Abstract
We evaluated the lethal and sublethal effects of azoxystrobin, cyhalofop-butyl, and thiamethoxam on Telenomus podisi after spraying rice plants in a greenhouse, as well as the degradation kinetics of these compounds over time. Pesticides were sprayed at 50 and 100% of the maximum field recommended concentration for the crop (MFRC). At 0, 5, 10, and 20 days after application of the treatments (DAAT), T. podisi was exposed to leaves containing dry pesticide residues. On these same dates, rice leaves from each treatment were collected for determination of pesticide residues by UHPLC–MS/MS. Based on the results for mortality, parasitism, emergence, and sex ratio of T. podisi, the effects were grouped using a reduction coefficient (Ex) and classified according to the scale of the International Organization for Biological and Integrated Control (IOBC). The fungicide azoxystrobin (at 50 and 100% MFRC) was the only one classified as harmless (Class 1). The herbicide cyhalofop-butyl was classified as slightly harmful (Class 2) to T. podisi until 5 DAAT. The insecticide thiamethoxam (50 and 100% MFRC), up to 5 DAAT, was classified as harmful (Class 4) on T. podisi. Regarding residue, the initial concentrations (0 DAAT) of azoxystrobin, cyhalofop-butyl, and thiamethoxam at 100% MFRC in rice leaves were 102.14, 210.09, and 36.93 mg kg−1, respectively. At 50% MFRC, initial waste was approximately half that extracted at 100% MFRC. The estimated half-lives (DT50) were approximately 17, 4, and 5 days for azoxystrobin, cyhalofop-butyl, and thiamethoxam, respectively. Furthermore, we found a positive correlation between effects and residues.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Amarasekare KG, Shearer PW, Mills NJ (2016) Testing the selectivity of pesticides effects on natural enemies in laboratory bioassays. Biol Control 102:7–16. https://doi.org/10.1016/j.biocontrol.2015.10.015
Andres A, Freitas GD, Concenço G, Melo PTBS, Ferreira FA (2007) Desempenho do cultivar de arroz BRS-Pelota e controle de capim-arroz (Echinochloa sp.) submetidos a quatro épocas de entrada d’água após aplicação de doses reduzidas de herbicidas. Planta Daninha 25:859–867. https://doi.org/10.1590/S0100-83582007000400023
Bayram A, Salerno G, Onofri A, Conti E (2010) Sub-lethal effects of two pyrethroids on biological parameters and behavioral responses to host cues in the egg parasitoid Telenomus busseolae. Biol Control 53:153–160. https://doi.org/10.1016/j.biocontrol.2009.09.012
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. https://doi.org/10.1016/j.chemosphere.2011.12.082
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. https://doi.org/10.1371/journal.pone.0076548
Boesten JJTI, Aden K, Beigel C, Beulke S, Dust M, Dyson JS, Fomsgaard IS, Jones RL, Karlsson S, Van der Linden AMA, Richter O, Magrans JO, Soulas G (2006). The Final Report of the Work Group on Degradation Kinetics of FOCUS (Forum for the Coordination of Pesticide Fate Models and Their Use). Guidance Document on Estimating Persistence and Degradation Kinetics from Environmental Fate Studies on Pesticides in EU Registration Sanco/10058/2005. version 2.0, June 2006
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. https://doi.org/10.1590/0100-5405/2012
Brasil. Ministério da Agricultura, Pecuária e Abastecimento (2020) Agrofit. http://agrofit.agricultura.gov.br/agrofit_cons/principal_agrofit_cons. Accessed in 05 February 2020.
Bueno ADF, Carvalho GA, Santos ACD, Sosa-Gómez DR, Silva DMD (2017) Pesticide selectivity to natural enemies: challenges and constraints for research and field recommendation. Cienc Rural 47:e20160829. https://doi.org/10.1590/0103-8478cr20160829
Bueno ADF, Braz EC, Favetti BM, França-Neto J, Silva GV (2020) Release of the egg parasitoid Telenomus podisi to manage the Neotropical Brown Stink Bug, Euschistus heros, in soybean production. Crop Protec 137:105310. https://doi.org/10.1016/j.cropro.2020.105310
Carvalho GA, Grützmacher AD, Passos LC, Oliveira RL (2019). Physiological and ecological selectivity of pesticides for natural enemies of insects. In: Souza B, Vázquez L, Marucci R (Eds.) Natural enemies of insect pests in neotropical agroecosystems. Springer, pp 469–478.
