Abstract
The objective of this study was to evaluate possible side effects of insecticides used in soybean crops on pupae and adults of the egg parasitoid Telenomus podisi Ashmead (Hymenoptera: Platygastridae) under laboratory conditions. The protocol was adapted from standard methodology stablished by the Pesticides and Beneficial Organisms Working Group of the International Organization for Biological and integrated Control (IOBC) for Trichogramma cacoeciae (Marchal) (Hymenoptera: Trichogrammatidae). All tested benzoylureas, diacylhydrazines, diamides and spinosins as well as pyrethroid beta-cyfluthrin were harmless to T. podisi pupae and adults, and therefore, can be used in IPM without damage to this biological control agent. The tested organophosphate, pyrethroids (except beta-cyfluthrin) and its combinations with either neonicotinoids or diamides triggered deleterious effects on at least one of the life stages of the parasitoid and should, whenever possible, be replaced by other insecticides more selective to natural enemies.
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References
Ávila CJ, Nakano O (1999) Efeito do regulador de crescimento lufenuron na reprodução de Diabrotica speciosa (Germar) (Coleoptera: Chrysomelidae). An Soc Entomol Bras 28:293–299
Bret BL, Larson LL, Schoonover JR, Sparks TC, Thompson GD (1997) Biological properties of Spinosad. Down to Earth 52:6–13
Bueno AF, Bueno RCOF, Parra JRP, Vieira SS (2008) Effects of pesticides used in soybean crops to the egg parasitoid Trichogramma pretiosum. Ciênc Rural 38:1495–1503
Burr IW, Foster LA (1972) A test for equality of variances. University of Purdue, West Lafayette, 26p
Carmo EL, Bueno AF, Bueno RCOF (2010) Pesticide selectivity for the insect egg parasitoid Telenomus remus. BioControl 55:455–464
Carmo EL, Bueno AF, Bueno RCOF, Vierira SS, Gobbi AL, Vasco FR (2009) Seletividade de diferentes agrotóxicos usados na cultura da soja ao parasitoide de ovos Telenomus remus. Ciênc Rural 39:2293–2300
Carvalho AJFGA, Lasmar MBO (2006) Seletividade de inseticidas usados na cultura da macieira a duas populações de Chrysoperla externa (Hagen, 1861) (Neuropetra: Crysopidae). Ciênc Rural 36:378–384
Carvalho GA, Parra JRP, Baptista GC (1999) Ação residual de alguns inseticidas pulverizados em plantas de tomateiro sobre duas linhagens de Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae) em casa-de-vegetação. Ciênc Agrotec 23:770–775
Carvalho GA, Rezende DT, Moura AP, Moscardini VF, Lasmar O, Souza JR (2005) Selectivity of flubendiamide, a new insecticide used to control tomato pests in Brazil to Trichogramma pretiosum Riley (Hym., Trichogrammatidae). Egg Parasit News 17: 27
Corrêa-Ferreira BS, Azevedo J (2002) Soybean seed damage by different species of stink bugs. Agric For Entomol 4:145–150
Corrêa-Ferreira BS, Zamataro CEO (1989) Capacidade reprodutiva e longevidade dos parasitoides de ovos Trissolcus basalis (Wollaston) e Trissolcus mitsukurii Ashmead (Hymenoptera: Scelionidae). Rev Bras Biol 49:621–626
Croft BA (1990) Arthropod biological control agents and pesticides. Wiley-Interscience, New York, USA
Dhadialla TS, Carlson GR, Le DP (1998) New insecticides with ecdysteroidal and juvenile hormone activity. Annu Rev Entomol 43:545–569
Ebbinghaus-Kintscher U, Lummen P, Raming K, Masaki T, Yasokawa N (2007) Flubendiamide, the first insecticide with a novel mode of action on insect ryanodine receptors. Pflanzenschutz-Nachr Bayer 60:117–140
Fernandes FL, Bacci L, Fernandes MS (2010) Impact and selectivity of insecticides to predators and parasitoids. EntomoBrasilis 3:1–10
Foerster LA, Doetzer AK, Castro LCF (2004) Emergence, longevity and fecundity of Trissolcus basalis and Telenomus podisi after cold storage in the pupal stage. Pesq. Agropec Bras 39:841–845
Foerster LA, Parra JRP, Botelho PSM, Corrêa-Ferreira BS, Bento JMS (2002) Seletividade de inseticidas a predadores e parasitoides. In: Parra JRP et al (eds) Controle Biológico no Brasil: parasitoides e predadores. Manole, São Paulo, pp 95–114
