Abstract
Advances in agriculture include integrated methods of controlling pests, diseases, and weeds with biocontrollers, which are constantly increasing, along with herbicides. The objective is to present a systematic review of the main reports of herbicide effects on non-target organisms used in applied biological control and those naturally occurring in the ecosystems controlling pests. The categories were divided into predatory and parasitoid arthropods. Three hundred and fifty reports were analyzed, being 58.3% with parasitoids and 41.7% with predators. Lethal or sublethal effects of herbicides on reproduction, predation, genotoxicity, and abundance of biological control organisms have been reported. Two hundred and four reports of the impact of herbicides on parasitoids were analyzed. The largest number of reports was with parasitoids of the genus Trichogramma, with wide use in managing pests of the herbicide-tolerant transgenic plants. Most tests evaluating effects on parasitism, emergence, and mortality of natural enemies subjected to herbicides are with parasitoids of Lepidoptera eggs with a high diversity and use in managing these pests in different crops. Additive and synergistic effects of molecules increase the risks of herbicide mixtures. Herbicide use for weed management must integrate other control methods, as the chemical can impact natural enemies, reducing the biological control of pests.
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References
Adu-Yeboah P, Malone JM, Fleet B, Gill G, Preston C (2020) EPSPS gene amplification confers resistance to glyphosate resistant populations of Hordeum glaucum Stued (northern barley grass) in South Australia. Pest Manag Sci 76(4):1214–1221. https://doi.org/10.1002/ps.5671
Ahn YJ, Kim YJ, Yoo JK (2001) Toxicity of the herbicide glufosinate-ammonium to predatory insects and mites of Tetranychus urticae (Acari: Tetranychidae) under laboratory conditions. J Econ Entomol 94(1):157–161. https://doi.org/10.1603/0022-0493-94.1.157
Albajes R, Lumbierres B, Pons X (2011) Two heteropteran predators in relation to weed management in herbicide-tolerant corn. Biol Control 59(1):30–36. https://doi.org/10.1016/j.biocontrol.2011.03.008
Anderson J, Ellsworth PC, Faria JC, Head GP, Owen MD, Pilcher CD, Shelton AM, Meissle M (2019) Genetically engineered crops: importance of diversified integrated pest management for agricultural sustainability. Front Bioeng Biotechnol 7(1):24. https://doi.org/10.3389/fbioe.2019.00024
Araujo RA, Badji CA, Correa AS, Ladeira JA, Guedes RNC (2004) Impacto causado por deltametrina em coleopteros de superfıcie do solo associados a cultura do milho em sistemas de plantio direto e convencional. Neotrop Entomol 33(3):379–385. https://doi.org/10.1590/S1519-566X2004000300017
Badji CA, Guedes RNC, Silva AA, Correa AS, Queiroz MELR, Michereff-Filho M (2007) Non-target of deltamethrin on soil arthropods of maize fields under conventional and no-tillage cultivation. J Appl Entomol 131(1):50–58. https://doi.org/10.1111/j.1439-0418.2006.01118.x
Bain C, Selfa T, Dandachi T, Velardi S (2017) ‘Superweeds’ or ‘survivors’? Framing the problem of glyphosate resistant weeds and genetically engineered crops. J Rural Stud 51(1):211–221. https://doi.org/10.1016/j.jrurstud.2017.03.003
Baker BP, Green TA, Loker AJ (2020) Biological control and integrated pest management in organic and conventional systems. Biol Control 140(1):104095. https://doi.org/10.1016/j.biocontrol.2019.104095
Barcellos PS, Araújo TM, Gomes G, Bila DM, Canela MC (2022) The fate of atrazine in tropical environments: photolysis, acute toxicity and endocrine disruptor potential. J Braz Chem Soc 33(8):927–937. https://doi.org/10.21577/0103-5053.20220030
Bastos CS, Almeida RP, Suinaga FA (2006) Selectivity of pesticides used on cotton (Gossypium hirsutum) to Trichogramma pretiosum reared on two laboratory-reared hosts. Pest Manag Sci 62(1):91–98. https://doi.org/10.1002/ps.1140