Casida JE, Durkin KA (2013) Neuroactive insecticides: targets, selectivity, resistance, and secondary effects. Annu Rev Entomol 58:99–117. https://doi.org/10.1146/annurev-ento-120811-153645
Chapman RF, Simpson SJ, Douglas A (2013) The insects structure and function, 5th edn. Cambridge University Press, New York USA
CONAB. Companhia Nacional De Abastecimento. Acompanhamento de safra brasileira: grãos, décimo segundo levantamento, setembro 2020. Brasília: Conab, 2020. Disponível em: < https://www.conab.gov.br/info-agro/safras>. Accessed in 18 November 2020.
Counce PA, Keisling TC, Mitchell A (2000) A uniform, objective, and adaptive system for expressing rice development. Crop Sci 40:436–443. https://doi.org/10.2135/cropsci2000.402436x
Dean R, Van Kan JA, Pretorius ZA, Hammond-Kosack KE, Di Pietro A, Spanu PD, Rudd JJ, Dickman M, Kahmann R, Ellis J, Foster GD (2012) The Top 10 fungal pathogens in molecular plant pathology. Mol Plant Pathol 13:414–430. https://doi.org/10.1111/j.1364-3703.2011.00783.x
Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52:81–106. https://doi.org/10.1146/annurev.ento.52.110405.091440
FAOSTAT. Food and Agriculture Organization of the United Nations - Statistics division. Food and agricultural commodities production/Countries by commodity, Rome, Italy, 2020. Available in: http://www.fao.org/faostat/en/#rankings/countries_by_commodity Accessed in 18 November 2020.
Farias PM, 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. https://doi.org/10.1590/S0085-56262012005000044
Giolo FP, Grützmacher AD, Procópio SO, Manzoni CG, Lima CAB, Nörnberg SD (2005) Side-effects of glyphosate formulations on Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). Planta Daninha 23:457–462. https://doi.org/10.1590/S0100-83582005000300009
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. https://doi.org/10.1590/S0103-84782005000200034
Hirooka T, Ishii H (2013) Chemical control of plant diseases. J Gen Plant Pathol 79:390–401. https://doi.org/10.1007/s10327-013-0470-6
Idalgo TDN, Sant’Ana J, Redaelli LR, Pires PDS (2013) Egg parasitism of Tibraca limbativentris Stål (Hemiptera: Pentatomidae) in irrigated rice crops, Eldorado do Sul, RS. Arq Inst Biol 80:453–456. https://doi.org/10.1590/S1808-16572013000400014
Itoiz ES, Fantke P, Juraske R, Kounina A, Vallejo AA (2012) Deposition and residues of azoxystrobin and imidacloprid on greenhouse lettuce with implications for human consumption. Chemosphere 89:1034–1041. https://doi.org/10.1016/j.chemosphere.2012.05.066
Jacobsen RE, Fantke P, Trapp S (2015) Analysing half-lives for pesticide dissipation in plants. SAR QSAR Environ Res 26:325–342. https://doi.org/10.1080/1062936X.2015.1034772
Kemmerich M, Bernardi G, Adaime MB, Zanella R, Prestes OD (2015) A simple and efficient method for imidazolinone herbicides determination in soil by ultra-high performance liquidchromatography–tandem mass spectrometry. J Chromatogr A 1412:82–89. https://doi.org/10.1016/j.chroma.2015.08.005
Maciel AAS, Lemos RNS, Souza JR, Costa VA, Barrigossi JAF, Chagas EF (2007) Natural egg parasitism of Tibraca limbativentris Stal (Hemiptera: Pentatomidae) in rice crop in the State of Maranhão, Brazil. Neotrop Entomol 36:616–618. https://doi.org/10.1590/S1519-566X2007000400023
Magano DA, Krolow IRC, Grützmacher AD, Panozzo LE, Armas FS, Zimmer M (2013) Efeitos secundários de herbicidas aplicados em soja sobre Trichogramma pretiosum. Pesq Agropec Gaúcha 19:49–56
Marchesi C, Chauhan BS (2019) The efficacy of chemical options to control Echinochloa crus-galli in dry-seeded rice under alternative irrigation management and field layout. Crop Prot 118:72–78. https://doi.org/10.1016/j.cropro.2018.12.016
Martins JFS, Barrigossi JAF, Oliveira JV, Cunha US (2009). Situação do manejo integrado de insetos-praga na cultura do arroz no Brasil. Pelotas: Embrapa Clima Temperado, 2009. 40 p. (Embrapa Temperate Climate. Documents, 290).
