Skip to main content
Log in

Side-Effects of Glyphosate to the Parasitoid Telenomus remus Nixon (Hymenoptera: Platygastridae)

  • Biological Control
  • Published:
Neotropical Entomology Aims and scope Submit manuscript

Abstract

The aim of this study was to compare the side-effects of glyphosate to the parasitoid Telenomus remus Nixon (Hymenoptera: Platygastridae) when parasitoids were exposed to this chemical at the pupal (inside host eggs) and adult stages. Bioassays were conducted under laboratory conditions according to the International Organization for Biological Control (IOBC) standard methods for testing side-effects of pesticides to egg parasitoids. Different glyphosate-based pesticides (Roundup Original®, Roundup Ready®, Roundup Transorb®, Roundup WG®, and Zapp Qi®) were tested at the same acid equivalent concentration. Treatments were classified following the IOBC toxicity categories as (1) harmless, (2) slightly harmful, (3) moderately harmful, and (4) harmful. When tested against T. remus adults, Roundup Original®, Roundup Ready®, Roundup Transorb®, and Roundup WG® reduced parasitism 2 days after parasitoid emergence, being classified as slightly harmful. Differently, when tested against T. remus pupae, all tested glyphosate-based products did not differ in their lethal effect and therefore did not reduce T. remus adult emergence or parasitism capacity, being classified as harmless. However, differences on sublethal toxicity were found. Parasitism of individuals emerging from parasitized eggs sprayed at the pupal stage of T. remus with Zapp Qi® was lower compared to control, but parasitism was still higher than 66%, and therefore, Zapp Qi® was still classified as harmless. In conclusion, all tested glyphosate-based products can be used in agriculture without negative impact to T. remus as none was classified as harmful or moderately harmful to this parasitoid when exposure occurred at the pupal or adult stages.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

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

    Article  Google Scholar 

  • Amarante Júnior OP, Santos TCR, Brito NM, Ribeiro ML (2002) Glifosato: propriedades, toxicidade, uso e legislação. Quim Nova 25:589–593

    Article  Google Scholar 

  • Bacci L, Picanço MC, Gusmão MR, Crespo ALB, Pereira EJG (2001) Seletividade de inseticidas a Brevicoryne brassicae (L.) (Hemiptera: Aphididae) e ao predador Doru luteipes (Scudder) (Dermaptera: Forficulidae). Neotrop Entomol 30:707–713

    Article  Google Scholar 

  • Barbier R, Chauvin G (1974) Ultrastructure et role des aeropyles et des envelopes de l’oeufs de Galleria mellonella. J Insect Physiol 20:809–820

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Biondi A, Zappala 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(9):e76548. doi:10.1371/journal.pone.0076548

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bueno AF, Bueno RCOF, Parra JRP, Vieira SS (2008) Effects of pesticides used in soybean crops to the egg parasitoid Trichogramma pretiosum. Cienc Rural 38:1495–1503

    Article  CAS  Google Scholar 

  • Burr IW, Foster LA (1972) A test for equality of variances. Mimeo series no 282. University of Purdue, West Lafayette, 26 p

    Google Scholar 

  • Carmo EL, Bueno AF, Bueno RCOF, 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

    Article  Google Scholar 

  • Carmo EL, Bueno AF, Bueno RCOF (2010a) Pesticide selectivity for the insect egg parasitoid Telenomus remus. BioControl 55:455–464

    Article  CAS  Google Scholar 

  • Carmo EL, Bueno AF, Bueno RCOF, Vieira SS, Goulart MMP, Carneiro TR (2010b) Seletividade de produtos fitossanitários utilizados na cultura da soja para pupas de Trichogramma pretiosum Riley 1879 (Hymenoptera: Trichogrammatidae). Arq Inst Biol 77:283–290

    Google Scholar 

  • Cave RD (2000) Biology, ecology and use in pest management of Telenomus remus. BioControl 21:21–26

    Google Scholar 

  • Chauvin JT, Chauvin G (1980) Formation des reliefs externs de l’oeuf de Micropteryx caltella L. (Lepidoptera: Micropterigidae). Can J Zool 58:761–766

    Article  Google Scholar 

  • Chen CY, Hathaway KM, Folt CL (2004) Multiple stress effects of vision 1 herbicide, pH, and food on zooplankton and larval amphibian species from forest wetlands. Environ Toxicol Chem 23:823–831

    Article  CAS  PubMed  Google Scholar 

  • Cônsoli FL, Parra J, Hassan S (1998) Side-effects of insecticides used in tomato fields on the egg parasitoid Trichogramma pretiosum Riley (Hym., Trichogrammatidae), a natural enemy of Tuta absoluta (Meyrick) (Lep., Gelechiidae). J Appl Entomol 122:43–47

    Article  Google Scholar 

  • Cônsoli FL, Kitajima EW, Parra JRP (1999) Ultrastructure of the natural and factitious host eggs of Trichogramma galloi Zucchi and Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). Int J Insect Morphol Embryol 28:211–231