Behrend JE, Rypstra AL (2018) Contact with a glyphosate-based herbicide has long-term effects on the activity and foraging of an agrobiont wolf spider. Chemosphere 194(1):714–721. https://doi.org/10.1016/j.chemosphere.2017.12.038
Benamú MA, Schneider MI, Sanchez NE (2010) Effects of the herbicide glyphosate on biological attributes of Alpaida veniliae (Araneae, Araneidae), in laboratory. Chemosphere 78(7):871–876. https://doi.org/10.1016/j.chemosphere.2009.11.027
Benbrook CM (2016) Trends in glyphosate herbicide use in the United States and globally. Environ Sci Eur 28(1):1–15. https://doi.org/10.1186/s12302-016-0070-0
Biondi A, Mommaerts V, Smagghe G, Viñuela E, Zappalà L, Desneux N (2012) The non-target impact of spinosyns on beneficial arthropods. Pest Manag Sci 68(12):1523–1536. https://doi.org/10.1002/ps.3396
Boutin C, Strandberg B, Carpenter D, Mathiassen SK, Thomas PJ (2014) Herbicide impact on non-target plant reproduction: what are the toxicological and ecological implications? Environ Pollut 185(1):295–306. https://doi.org/10.1016/j.envpol.2013.10.009
Brookes G, Taheripour F, Tyner WE (2017) The contribution of glyphosate to agriculture and potential impact of restrictions on use at the global level. GM Crops Food 8(4):216–228. https://doi.org/10.1080/21645698.2017.1390637
Bull DL, Coleman RJ (1985) Effects of pesticides on Trichogramma spp. Southwest Entomol 1(8):156–168
Camilo S, Soares MA, Santos JB, De Assis Júnior SL, Ferreira EA, De Menezes CWG (2012) Impactos toxicológicos de herbicidas recomendados para a cultura do milho em ninfas do predador Podisus nigrispinus (Hemiptera: Pentatomidae). Revista Brasileira de Herbicidas 11(3):339–346. https://doi.org/10.7824/rbh.v11i3.189
Camilo S, Soares MA, Leite GLD, Santos JB, Assis Junior SL, Zanuncio JC (2016) Do floral resources in Eucalyptus plantations affect fitness parameters of the parasitoid Palmistichus elaeisis (Hymenoptera: Eulophidae)? Phytoparasitica 44(5):651–659. https://doi.org/10.1007/s12600-016-0549-7
Castilhos RV, Grützmacher AD, Siqueira PRB, Moraes ÍLD, Gauer CJ (2014) Seletividade de agrotóxicos utilizados em pessegueiro sobre ovos e pupas do predador Chrysoperla externa. Ciência Rural 44:1921–1928. https://doi.org/10.1590/0103-8478cr20140248
Cavaliere F, Brandmayr P, Giglio A (2019) DNA damage in haemocytes of Harpalus (Pseudophonus) rufipes (De Geer, 1774) (Coleoptera, Carabidae) as an indicator of sublethal effects of exposure to herbicides. Ecol Ind 98:88–91. https://doi.org/10.1016/j.ecolind.2018.10.055
Cheng S, Lin R, Wang L, Qiu Q, Qu M, Ren X, Zong F, Jiang H, Yu C (2018) Comparative susceptibility of thirteen selected pesticides to three different insect egg parasitoid Trichogramma species. Ecotoxicol Environ Saf 166(1):86–91. https://doi.org/10.1016/j.ecoenv.2018.09.050
Cherif A, Mansour R, Grissa-Lebdi K (2021) The egg parasitoids Trichogramma: from laboratory mass rearing to biological control of lepidopteran pests. Biocontrol Sci Tech 31(7):661–693. https://doi.org/10.1080/09583157.2020.1871469
Chiverton PA, Sotherton NW (1991) The effects of beneficial arthropods of the exclusion of herbicides from cereal crop edges. J Appl Ecol 28(1):1027–1039. https://doi.org/10.2307/2404223
Cloyd RA, Bethke JA (2011) Impact of neonicotinoid insecticides on natural enemies in greenhouse and interior scape environments. Pest Manag Sci 67(1):3–9. https://doi.org/10.1002/ps.2015
Cousin M, Silva-Zacarin E, Kretzschmar A, E Maataoui M, Brunet JL, Belzunces LP (2013) Size changes in honeybee larvae oenocytes induced by exposure to paraquat at very low concentrations. PLoS One 8(5):65–693. https://doi.org/10.1371/journal.pone.0065693
Croft BA (1990) Arthropod biological control agents and pesticides. John Wiley and Sons Inc, USA, p 723
Cruz RADL, Zanuncio JC, Lacerda MC, Wilcken CF, Fernandes FL, Tavares WDS, Sediyama CS (2017) Side-effects of pesticides on the generalist endoparasitoid Palmistichus elaeisis (Hymenoptera: Eulophidae). Sci Rep 7(1):10064. https://doi.org/10.1590/1519-6984.176665
Dan HA, Barroso ALL, Dan LGM, Finotti TR, Feldkircher C, Santos VS (2010) Controle de plantas daninhas na cultura do milho por meio de herbicidas aplicados em pré-emergência. Pesquisa Agropecuária Tropical 40(4):388–393. https://doi.org/10.1590/S1983-40632010000400017