Medeiros MA, Schimidt FVG, 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. https://doi.org/10.1590/S0301-80591997000200026
Morales SI, Martínez AM, Figueroa JI, Campos-García J, Gómez-Tagle A, Lobit P, Smagghe G, Pineda S (2019) Foliar persistence and residual activity of four insecticides of different mode of action on the predator Engytatus varians (Hemiptera: Miridae). Chemosphere 235:76–83. https://doi.org/10.1016/j.chemosphere.2019.06.163
Müller C (2018) Impacts of sublethal insecticide exposure on insects - Facts and knowledge gaps. Basic Appl Ecol 30:1–10. https://doi.org/10.1016/j.baae.2018.05.001
NCBI. National Center for Biotechnology Information (2021). PubChem Compound Summary for CID 180089, Cyhalofop-butyl. Retrieved January 20, 2021 from https://pubchem.ncbi.nlm.nih.gov/compound/Cyhalofop-butyl
Neto AJM, Souza JR, Santiago CM, Pereira FAZ, Lima MHF, Wengrat APGS (2020). Primeiro registro de parasitoides de ovos de Oebalus poecilus (Dallas, 1851) (Hemiptera: Pentatomidae) em arroz no Maranhão, Brasil. Entomological Communications 2: ec02032. https://doi.org/10.37486/2675-1305.ec02032e-IS
Olajumoke B, Juraimi AS, Uddin M, Husni MH, Alam M (2016) Competitive ability of cultivated rice against weedy rice biotypes: A review. Chil J Agric Res 76:243–252. https://doi.org/10.4067/S0718-58392016000200015
Parra JRP (2019). Controle Biológico na Agricultura Brasileira. Entomol Commun 1:ec01002. https://doi.org/10.37486/2675-1305.ec0100
Pasini RA, Grützmacher AD, Spagnol D, Armas FS, Normberg AV, Carvalho AJS (2017) Residual action of pesticides sprayed on corn plants on Trichogramma pretiosum. Rev Ceres 64:242–249. https://doi.org/10.1590/0034-737x201764030004
Pasini RA, Rakes M, Castilhos RV, Armas FS, Pazini JB, Zantedeschi R, Grützmacher AD (2020) Residual action of five insecticides on larvae and adults of the neotropical predators Chrysoperla externa (Neuroptera: Chrysopidae) and Eriopis connexa (Coleoptera: Coccinellidae). Ecotoxicology. https://doi.org/10.1007/s10646-020-02314-0
Patel DT, Stout MJ, Fuxa JR (2006) Effects of rice panicle age on quantitative and qualitative injury by the rice stink bug (Hemiptera: Pentatomidae). Fla Entomol 89:321–327
Pazini JB, Grützmacher AD, Martins JFS, Pasini RA, Rakes M (2016) Selectivity of pesticides used in rice crop on Telenomus podisi and Trichogramma pretiosum. Pesqui Agropecu Trop 46:327–335. https://doi.org/10.1590/1983-40632016v4640844
Pazini JB, Pasini RA, Seidel EJ, Rakes M, Martins JFS, Grützmacher AD (2017a) Side-effects of pesticides used in irrigated rice areas on Telenomus podisi Ashmead (Hymenoptera: Platygastridae). Ecotoxicology 26:782–791. https://doi.org/10.1007/s10646-017-1809-0
Pazini JB, Pasini RA, Rakes M, Armas FS, Seidel EJ, Martins JFS, Grützmacher AD (2017b) Toxicity of pesticide tank mixtures from rice crops against Telenomus podisi Ashmead (Hymenoptera: Platygastridae). Neotrop Entomol 46:461–470. https://doi.org/10.1007/s13744-017-0483-5