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Coutinho CFB, Mazo LH (2005) Complexos metálicos com o herbicida glifosato: revisão. Quim Nova 28:1038–1045

    Article  CAS  Google Scholar 

  • Croft BA (1990) Arthropod biological control agents and pesticides. Wiley, New York, 723 p

    Google Scholar 

  • Cruz I, Figueiredo MLC, Oliveira CE, Vasconcelos CA (1999) Damage of Spodoptera frugiperda (Smith) in different maize genotypes cultivated in soil under three levels of aluminium saturation. Int J Pest Manag 45:293–296

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ferrer F (2001) Biological control of agricultural insects in Venezuela: advances, achievements, and future perspectives. Biocontrol News Inf 22:67–74

    Google Scholar 

  • Folmar LC, Sanders HO, Julin AM (1979) Toxicity of the herbicide glyphosate and several of its formulations to fish and aquatic invertebrates. Arch Environ Contam Toxicol 8:269–278

    Article  CAS  PubMed  Google Scholar 

  • Giesy JP, Dobson S, Solomon KR (2000) Ecotoxicological risk assessment for Roundup® herbicide. Rev Environ Contam Toxicol 167:35–120

    CAS  Google Scholar 

  • 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 23:457–462

    Article  Google Scholar 

  • González CE, Zocco JL (1996) Controle integrado de Spodoptera frugiperda (Smith) utilizando Telenomus remus (Nixon) em Zea mays L. Rev Investig Agríc 1:201–219

    Google Scholar 

  • Greene GL, Leppla NC, Dickerson WA (1976) Velvetbean caterpillar: a rearing procedure and artificial medium. J Econ Entomol 69:487–488

    Article  Google Scholar 

  • Guo L, Desneux N, Sonoda S, Liang P, Han P, Gao X-W (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 (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 beneficial 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 Beneficial Organisms’. EPPO Bull 15:214–255

    Article  Google Scholar 

  • Hassan SA, Halsall N, Gray AP, Kuehner C, Moll M, Bakker FM, Roembke J, Yousef A, Nasr F, Abdelgader HA (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, pp 107–119

    Google Scholar 

  • Hernández D, Ferrer F, Linares B (1989) Introdución de Telenomus remus Nixon (Hym.: Scelionidae) para controlar Spodoptera frugiperda (Lep.: Noctuidae) em Yaritagua, Venezuela. Agron Trop 39:199–205

    Google Scholar 

  • Hinton HE (1981) Biology of insect eggs. Pergamon, Oxford, 473 p

    Google Scholar 

  • Howe CM, Berrill M, Pauli BD, Helbing CC, Werry K, Veldhoen N (2004) Toxicity of glyphosate-based pesticides to four North American frog species. Environ Toxicol Chem 23:1928–1938

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Lorenzi H (2000) Plantas daninhas do Brasil: terrestres, aquáticas, parasitas, tóxicas e medicinais, 3rd edn. Instituto Plantarum, Nova Odessa, 425p

    Google Scholar 

  • Mann RM, Bidwell JR (1999) The toxicity of glyphosate and several glyphosate formulations to four species of southwestern Australian frogs. Arch Environ Contam Toxicol 36:193–199

    Article  CAS  PubMed  Google Scholar 

  • Manzoni CG, Grützmacher AD, Giolo FP, Härter WR, Müller C (2007) Seletividade de agrotóxicos usados na produção integrada de maçã para adultos de Trichogramma pretiosum. Pesq Agrop Brasileira 41:1461–1467

    Article  Google Scholar 

  • Morales J, Gallardo S, Vásquez C, Ríos Y (2000) Patrón de emergência, longevidad, parasitismo y proporción sexual de Telenomus remus (Hymenoptera: Scelionidae) com relación al cogollero Del maíz. Bioagro 12:47–54

    Google Scholar 

  • Nörnberg SD, Grützmacher AD, Giolo FP, Júnior GJE, Lima CAB, Grützmacher DD (2008) Seletividade de formulações de glyphosate aplicado nos estádios imaturos de Trichogramma pretiosum. Planta Daninha 26:611–617

    Article  Google Scholar 

  • Pak GA, van Dalen A, Kaashoek N, Dijkman H (1990) Host egg chorion structure influencing host suitability for the egg parasitoid Trichogramma Westwood. J Insect Physiol 36:869–875

    Article  Google Scholar 

  • Parra JRP (2001) Técnicas de criação de insetos para programas de controle biológico. FEALQ, Piracicaba, 134p

    Google Scholar 

  • Planes L, Catalán J, Tena A, Porcuna JL, Jacas JA, Izquierdo J, Urbaneja A (2013) Lethal and sublethal effects of spirotetramat on the mealybug destroyer, Cryptolaemus montrouzieri. J Pest Sci 86:321–327

    Article  Google Scholar 

  • Pomari AF, Bueno AF, Bueno RCOF, Menezes Junior AO (2012) Biological characteristics and thermal requirements of the biological control agent Telenomus remus (Hymenoptera: Platygastridae) reared on eggs of different species of the genus Spodoptera (Lepidoptera: Noctuidae). Ann Entomol Soc Am 105:73–81