Dash PK, Rai R (2022) Green revolution to grain revolution: Florigen in the frontiers. J Biotechnol 343(1):38–46. https://doi.org/10.1016/j.jbiotec.2021.10.002
De Castro AA, Corrêa 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(6):1043–1050. https://doi.org/10.1016/j.chemosphere.2013.05.075
De Rezende Antigo M, Shimbori EM, Glaeser DF, de Oliveira HN, Carvalho GA (2016) Herbicidas e reguladores de crescimento de plantas utilizados na cana-de-açúcar e sua ação sobre adultos de Trichogramma galloi Zucchi (Hymenoptera: Trichogrammatidae). EntomoBrasilis 9(1):36–40. https://doi.org/10.12741/ebrasilis.v9i1.556
De Souza CP, De Andrade Guedes T, Fontanetti CS (2016) Evaluation of herbicides action on plant bioindicators by genetic biomarkers: a review. Environ Monit Assess 188(12):694. https://doi.org/10.1007/s10661-016-5702-8
Desneux N, Decourtye A, Delpuech JM (2007) The sublethal effects of pesticides on beneficial arthropods. Annu Rev Entomol 52(1):81–106. https://doi.org/10.1146/annurev.ento.52.110405.091440
Ditillo JL, Kennedy GG, Walgenbach JF (2016) Effects of insecticides and fungicides commonly used in tomato production on Phytoseiulus persimilis (Acari: Phtyoseiidae). J Econ Entomol 109(6):2298–2308. https://doi.org/10.1093/jee/tow234
FAO (2022) Disponível em: <https://www.fao.org/faostat/en/#data/RP/visualize>. Último acesso: Maio de 2022
Fleeger JW, Carman KR, Nisbet RM (2003) Indirect effects of contaminants in aquatic ecosystems. Sci Total Environ 317(1–3):207–233. https://doi.org/10.1016/S0048-9697(03)00141-4
Freemark K, Boutin C (1995) Impacts of agricultural herbicide use on terrestrial wildlife in temperate landscapes: A review with special reference to North America. Agr Ecosyst Environ 52(2–3):67–91. https://doi.org/10.1016/0167-8809(94)00534-L
Gao X, Hu F, Zhang S, Luo J, Zhu X, Wang L, Zhang K, Li D, Ji J, Niu L, Wu C, Cui J (2021) Glyphosate exposure disturbs the bacterial endosymbiont community and reduces body weight of the predatory ladybird beetle Harmonia axyridis (Coleoptera: Coccinellidae). Sci Total Environ 790(1):147847. https://doi.org/10.1016/j.scitotenv.2021.147847
Gianessi LP (2013) The increasing importance of herbicides in worldwide crop production. Pest Manag Sci 69(10):1099–1105
Giglio A, Cavaliere F, Giulianini PG, Kurtz J, Vommaro ML, Brandmayr P (2019) Continuous agrochemical treatments in agroecosystems can modify the effects of pendimethalin-based herbicide exposure on immunocompetence of a beneficial ground beetle. Diversity 11(12):241. https://doi.org/10.3390/d11120241
Giolo FP, Grützmacher AD, Procópio SO, Manzoni CG, Lima CAB, Nörnberg SD (2005) Seletividade de formulações de glyphosate a Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). Planta Daninha 23(3):457–462. https://doi.org/10.1590/S0100-83582005000300009
Gonçalves TS, Soares MA, Santos CA, Santos DA, Santos JB, Barroso GA (2016) Does the ingestion of isoxaflutole herbicide affect the midgut and salivary glands of pentatomidae predators? Planta Daninha 34(1):125–132. https://doi.org/10.1590/S0100-83582016340100013
Guerra N, Haramoto R, Schmitt J, Costa GD, Schiessel JJ, Oliveira Neto AM (2020) Weed control and selectivity herbicides pre emerging in garlic cultivars. Planta Daninha 38(1):e020228966. https://doi.org/10.1590/S0100-83582020380100074
Habel JC, Samways MJ, Schmitt T (2019) Mitigating the precipitous decline of terrestrial European insects: Requirements for a new strategy. Biodivers Conserv 28(6):1343–1360. https://doi.org/10.1007/s10531-019-01741-8
Hosamani R, Muralidhara (2013) Acute exposure of Drosophila melanogaster to paraquat causes oxidative stress and mitochondrial dysfunction. Arch Insect Biochem Physiol 83(1):25–40. https://doi.org/10.1002/arch.21094
HRAC (2022) Comitê de Ação à Resistencia ao Herbicidas. Disponível em: <https://www.hrac-br.org/registros>. Último acesso: Junho de 2022
Jervis MA (2005) Insects as natural enemies: a practical perspective. Springer, New York