Pazini JB, Padilha AC, Cagliari D, Bueno FA, Rakes M, Zotti MJ, Martins JFS, Grützmacher AD (2019). Differential impacts of pesticides on Euschistus heros (Hem.: Pentatomidae) and its parasitoid Telenomus podisi (Hym.: Platygastridae). Sci Rep 9:6544. https://doi.org/10.1038/s41598-019-42975-4
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. https://doi.org/10.1590/S1519-566X2004000400010
R Development Core Team. (2020) R - A language and environment for statistical computing. version 3.6.2. http://r-project.org
Rakes M, Grützmacher AD, Pazini JB, Pasini RA, Schaedler CE (2017) Physicochemical compatibility of agrochemical mixtures in spray tanks for paddy field rice crops. Planta Daninha 35:e017165185. https://doi.org/10.1590/s0100-83582017350100090
Rakes M, Pasini RA, Morais MC, Araújo MB, Pazini JB, Seidel EJ, Bernardi D, Grützmacher AD (2020) Pesticide selectivity to the parasitoid Trichogramma pretiosum: A pattern 10-year database and its implications for Integrated Pest Management. Ecotox Environ Safe 208:111504. https://doi.org/10.1016/j.ecoenv.2020.111504
Reunião Técnica Da Cultura do Arroz Irrigado (2018) Farroupilha. Arroz irrigado: recomendações técnicas da pesquisa para o Sul do Brasil. Cachoeirinha: SOSBAI (32) 209 p.
Ricupero M, Desneux N, Zappalà L, Biondi A (2020) Target and non-target impact of systemic insecticides on a polyphagous aphid pest and its parasitoid. Chemosphere 247:125728. https://doi.org/10.1016/j.chemosphere.2019.125728
Riffel CT, Prando HF, Boff MIC (2010) First record of Telenomus podisi (Ashmead) and Trissolcus urichi (Crawford) (Hymenoptera: Scelionidae) Parasitizing eggs of the Rice Stem Bug, Tibraca limbativentris (Stål) (Hemiptera: Pentatomidae), in Santa Catarina, Brazil. Neotrop Entomol 39:447–448. https://doi.org/10.1590/S1519-566X2010000300021
Rizzetti TM, Kemmerich M, Martins ML, Prestes OD, Adaime MB, Zanella R (2016) Optimization of a QuEChERS based method by means of central composite design for pesticide multiresidue determination in orange juice by UHPLC-MS/MS. Food Chem 196:25–33. https://doi.org/10.1016/j.foodchem.2015.09.010
Santana MV, Macedo RDS, Santos TTMD, Barrigossi JA (2018) Economic injury levels and economic thresholds for Tibraca limbativentris (Hemiptera: Pentatomidae) on paddy rice based on insect-days. J Econ Entomol 111:2242–2249. https://doi.org/10.1093/jee/toy208
SANTE, EUROPEAN COMMISSION (2015). Guidance document on analytical quality control and validation procedures for pesticide residues analysis in food and feed Document SANTE/11945/2015.
Santos AB, Stone LF, Vieira NRA (2006). A cultura do arroz no Brasil. 2ª ed. ampl. - Santo Antônio de Goiás: Embrapa Arroz e Feijão. 1000 p.
