Susceptibility of the egg parasitoid Trichogramma achaeae (Hymenoptera: Trichogrammatidae) to selected insecticides used in tomato greenhouses

Juan R. Gallego, Jesús Guerrero-Manzano, Francisco J. Fernández-Maldonado, Tomas Cabello

Abstract


The South American tomato moth Tuta absoluta (Meyrick) (Lepidoptera: Gelechiidae) is a pest species of great economic importance in tomatoes, both in greenhouses and in open-air crops. This importance has increased in recent years because it has been introduced in many countries in Europe, Africa, and Asia. Insecticides different active ingredients and biological control agents are being used in the control of this pest species. This implies the need to make both groups compatible within IPM programmes. Therefore, the objective of this work was to study the compatibility between different insecticides and the use of the egg parasitoid Trichogramma achaeae Nagaraja and Nagakartti (Hymenoptera: Trichogrammatidae). Three groups of trials were carried out under laboratory and greenhouse conditions. Ten insecticides with the following active ingredient were evaluated: abamectin, azadirachtin, Bacillus thuringiensis, chlorantraniliprole, emamectin, flubendiamide, indoxacarb, methomyl, spinosad, and spiromesifen. In the results, three groups of insecticides were established based on their compatibility with the use of biological control: The first group (abamectin, B. thurigiensis, flubendiamide, indoxacarb and spiromesifen) showed a high degree of compatibility with egg parasitoid releases. The second group (azadirachtin and chlorantraniliprole, and methomyl) presented compatibility problems. Finally, the last group (emamectin, methomyl, and spinosad) did not apper to be compatible. The results found will allow a better application of IPM programmes in tomato crops for the control of this pest species.


Keywords


biological control; IPM; ecotoxicology; South American tomato moth; parasitoid; insecticides; side effects

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References


Amano H, Haseeb M, 2001. Recently-proposed methods and concepts of testing the effects of pesticides on the beneficial mite and insect species: study limitations and implications in IPM. Appl Entomol Zool 36: 1-11. https://doi.org/10.1303/aez.2001.1

Aruna KT, Aruna RK, 2015. Pairwise comparison of coefficients of variation for correlated samples. Int J Stat Apl 5: 231-236.

Bielza P, 2010. La resistencia a insecticidas en Tuta absoluta. Phytoma España 217: 103-106.

Biondi A, Guedes RNC, Wan FH, Desneux N, 2018. Ecology, worldwide spread, and management of the invasive South American tomato pinworm, Tuta absoluta: past, present, and future. Annu Rev Entomol 63: 239-258. https://doi.org/10.1146/annurev-ento-031616-034933

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. https://doi.org/10.1002/ps.1977

Brunner JF, Dunley JE, Doerr MD, Beers EH., 2001. Effect of pesticides on Colpoclypeus florus (Hym.: Eulophidae) and Trichogramma platneri (Hym.: Trichogrammatidae), parasitoids of leafrollers in Washington. J Econ Entomol 94: 1075-1084. https://doi.org/10.1603/0022-0493-94.5.1075

Bueno AF, Bueno COF, Parra JRP, Vieira SS, 2008. Effects of pesticides used in soybean crops to the egg parasitoid Trichogramma pretiosum. Cienc Rural 38: 1495-1503. https://doi.org/10.1590/S0103-84782008000600001

Bull DL, House VS, 1983. Effects of different insecticides on parasitism of host eggs by Trichogramma pretiosum Riley. Southwestern Entomol 8:46-53.

Cabello T, 1985. Biología de dos especies de Trichogramma (Hym.: Trichogrammatidae) parasitas de Helicoverpa spp. (Lep.: Noctuidae) en algodonero. Posibilidades de su empleo como agentes de control biológico. Dissertation, Universidad de Cordoba, Spain.

Cabello T, 2009. Cultivos hortícolas bajo abrigo: control biológico de Tuta absoluta en tomate. In: Uso sostenible de fitosanitarios; pp: 199-217. Junta de Andalucía, Sevilla, Spain.

Cabello T, Gallego JR, Vila E, Soler A, Pino M del, Carnero A, Hernández-Suárez E, Polaszek A, 2009. Biological control of the South American tomato pinworm Tuta absoluta (Lep.: Gelechiidae), with releases of Trichogramma achaeae (Hym.: Trichogrammatidae) in tomato greenhouses of Spain. IOBC/WPRS Bull 49: 225-230.

Cabello T, Gallego JR, Fernandez, de Scals D, Rubio A, Salvatierra S, Parra A, 2010. New simple methodology to evaluate the insecticide side-effects on Trichogramma species (Hym.: Trichogrammatidae) in greenhouse crops. IX Eur Congr Entomol, Budapest, Aug 22-27. p: 222.