Kanissery R, Liu W, Tiwari R, Sims G (2021) Impact of soil aeration on the environmental fate of pre-emergent herbicide metolachlor. Appl Sci 11(18):8567. https://doi.org/10.3390/app11188567
Khan MA (2020) Lethal and parasitism effects of selected novel pesticides on adult Trichogramma chilonis (Hymenoptera: Trichogrammatidae). J Plant Dis Prot 127(1):81–90. https://doi.org/10.1007/s41348-019-00280-2
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. https://doi.org/10.1002/ps.4639
Kniss AR (2017) Long-term trends in the intensity and relative toxicity of herbicide use. Nat Commun 8(1):14865. https://doi.org/10.1038/ncomms14865
Korenko S, Niedobová J, Kolárˇová M, Hamouzová K, Kysilková K, Michalko R (2016) The effect of eight common herbicides on the predatory activity of the agrobiont spider Pardosa agrestis. Biocontrol 61(5):507–517. https://doi.org/10.1007/s10526-016-9729-0
Lacava M, García LF, Vieira C, Michalko R (2021) The pest-specific effects of glyphosate on functional response of a wolf spider. Chemosphere 262(1):127785. https://doi.org/10.1016/j.chemosphere.2020.127785
Leite GLD, De Paulo PD, Zanuncio JC, Alvarenga AC, Soares MA, Souza Tavares W, Tuffi-Santos LD, De Carvalho Spínola-Filho PR (2015) Effects of atrazine-based herbicide on emergence and sex ratio of Trichogrammatidae (Hymenoptera). Flo Entomol 98(3):899–902. https://doi.org/10.1653/024.098.0313
Leite GL, De Paulo PD, Zanuncio JC, Tavares WDS, Alvarenga AC, Dourado LR, Bispo EPR, Soares MA (2017a) Herbicide toxicity, selectivity and hormesis of nicosulfuron on 10 Trichogrammatidae (Hymenoptera) species parasitizing Anagasta (= Ephestia) kuehniella (Lepidoptera: Pyralidae) eggs. J Environ Sci Health B 52(1):70–76. https://doi.org/10.1080/03601234.2016.1229476
Leite GL, De Paulo PD, Zanuncio JC, Tavares WDS, Alvarenga AC, Dourado LR, Bispo EPR, Soares MA (2017b) Nicosulfuron plus atrazine herbicides and Trichogrammatidae (Hymenoptera) in no-choice test: selectivity and hormesis. Bull Environ Contam Toxicol 99(5):589–594. https://doi.org/10.1007/s00128-017-2174-7
Leite GLD, Paulo PD, Tuffi-Santos LD, Alvarenga AC (2019) Eficácia de espécies de Trichogrammatidae (Hymenoptera) submetidas ao herbicida glyphosate. Planta Daninha 37(1):e019216439. https://doi.org/10.1590/S0100-83582019370100147
Lundgren JG, Gassmann AJ, Bernal J, Duan JJ, Ruberson J (2009) Ecological compatibility of GM crops and biological control. Crop Prot 28(12):1017–1030. https://doi.org/10.1016/j.cropro.2009.06.001
Magano DA, Krolow IR, Grützmacher AD, Panozzo LE, Armas FS, Zimmer M (2013) Efeitos secundários de herbicidas aplicados em soja sobre Trichogramma pretiosum. Pesq Agrop Gaúcha 19(1–2):49–57
Magano DA, Grutzmacher AD, De Armas FS, 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(40):3825–3831. https://doi.org/10.5897/AJAR2014.9083
Mahdian K, Van Leeuwen T, Tirry L, De Clercq P (2007) Susceptibility of the predatory stinkbug Picromerus bidens to selected insecticides. Biocontrol 52(6):765–774. https://doi.org/10.1007/s10526-007-9075-3
Mangena P (2022) Pleiotropic effects of recombinant protease inhibitors in plants. Front Plant Sci 13:994710. https://doi.org/10.3389/fpls.2022.994710
Mantzos N, Karakitsou A, Hela D, Patakioutas G, Leneti E, Konstantinou I (2014) Persistence of oxyfluorfen in soil, runoff water, sediment and plants of a sunflower cultivation. Sci Total Environ 472(1):767–777. https://doi.org/10.1016/j.scitotenv.2013.11.016
Manzoni C, Grützmacher A, Giolo F, Härter W, Castilhos R, Paschoal M (2007) Seletividade de agroquímicos utilizados na produção integrada de maçã aos parasitoides Trichogramma pretiosum Riley e Trichogramma atopovirilia Oatman & Platner (Hymenoptera: Trichogrammatidae). BioAssay 2(1):1–11. https://doi.org/10.14295/BA.v2.0.50
McMurtry JA, Croft BA (1997) Life-styles of phytoseiid mites and their roles in biological control. Annu Rev Entomol 42(1):291–321. https://doi.org/10.1146/annurev.ento.42.1.291
Menezes CWG, Soares MA (2016) Impacts of the control of weeds and herbicides applied to natural enemies. Revista Brasileira De Herbicidas 15(1):2–13. https://doi.org/10.7824/rbh.v1i1.407