Seidel EJ, Pazini JB, Tomazella VLD, Vieira AMC, Silva FF, Martins JFS, Barrigossi JAF (2020) Predicting rice stem stink bug population dynamics based on GAMLSS Models. Environ Entomol 49:1145–1154. https://doi.org/10.1093/ee/nvaa091
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. https://doi.org/10.1590/S0100-204X2008000500004
Silva GV, Bueno ADF, Favetti BM, Neves PMOJ (2018) Selectivity of chlorantraniliprole and lambda-cyhalothrin to the egg parasitoid Telenomus podisi (Hymenoptera: Platygastridae). Semin Ciênc Agrar 39:549–564. https://doi.org/10.5433/1679-0359.2018v39n2p549
Silva GS, Jahnke SM, Johnson NF (2020) Riparian forest fragments in rice fields under different management: differences on hymenopteran parasitoids diversity. Braz J Biol 80:122–132. https://doi.org/10.1590/1519-6984.194760
Silva NN, Sousa KK, Silva PHS, Querino RB (2021). New Records of Egg Parasitoids of Stink Bugs (Hemiptera: Pentatomidae) on Rice in Piauí, Brazil: Rate Parasitism, Incidence and Seasonality. Entomological Communications 3:ec03020. https://doi.org/10.37486/2675-1305.ec03020
Soares MA, Campos MR, Passos LC, Carvalho GA, Haro MM, Lavoir AV, Biondi A, Zappalà L, Desneux N (2019) Botanical insecticide and natural enemies: a potential combination for pest management against Tuta absoluta. J Pest Sci 92:1433–1443. https://doi.org/10.1007/s10340-018-01074-5
Stecca CS, Bueno ADF, Pasini A, Silva DM, Andrade K, Zirondi Filho DM (2018) Impact of insecticides used in soybean crops to the egg parasitoid Telenomus podisi (Hymenoptera: Platygastridae). Neotrop Entomol 47:281–291. https://doi.org/10.1007/s13744-017-0552-9
Stefanello Júnior GJ, Grützmacher AD, Spagnol D, Pasini RA, Bonez C, Moreira DC (2012) Persistence of pesticides used in corn field to the parasitoid Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae). Cienc Rural. https://doi.org/10.1590/S0103-84782012000100004
Torres JB, Bueno ADF (2018) Conservation biological control using selective insecticides–a valuable tool for IPM. Biol Control 126:53–64. https://doi.org/10.1016/j.biocontrol.2018.07.012
Turchen LM, Golin V, Butnariu AR, Guedes RN, Pereira MJ (2015) Lethal and sublethal effects of insecticides on the egg parasitoid Telenomus podisi (Hymenoptera: Platygastridae). J Econ Entomol 109:84–92. https://doi.org/10.1093/jee/tov273
Viera MS, Rizzetti TM, de Souza MP, Martins ML, Prestes OD, Adaime MB, Zanella R (2017) Multiresidue determination of pesticides in crop plants by the quick, easy, cheap, effective, rugged, and safe method and ultra-high-performance liquid chromatography tandem mass spectrometry using a calibration based on a single level standard addition in the sample. J Chromatogr A 1526:119–127. https://doi.org/10.1016/j.chroma.2017.10.048
Wang HY, Yang Y, Su JY, Shen JL, Gao CF, Zhu YC (2008) Assessment of the impact of insecticides on Anagrus nilaparvatae (Pang et Wang) (Hymenoptera: Mymanidae), an egg parasitoid of the rice planthopper, Nilaparvata lugens (Hemiptera: Delphacidae). Crop Prot 27:514–522. https://doi.org/10.1016/j.cropro.2007.08.004
Wang X, Xiang Z, Yan X, Sun H, Li Y, Pan C (2013) Dissipation rate and residual fate of thiamethoxam in tobacco leaves and soil exposed to field treatments. B Environ Contam Tox 91:246–250. https://doi.org/10.1007/s00128-013-1043-2
Weber NC, Redaelli LR, Santos EMD, Werner FM (2020) Quantitative and qualitative damages of Oebalus poecilus on irrigated rice in southern Brazil. Rev Ceres 67:126–132. https://doi.org/10.1590/0034-737x202067020005
Wu J, Wang K, Zhang Y, Zhang H (2014) Determination and study on dissipation and residue determination of cyhalofop-butyl and its metabolite using HPLC-MS/MS in a rice ecosystem. Environ Monit Assess 186:6959–6967. https://doi.org/10.1007/s10661-014-3902-7
Zantedeschi R, Grützmacher AD, Pazini JB, Bueno FA, Machado LL (2018) Selectivity of pesticides registered for soybean crop on Telenomus podisi and Trissolcus basalis. Pesqui Agropecu Trop 48:52–58. https://doi.org/10.1590/1983-40632018v4850348
Acknowledgements
The authors would like to thank the National Council for Scientific and Technological Development (CNPq) and Coordination for the Improvement of Higher Education Personnel (CAPES) for their financial support for research execution and scholarships provisions.
Funding
National Council for Scientific and Technological Development (CNPq) code 001.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare no conflict of interest.
Additional information
Communicated by Chris Cutler.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Rakes, M., Pasini, R.A., Morais, M.C. et al. Residual effects and foliar persistence of pesticides used in irrigated rice on the parasitoid Telenomus podisi (Hymenoptera: Platygastridae). J Pest Sci 95, 1121–1133 (2022). https://doi.org/10.1007/s10340-021-01436-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10340-021-01436-6