Godoy KB, Ávila CJ (2000) Parasitismo natural em ovos de dois percevejos da soja, na região de Dourados, MS. Rev Agric (Piracicaba) 75:271–279
Grande MLM, Silva DM, Bueno AF, Queiroz AP, Ventura UM (2016) O que muda em seletividade de inseticidas a Trichogramma pretiosum após a detecção de Helicoverpa armigera no Brasil? XXXV Reunião de Pesquisa de Soja, Londrina, PR:73–76
Hassan SA (1992) Guideline for the evaluation of side-effects of plant protection product on Trichogramma cacoeciae. In: Hassan, SA (Ed.). Guidelines for testing the effects of pesticides on benefi cial organisms: description of test methods. IOBC/WPRS Bulletin, 15: 18–39
Hassan SA, Bigler F, Blaisinger P, Bogenschütz H, Brun J, Chiverton P, Dickler E, Easterbrook MA, Edwards PJ, Englert WD, Firth SL, Huang P, Inglesfield C, Klingauf F, Kühner C, Ledieu MS, Naton E, Oomen PA, Overmeer WPJ, Plevoets P, Reboulet JN, Rieckmann W, Samsoe-Petersen L, Shires SW, Staubli A, Stevenson J, Tuset JJ, Vanwetswinkel G, Van Zon AQ (1985) Standard methods to test the side-effects of pesticides on natural enemies of insects and mites developed by the IOBC/WPRS Working Group ‘Pesticides and Benefitial Organisms’. EPPO Bulletin 15:214–255
Herbert JJ, Toews MD (2011) Seasonal abundance and population structure of brown stink bug (Hemiptera: Pentatomidae) in farmscapes containing corn, cotton, peanut, and soybean. Ann Entomol Soc Am 104:909–918
Jeschke P, Nauen R (2008) Neonicotinoids—from zero to hero in insecticide chemistry. Pest Manag Sci 64:1084–1098
Jones Junior WA (1979) The distribution and ecology of pentatomid pests of soybeans in South Carolina. 150p
Lahm GP, Cordova D, Barry JD (2009) New and selective ryanodine receptor activators for insect control. Bioorg Med Chem 17:4127–4133
Leite GLD, Picanço M, Guedes RNC, Gusmão MR (1998) Selectivity of insecticides with and without mineral oil to Brachygastra lecheguana (Hymenoptera: Vespidae): a predator of Tuta absoluta (Lepidoptera: Gelechiidae). Ceiba 39:3–6
Masuda T, Goldsmith PD (2009) World soybean production: area harvested, yield, and long-term projections. Int Food Agribus Man Rev 12:145–164
Medeiros MA, Schimidt FV, Loiácono MS, Carvalho VF, Borges M (1997) Parasitismo e predação em ovos de Euschistus heros (Fab.) (Heteroptera: Pentatomidae) no Distrito Federal, Brasil. An Soc Entomol Brasil 26:397–401
Moreira GRP, Becker M (1986) Mortalidade de Nezara viridula (Linnaeus, 1758) (Heteroptera: Pentatomidae) no estágio de ovo na cultura da soja: II. Parasitóides. An Soc Entomol Bras 15:291–308
Nakama PA, Foerster LA (2001) Efeito da alternância de temperaturas no desenvolvimento e emergência de Trissolcus basalis (Wollaston) e Telenomus podisi Ashmead (Hymenoptera: Scelionidae). Neotrop Entomol 30:269–275
Oerke EC (2006) Crop losses to pests. J Agr Sci 144:31–43
Oerke EC, Dehne HW (2004) Safeguarding production—losses in major crops and the role of crop protection. Crop Prot 23:275–285
Pacheco DJP, Corrêa-Ferreira BS (2000) Parasitismo de Telenomus podisi Ashmead (Hymenoptera: Scelionidae) em populações de percevejos pragas da soja. An Soc Entomol Bras 29:295–302
Panizzi AR (1997) Wild hosts of pentatomids: ecological significance and role in their pest status on crops. Annu Rev Entomol 42:99–122
Panizzi AR, Corrêa-Ferreira BS (1997) Dynamics in the insect fauna adaptation to soybean in the tropics. Trends Entomol 1:71–88
Pazini JB, Pasini RA, Rakes M, de Armas FS, Seidel EJ, Martins JFS, Grützmacher AD (2017) Toxicity of pesticide tank mixtures from rice crops against Telenomus podisi Ashmead (Hymenoptera: Platygastridae). Neotrop Entomol [Epub ahead of print]. doi:10.1007/s13744-017-0483-5
Perez WAA, Corrêa-Ferreira BS (2004) Methodology of mass multiplication of Telenomus podisi ash. And Trissolcus basalis (Woll.) (Hymenoptera: Scelionidae) on eggs of Euschistus heros (fab.) (Hemiptera: Pentatomidae). Neotrop Entomol 33:457–462