Menezes CWG, Santos JB, Assis SL, Fonseca AJ, Franca AC, Soares MA, Fernandes AF (2012a) Selectivity of atrazin and nicosulfurom to Podisus nigrispinus (Heteroptera: Pentatomidae). Planta Daninha 30(2):327–334. https://doi.org/10.1590/S0100-83582012000200011
Menezes CD, Soares MA, Santos JB, Assis Júnior SL, Fonseca AJ, Zanuncio JC (2012b) Reproductive and toxicological impacts of herbicides used in Eucalyptus culture in Brazil on the parasitoid Palmistichus elaeisis (Hymenoptera: Eulophidae). Weed Res 52(6):520–525. https://doi.org/10.1111/j.1365-3180.2012.00938.x
Menezes CW, Soares MA, Fonseca AJ, dos Santos JB, Camilo SDS, Zanuncio JC (2014) Palmistichus elaeisis (Hymenoptera: Eulophidae) as an indicator of toxicity of herbicides registered for corn in Brazil. Chilean J Agric Res 74(3):361–365. https://doi.org/10.4067/S0718-58392014000300016
Michalkova V, Pekar S (2009) How glyphosate altered the behaviour of agrobiont spiders (Araneae: Lycosidae) and beetles (Coleoptera: carabidae). Biol Control 51(3):444–449. https://doi.org/10.1016/j.biocontrol.2009.08.003
Michaud JP, Vargas G (2010) Relative toxicity of three wheat herbicides to two species of Coccinellidae. Insect Sci 17(5):434–438. https://doi.org/10.1111/j.1744-7917.2009.01308.x
Milesi MM, Lorenz V, Durando M, Rossetti MF, Varayoud J (2021) Glyphosate herbicide: reproductive outcomes and multigenerational effects. Front Endocrinol 12(1):672532. https://doi.org/10.3389/2Ffendo.2021.672532
Miñarro M, Dapena E (2003) Effects of groundcover management on ground beetles (Coleoptera: Carabidae) in an apple orchard. Appl Soil Ecol 23(2):111–117. https://doi.org/10.1016/S0929-1393(03)00025-8
Msebah AH, El-Husseini MM (2009) Effect of weed borders on insect pests and their associated predators on sugar beet and cotton plant fields. Egypt Acad J Biol Sci A, Entomol 2(1):73–80. https://doi.org/10.21608/eajbsa.2009.15455
Norris RF, Kogan M (2000) Interactions between weeds, arthropod pests, and their natural enemies in managed ecosystems. Weed Sci 48(1):94–158. https://doi.org/10.1614/0043-1745(2000)048[0094:IBWAPA]2.0.CO;2
Norris RF, Kogan M (2005) Ecology of interactions between weeds and arthropods. Annu Rev Entomol 50(1):479–503. https://doi.org/10.1146/annurev.ento.49.061802.123218
Parra JRP (2014) Biological control in Brazil: an overview. Scientia Agricola 71(5):420–429. https://doi.org/10.1590/0103-9016-2014-0167
Pasini RA, Grützmacher AD, Spagnol D, Zantedeschi R, Friedrich FF (2017) Persistência de herbicidas dessecantes aplicados em milho transgênico sobre Trichogramma pretiosum Riley, 1879 (Hymenoptera: Trichogrammatidae). Revista Ciência Agronômica 48(1):175–181. https://doi.org/10.5935/1806-6690.20170020
Pasini RA, Pazini JB, Grützmacher A, Rakes M, Armas FS (2018) comparative selectivity of herbicides used in wheat crop on the predators Chrysoperla externa and Eriopis connexa. Planta Daninha 36(1):e018179968. https://doi.org/10.1590/S0100-83582018360100135
Pontes JP, Leite GLD, Bispo EPR, Souza Tavares W, de Menezes CWG, Wilcken CF, Zanuncio JC (2020) A glyphosate-based herbicide in a free-choice test on parasitism, emergence, and female-biased sex ratio of 10 Trichogrammatidae. J Plant Dis Prot 127(1):73–79. https://doi.org/10.1007/s41348-019-00277-x
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(3):209–215. https://doi.org/10.1007/s12600-009-0031-x
Prosser RS, Anderson JC, Hanson ML, Solomon KR, Sibley PK (2016) Indirect effects of herbicides on biota in terrestrial edge-of-field habitats: a critical review of the literature. Agric Ecosyst Environ 232(1):59–72. https://doi.org/10.1016/j.agee.2016.07.009
Rakes M, Pasini RA, Morais MC, Araujo MB, de Bastos Pazini J, Seidel EJ, Bernardi D, Grützmacher AD (2021) Pesticide selectivity to the parasitoid Trichogramma pretiosum: A pattern 10-year database and its implications for Integrated Pest Management. Ecotoxicol Environ Saf 208(1):111504. https://doi.org/10.1016/j.ecoenv.2020.111504
