Maria, RS, Brazil

    Enio Júnior Seidel

  3. Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA), Embrapa Clima Temperado, Caixa postal 403, CEP 96001-970, Pelotas, RS, Brazil

    José Francisco da Silva Martins

Authors
  1. Juliano de Bastos Pazini
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Rafael Antonio Pasini
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Enio Júnior Seidel
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Matheus Rakes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. José Francisco da Silva Martins
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Anderson Dionei Grützmacher
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Juliano de Bastos Pazini.

Ethics declarations

Conflict of interest

The authors declare that they have no competing interests.

Ethical approval

This article does not contain any studies with human participants or animals performed by any of the authors.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Pazini, J.d.B., Pasini, R., Seidel, E. et al. Side-effects of pesticides used in irrigated rice areas on Telenomus podisi Ashmead (Hymenoptera: Platygastridae). Ecotoxicology 26, 782–791 (2017). https://doi.org/10.1007/s10646-017-1809-0

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10646-017-1809-0

Keywords

Search

Navigation