    Article  Google Scholar 

  • Prezotti L, Parra JRP, Vencovsky R, Dias CT, Cruz I, Chagas MCM (2002) Teste de vôo como critério de avaliação da qualidade de Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae): Adaptação de metodologia. Neotrop Entomol 31:411–417

    Article  Google Scholar 

  • Rizzardi MA, Fleck NG, Agostinetto D, Balbinot Junior AA (2003) Ação de herbicidas sobre mecanismos de defesa das plantas aos patógenos. Cienc Rural 33:957–965

    Article  Google Scholar 

  • Routledge EJ, Sumpter JP (1996) Estrogenic activity of surfactants and some of their degradation products assessed using a recombinant yeast screen. Environ Toxicol Chem 15:241–248

    Article  CAS  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 

  • Salt G (1938) Experimental studies in insect parasitism. VI. Host suitability. Bull Entomol Res 29:223–246

    Article  Google Scholar 

  • Santos KB, Meneguim AM, Santos WJ, Neves PMOJ, Santos RB (2010) Caracterização dos danos de Spodoptera eridania (Cramer) e Spodoptera cosmioides (Walker) (Lepidoptera: Noctuidae) a estruturas de algodoeiro. Neotrop Entomol 39:626–631

    Article  PubMed  Google Scholar 

  • SAS Institute (2001) SAS user’s guide: statistics: version 8.2. 6.ed. Cary. 201p

  • Schmidt JM (1994) Host recognition and acceptance by Trichogramma. In: Wajnberg E, Hassan SA (eds) Biological control with egg parasitoids. CAB International, Wallingford, pp 165–200

    Google Scholar 

  • Schmidt JM, Smith JJB (1987) The measurement of exposed host volume by the parasitoid wasp Trichogramma minutum and effects of wasp size. Can J Zool 65:2837–2845

    Article  Google Scholar 

  • Shaner DL (2000) The impact of glyphosate-tolerant crops on the use of other herbicides and on resistance management. Pest Manag Sci 56:320–326

    Article  CAS  Google Scholar 

  • Shapiro SS, Wilk MB (1965) An analysis of variance test for normality. Biometrika 52:591–611

    Article  Google Scholar 

  • Shrestha A, Steinhauer KM, Moretti ML, Hanson BD, Jasieniuk M, Hembree KJ, Wright SD (2014) Distribution of glyphosate-resistant and glyphosate-susceptible hairy fleabane (Conyza bonariensis) in central California and their phenological development. J Pest Sci 87:201–209

    Article  Google Scholar 

  • Sohrabi F, Shishehbor P, Saber M, Mosaddegh MS (2013) Lethal and sublethal effects of imidacloprid and buprofezin on the sweetpotato whitefly parasitoid Eretmocerus mundus (Hymenoptera: Aphelinidae). Crop Prot 45:98–103

    Article  CAS  Google Scholar 

  • Stinner RE (1977) Efficacy of inundative releases. Annu Rev Entomol 22:515–531

    Article  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Travlos IS, Chachalis D (2013) Relative competitiveness of glyphosate-resistant and glyphosate-susceptible populations of hairy fleabane, Conyza bonariensis. J Pest Sci 86:345–351

    Article  Google Scholar 

  • van der Werf HMG (1996) Assessing the impact of pesticides on the environment. Agric Ecosyst Environ 60:81–96

    Article  Google Scholar 

  • Wijnands FG (1997) Integrated crop protection and environment exposure to pesticides: methods to reduce use and impact of pesticides in arable farming. Eur J Agron 7:251–260

    Article  Google Scholar 

  • Williams GM, Kroes R, Munro IC (2000) Safety evaluation and risk assessment of the herbicide Roundup and is active ingredient, glyphosate, for humans. Regul Toxicol Pharmacol 31:117–165

    Article  CAS  PubMed  Google Scholar 

  • Yu SJ (1987) Biochemical defense capacity in the spined soldier bug (Podisus maculiventris) and its lepidopterous prey. Pestic Biochem Physiol 28:216–223

    Article  CAS  Google Scholar 

Download references

Acknowledgments

Thanks are extended to Dagmar Frisch for the English revision of this manuscript. This paper was approved for publication by the Editorial Board of Embrapa Soja. The authors would like to thank Embrapa Soja, the “Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES),” and the “Conselho Nacional de Desenvolvimento Científico e Tecnológico” (CNPq), grant number 301420/2012-2, for funds that supported this research.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to A F Bueno.

Additional information

Edited by Moisés J Zotti - UFPel

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Stecca, C.S., Bueno, A.F., Pasini, A. et al. Side-Effects of Glyphosate to the Parasitoid Telenomus remus Nixon (Hymenoptera: Platygastridae). Neotrop Entomol 45, 192–200 (2016). https://doi.org/10.1007/s13744-016-0363-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13744-016-0363-4

Keywords

Navigation