Reddy PP (2016) Sustainable crop protection under protected cultivation (No. BOOK). Springer, Singapore
Reis TC, Soares MA, Santos JB, Santos CA, Serrão JE, Zanuncio JC, Ferreira EA (2018) Atrazine and nicosulfuron affect the reproductive fitness of the predator Podisus nigrispinus (Hemiptera: Pentatomidae). An Acad Bras Ciênc 90(4):3625–3633. https://doi.org/10.1590/0001-3765201820170748
Relyea R, Hoverman J (2006) Assessing the ecology in ecotoxicology: a review and synthesis in freshwater systems. Ecol Lett 9(10):1157–1171. https://doi.org/10.1111/j.1461-0248.2006.00966.x
Ribeiro VH, Oliveira MC, Smith DH, Santos JB, Werle R (2021) Evaluating efficacy of preemergence soybean herbicides using field treated soil in greenhouse bioassays. Weed Technol 35(5):830–837. https://doi.org/10.1017/wet.2021.22
Rodrigues MJ, Turozi TA, Netto APC, Timossi PC (2012) Épocas da adubação nitrogenada relacionada à aplicação de nicosulfuron na cultura do milho. Glob Sci Technol 5(1):70–77
Rose MT, Cavagnaro TR, Scanlan CA, Rose TJ, Vancov T, Kimber S, Kennedy IR, Kookana RS, Van Zwieten L (2016) Impact of herbicides on soil biology and function. Adv Agron 136:133–220. https://doi.org/10.1016/bs.agron.2015.11.005
Sánchez Bayo F (2021) Indirect effect of pesticides on insects and other arthropods. Toxics 9(8):177. https://doi.org/10.3390/toxics9080177
Santos JB, Santos EA, Santos EA (2023) Only -Glyphosate- Can Stop Glyphosate. Braz J Biol 83:1. https://doi.org/10.1590/1519-6984.246450
Saska P, Skuhrovec J, Lukáš J, Vlach M, Chi H, Tuan SJ, Honěk A (2017) Treating prey with glyphosate does not alter the demographic parameters and predation of the Harmonia axyridis (Coleoptera: Coccinellidae). J Econ Entomol 110(2):392–399. https://doi.org/10.1093/jee/tow325
Schmidt-Jeffris RA, Cutulle MA (2019) Non-target effects of herbicides on Tetranychus urticae and its predator, Phytoseiulus persimilis: implications for biological control. Pest Manag Sci 75(12):3226–3234. https://doi.org/10.1002/ps.5443
Schmidt-Jeffris RA, Moretti EA, Bergeron PE, Zilnik G (2022) Non-target impacts of herbicides on spiders in orchards. J Econ Entomol 115(1):65–73. https://doi.org/10.1093/jee/toab228
Serra LS, Mendes MRF, Soares MDA, Monteiro IP (2016) Revolução Verde: reflexões acerca da questão dos agrotóxicos. Revista Científica Do Centro De Estudos Em Desenvolvimento Sustentável Da UNDB 1(4):2–25
Sharifzadeh MS, Abdollahzadeh G, Damalas CA, Rezaei R (2018) Farmers’ criteria for pesticide selection and use in the pest control process. Agriculture 8(2):24. https://doi.org/10.3390/agriculture8020024
Silva DM, Bueno AF (2015) Organic products selectivity for Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). Arq Inst Biol 82(1):01–08. https://doi.org/10.1590/1808-1657000422013
Silva WM, Martínez LC, Plata-Rueda A, Serrão JE, Zanuncio JC (2021) Exposure to insecticides causes effects on survival, prey consumption, and histological changes in the midgut of the predatory bug, Podisus nigrispinus (Hemiptera: Pentatomidae). Environ Sci Pollut Res 28(41):57449–57458. https://doi.org/10.1007/s11356021-14589-9
Singh S, Kumar V, Chauhan A, Datta S, Wani AB, Singh N, Singh J (2018) Toxicity, degradation and analysis of the herbicide atrazine. Environ Chem Lett 16(1):211–237. https://doi.org/10.1007/s10311-017-0665-8
Soares MA, Leite GLD, Zanuncio JC, Rocha SL, De Sá VGM, Serrão JE (2007) Note: Flight capacity, parasitism and emergence of fiveTrichogramma (Hymenoptera: Trichogrammatidae) species from forest areas in Brazil. Phytoparasitica 35(3):314–318. https://doi.org/10.1007/BF02981165
Sondhia S (2009) Persistence of oxyfluorfen in soil and detection of its residues in rice crop. Toxicol Environ Chem 91(3):425–433. https://doi.org/10.1080/02772240802269096
Souza GK, Pikart TG, Zanuncio TV, Wilcken CF, Serrão JE, Zanuncio JC (2014) Reproductive tract histology of Thaumastocoris peregrinus (Hemiptera: Thaumastocoridae). Ann Entomol Soc Am 107(4):853–857. https://doi.org/10.1603/AN13061