Picanço MC, Ribeiro LJ, Leite GLD, Zanuncio JC (1997) Seletividade de inseticidas a Podisus nigrispinus predador de Ascia monuste orseis. Pesq Agrop Bras 32:369–372
Pratissoli D, Thuler RT, Pereira FF, Reis EF, Ferreira AT (2004) Ação transovariana de lufenuron (50 G/L) sobre adultos de Spodoptera frugiperda (J. E. Smith) (Lepidoptera: Noctuidae) e seu efeito sobre o parasitóide de ovos Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). Cienc Agrotec 28:9–14
Preetha G, Stanley J, Suresh S, Kuttalam S, Samiyappan R (2009) Toxicity of selected insecticides to Trichogramma hilonis: assessing their safety in the rice ecosystem. Phytoparasitica 37:209–215
Reynolds SE (1987) The cuticule, growth regulators and moulting in insects: the essential background to the action of acylurea insecticides. Pestic Sci 20:131–146
Rezende DT, Carvalho GA, Moura AP, Moscardini VF, Souza JR, Lasmar O (2005) Side effects of some pesticides used in maize crops in Brazil to the egg parasitoid Trichogramma atopovirilia (Oatman & Platner) (Hymenoptera: Trichogrammatidae). Egg Parasit News 17:28–29
Ruberson JR, Tillman PG (1999) Effect of selected insecticides on natural enemies in cotton: laboratory studies, pp. 1210–1213. In: Proceedings. Beltwide Cotton Conference, 3–7 January 1999, New Orleans. LA. National Cotton Council, Orlando, Florida, pp 1210–1212
Santos AC, Bueno AF, Bueno RCOF (2006) Seletividade de defensivos agrícolas aos inimigos naturais In: Pinto AS, Nava DE, Rossi MM. Malerbo-Souza DT (eds) Controle Biológico de pragas na prática 1:221–227
SAS Institute (2009) SAS user’s guide: statistics: version 8.2. 6 ed. Cary
Shapiro SS, Wilk MB (1965) An analysis of variance test for normality. Biometrika 52:591–611
Silva MTB, Corso IC, Belarmino LC, Link D, Tonet GL, Gomes AS, Santos B (1988) Avaliação de inseticidas sobre predadores das pragas da soja, em dez anos agrícolas, no Brasil. Trigo e Soja 96:3–16
Sosa-Gómez DR, Corso IC, Morales L (2001) Insecticide resistance to endosulfan, monocrotophos and methamidophos in the neotropical brown stink bug, Euschistus heros (F.) Neot Entomol 30:317–320
Sosa-Gómez DR, Silva JJD (2010) Neotropical brown stink bug (Euschistus heros) resistance to methamidophos in Paraná, Brazil. Pesq Agropec Bras 45:767–769
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
Júnior S, Grützmacher AD, Grützmacher DD, Dalmazo GO, Paschoal MDF, Härter WR (2008) Efeito de inseticidas usados na cultura do milho sobre a capacidade de parasitismo de Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae). Arq Inst Biol:75187–75194
Stock D, Holloway PJ (1993) Possible mechanisms for surfactant-induced foliar uptake of agrochemicals. Pest Sci 38:165–177
Talebi-Jahromi K (2007) Pesticide toxicology. University of Tehran Publication, Tehran
Williams T, Valle J, Viñuela E (2003) Is the naturally derived insecticide Spinosad® compatible with insect natural enemies? Biocontrol Sci Tech 13:459–475
Zotti MJ, Grützmacher AD, Grützmacher DD, Castilhos RV, Martins JFS (2010) Seletividade de inseticidas utilizados na cultura do milho para ovos e ninfas do predador Doru lineare (Eschscholts, 1822) (Dermaptera: Forficulidae). Arq Inst Biol 77:111–118
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The authors would like to thank Embrapa Soja and the “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES)” for the funds that supported this research. This paper was approved for publication by the Editorial Board of Embrapa Soja.
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Edited by Moisés J Zotti – UFPel
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Stecca, C.S., Bueno, A.F., Pasini, A. et al. Impact of Insecticides Used in Soybean Crops to the Egg Parasitoid Telenomus podisi (Hymenoptera: Platygastridae). Neotrop Entomol 47, 281–291 (2018). https://doi.org/10.1007/s13744-017-0552-9
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DOI: https://doi.org/10.1007/s13744-017-0552-9