Souza AM, Maciel JC, Barroso GM, Silva RS, Garraffoni ARS, Neves CA, Santos JB (2024) Ecotoxicological effects of commercial herbicides on the reproductive system of aquatic arthropod Limnocoris submontandoni (Hemiptera: Naucoridae). Braz J Biol 84(1):e247487. https://doi.org/10.1590/1519-6984.247487
Staudacher K, Rennstam Rubbmark O, Birkhofer K, Malsher G, Sint D, Jonsson M, Traugott M (2018) Habitat heterogeneity induces rapid changes in the feeding behaviour of generalist arthropod predators. Funct Ecol 32(3):809–819. https://doi.org/10.1111/1365-2435.13028
Stecca CS, Bueno AF, Pasini A, Silva DM, Andrade K (2016) Side-effects of glyphosate to the parasitoid Telenomus remus Nixon (Hymenoptera: Platygastridae). Neotrop Entomol 45(2):192–200. https://doi.org/10.1007/s13744-016-0363-4
Stefanello Júnior GJ, Grützmacher AD, Grützmacher DD, Lima CAB, Dalmozo DO, Paschoal MDF (2008) Seletividade de herbicidas registrados para a cultura do milho a adultos de Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). Planta Daninha 26(2):343–351. https://doi.org/10.1590/S0100-83582008000200010
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, Van de Veire M, 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(1):99–117. https://doi.org/10.1023/A:1009959009802
Strandberg M, Scott-Fordsmand JJ (2004) Effects of pendimethalin at lower trophic levels: a review. Ecotoxicol Environ Saf 57(2):190–201. https://doi.org/10.1016/j.ecoenv.2003.07.010
Suh CPC, Orr DB, Van Duyn JW (2000) Effect of insecticides on Trichogramma exiguum (Trichogrammatidae: Hymenoptera) preimaginal development and adult survival. J Econ Entomol 93(3):577–583. https://doi.org/10.1603/0022-049393.3.577
Svobodová Z, Habuštová OS, Holec J, Holec M, Boháč J, Jursík M, Soukup J, Sehnal F (2018) Split application of glyphosate in herbicide-tolerant maize provides efficient weed control and favors beneficial epigeic arthropods. Agr Ecosyst Environ 251:171–179. https://doi.org/10.1016/j.agee.2017.09.018
Tahir HM, Basheer T, Ali S, Yaqoob R, Naseem S, Khan SY (2019) Effect of pesticides on biological control potential of Neoscona theisi (Araneae: Araneidae). J Insect Sci 19(2):17. https://doi.org/10.1093/jisesa/iez024
Tiftikçi P, Kök Ş, Kasap İ (2022) The effect of host plant on the biological control efficacy of the predatory mite, Phytoseiulus persimilis Athias-Henriot against two-spotted spidermites, Tetranychus urticae Koch on field-grown vegetables. Crop Prot 158:106012. https://doi.org/10.1016/j.cropro.2022.106012
Togni PHB, Venzon M, Lagôa ACG, Sujii ER (2019) Brazilian legislation leaning towards fast registration of biological control agents to benefit organic agriculture. Neotrop Entomol 48(2):175–185. https://doi.org/10.1007/s13744-019-00675-8
Trager MD, Ristau TE, Stoleson SH, Davidson RL, Acciavatti RE (2013) Carabid beetle responses to herbicide application, shelterwood seed cut and insect defoliator outbreaks. For Ecol Manag 289(1):269–277. https://doi.org/10.1016/j.foreco.2012.10.025
Traoré H, Crouzet O, Mamy L, Sireyjol C, Rossard V, Servien R, Latrille E, Martin-Laurent F, Patureau D, Benoit P (2018) Clustering pesticides according to their molecular properties, fate, and effects by considering additional ecotoxicological parameters in the TyPol method. Environ Sci Pollut Res 25(5):4728–4738. https://doi.org/10.1007/s11356-017-0758-8
Turan NB, Sari Erkan H, Çaglak A, Bakırdere S, Engin GO (2020) Optimization of atrazine removal from synthetic groundwater by electrooxidation process using titanium dioxide and graphite electrodes. Sep Sci Technol 55(16):3036–3045. https://doi.org/10.1080/01496395.2019.1669659
Valadares NR, Soares MA, Ferreira EA, Sá VGM, Azevedo AM, Leite GLD, Zanuncio JC (2023) Physiological responses in genetically modified cotton and its isohybrid attacked by Aphis gossypii Glover (Hemiptera: Aphididae). Arthropod-Plant Interactions 11829:9943. https://doi.org/10.1007/s11829-022-09943-8
Van Lenteren JC (2012) The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. Biocontrol 57(1):3–38. https://doi.org/10.1007/s10526-011-9395-1
Van Lenteren JC, Bolckmans K, Köhl J, Ravensberg WJ, Urbaneja A (2018) Biological control using invertebrates and microorganisms: plenty of new opportunities. Biocontrol 63(1):39–59. https://doi.org/10.1007/s10526-017-9801-4
Villa M, Santos SA, Mexia A, Bento A, Pereira JA (2016) Ground cover management affects parasitism of Prays oleae (Bernard). Biol Control 96(1):72–77. https://doi.org/10.1016/j.biocontrol.2016.01.012
Vommaro ML, Giulianini PG, Giglio A (2021) Pendimethalin-based herbicide impairs cellular immune response and haemocyte morphology in a beneficial ground beetle. J Insect Physiol 131(1):104236. https://doi.org/10.1016/j.jinsphys.2021.104236
Wen L, Zhong J, Cui Y, Duan Z, Zhou F, Li C, Lin Y (2021) Coexpression of I. variabilis-EPSPS* and WBceGO-B3S1 genes contributes to high glyphosate tolerance and low glyphosate residues in transgenic rice. J Agric Food Chem 69(26):7388–7398. https://doi.org/10.1021/acs.jafc.1c00880
Yu X, Huang Y, Chen X, Zhou Z, Shen Z, Wang P (2022) Compositional and animal feeding assessments of a novel herbicide-tolerant maize variety. Agriculture 12(6):808. https://doi.org/10.3390/agriculture12060808
Zang LS, Wang S, Zhang F, Desneux N (2021) Biological control with Trichogramma in China: History, present status and perspectives. Annu Rev Entomol 66(1):463–484. https://doi.org/10.1146/annurev-ento-060120-091620
Zantedeschi R, Grützmacher AD, Pazini JDB, Bueno FA, Machado LL (2018) Selectivity of pesticides registered for soybean crop on Telenomus podisi and Trissolcus basalis. Pesquisa Agropecuária Tropical 48(1):52–58. https://doi.org/10.1590/1983-40632018v4850348
Zanuncio JC, Lacerda MC, Alcántara-de la Cruz R, Brügger BP, Pereira AI, Wilcken CF, Sediyama CS (2018) Glyphosate-based herbicides toxicity on life history parameters of zoophytophagous Podisus nigrispinus (Heteroptera: Pentatomidae). Ecotoxicol Environ Saf 147(1):245–250. https://doi.org/10.1016/j.ecoenv.2017.08.055
Zhang JX, Drummond FA, Leibman M (1998) Effect of crop habitat and potato management practices on the population abundance of adult Harpalus rufipes (Coleoptera: Carabidae) in Maine. J Agric Entomol 15(1):63–74
Zhu W, Schmehl DR, Mullin CA, Frazier JL (2014) Four common pesticides, their mixtures and a formulation solvent in the hive environment have high oral toxicity to honey bee larvae. PLoS One 9(1):e77547. https://doi.org/10.1371/journal.pone.0077547
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“To Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)”, “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES—Financial Code 001), Fundação de Amparo à Pesquisa do Estado de Minas Gerais (FAPEMIG)” and “Programa Cooperativo sobre Proteção Florestal (PROTEF) do Instituto de Pesquisas e Estudos Florestais (IPEF)”.
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Dos Santos, J.B; Soares, M.A: Conceptualization; Pinheiro, R.A; Duque, T.S: Data curation; Cabral, C.M: Formal analysis; Dos Santos J.B: Funding acquisition; Pinheiro, R.A; Duque, T.S; Barroso, G.M: Investigation; Pinheiro, R.A; Duque, T.S; Barroso, G.M: Methodology; Dos Santos J.B; Soares, M.A: Project administration; Dos Santos J.B: Resources; Duque, T.S: Software; Dos Santos J.B; Soares, M.A; Cabral, C.M: Supervision; Pinheiro, R.A; Duque, T.S; Barroso, G.M: Validation; Zanuncio, J.C: Visualization; Pinheiro, R.A; Duque, T.S; Barroso, G.M: Roles/Writing—original draft; Pinheiro, R.A; Duque, T.S; Barroso, G.M; Soares, M.A; Zanuncio, J.C; Dos Santos, J.B: Writing—review & editing.
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Highlights
• Chemical weed control is a threat to the success of biological pest control.
• The herbicide glyphosate is the least selective for parasitoids.
• Trichogramma sp used for biological control is the most affected by herbicides.
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Pinheiro, R.A., Duque, T.S., Barroso, G.M. et al. Herbicides may threaten advances in biological control of diseases and pests. Environ Sci Pollut Res 30, 111850–111870 (2023). https://doi.org/10.1007/s11356-023-30198-0
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DOI: https://doi.org/10.1007/s11356-023-30198-0