Cabello T, Gallego JR, Fernandez FJ, Gamez M, Vila E, Pino M del, Hernandez-Suarez E, 2012. Biological control strategies for the South American tomato moth (Lep.: Gelechiidae) in greenhouse tomatoes. J Econ Entomol 105: 2085-2096. https://doi.org/10.1603/EC12221

Campbell CD, Walgenbach JF, Kennedy GG, 1991. Effect of parasitoids on lepidopterous pest in insecticide treated and untreated tomatoes in western North Carolina. J Econ Entomol 84: 1662-1667. https://doi.org/10.1093/jee/84.6.1662

Campos MR, Biondi A, Adiga A, Guedes RNC, Desneux N, 2017. From the Western Palaeartic region to beyond: Tuta absoluta 10 years after invading Europe. J Pest Sci 90: 787-796. https://doi.org/10.1007/s10340-017-0867-7

Carvalho GA, Reis PR, Rocha LCD, Moraes JC, Fuini LC, Ecole CC, 2003. Side-effects of insecticides used in tomato fields on Trichogramma pretiosum (Hym.: Trichogrammatidae). Acta Sci-Agron 25: 275-279. https://doi.org/10.4025/actasciagron.v25i2.1771

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 Parasitoid News, IOBC 17: 27.

Chapman AV, Kuhar TP, Schultz PB, Brewster CC, 2009. Dispersal of Trichogramma ostriniae (Hym.: Trichogrammatidae) in potato fields. Environ Entomol 38: 677-685. https://doi.org/10.1603/022.038.0319

Clark B, Hillocks R, 2014. Integrated pest management for European agriculture. In: Integrated pest management; Pimentel D, Peshin, R (eds.). pp: 73-97. Springer, NL. https://doi.org/10.1007/978-94-007-7796-5_3

Consoli FL, Parra JRP, Hassan SA, 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. https://doi.org/10.1111/j.1439-0418.1998.tb01459.x

Consoli FL, Botelho PSM, Parra JRP, 2001. Selectivity of insecticides to the egg parasitoid Trichogramma galloi (Hym., Trichogrammatidae). J Appl Entomol 125: 37-43. https://doi.org/10.1046/j.1439-0418.2001.00513.x

Costa MA, Moscardini VF, da Costa-Gontijo P Carvalho GA, Oliveira RL, Oliveira HN, 2014. Sublethal and transgenerational effects of insecticides in developing Trichogramma galloi (Hym.: Trichogrammatidae). Ecotoxicology 23: 1399-1408. https://doi.org/10.1007/s10646-014-1282-y

Dent D, 2000. Insect pest management. CAB Int, Wallingford, UK. 410 pp. https://doi.org/10.1079/9780851993409.0000

Desneux N, Luna MG, Guillemaud T, Urbaneja A, 2011. The invasive South American tomato pinworm, Tuta absoluta, continues to spread in Afro-Eurasia and beyond: the new threat to tomato world production. J Pest Sci 84: 403-408. https://doi.org/10.1007/s10340-011-0398-6

EC, 2009. Regulation (EC) No 1107/2009 of the European Parliament and of the Council of 21 October 2009 concerning the placing of plant protection products on the market and repealing Council Directives 79/117/EEC and 91/414/EEC. https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=celex%3A32009R1107

EPPO, 1999. Standards PP1/180(2) - Side-effects on Trichogramma cacoeciae. In: EPPO standards: guidelines for the efficacy evaluation of plant protection products. Efficacy evaluation of plant protection products; EPPO. Vol 1, pp: 165-172. European and Mediterranean Plant Protection Organization, Paris.

FAO, 1966. Proceeding of the FAO symposium on integrated pest control. Rome. 129 pp.

Fontes J, Sanchez-Roja I, Tavares J, Oliveira L, 2018. Lethal and sublethal effects of various pesticides on Trichogramma achaeae (Hym.: Trichogrammatidae). J Econ Entomol 111:1219-1226. https://doi.org/10.1093/jee/toy064

Gentz MC, Murdoch G, King GF, 2010. Tandem use of selective insecticides and natural enemies for effective, reduced-risk pest management. Biol Control 52: 208-215. https://doi.org/10.1016/j.biocontrol.2009.07.012

Goulart RM, Volpe HXL, Vacari AM, Thuler RT, de Bortoli SA, 2012. Insecticide selectivity to two species of Trichogramma in three different hosts, as determined by IOBC/WPRS methodology. Pest Manag Sci 68: 240-244. https://doi.org/10.1002/ps.2251

Guedes RNC, Picanço MC, 2012. The tomato borer Tuta absoluta in South America: pest status, management and insecticide resistance. EPPO Bull 42: 211-216. https://doi.org/10.1111/epp.2557

Hassan SA, 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. https://doi.org/10.1111/j.1365-2338.1985.tb00224.x

Hassan SA, 1998. Defining the problem. Introduction. In: Ecotoxicology. Pesticides and beneficial organisms; Haskell PT, McEwen P (eds.). pp: 55-68. Springer, Boston, USA.

Hassan SA, Albert R, Bigler F, Blaisinger P.; Bogenschütz H, Boller E, Brun J, Chiverton P, Edwards P, Englert WD, Huang P, et al., 1987. Results of third joint pesticide testing programme by the IOBC/WPRS-working group pesticides and beneficial organisms. J Appl Entomol 103: 92-107. https://doi.org/10.1111/j.1439-0418.1987.tb00963.x

Hassan SA, Bigler F, Bogenschutz H, Boller E, Brun J, Calis JNM, Chiverton P, Coremans-Pelseneer J, Duso C, Lewis GB, et al., 1991. Results of the fifth joint pesticide testing programme carried out by the IOBC/wprs Working Group "Pesticides and Beneficial Organisms". Entomophaga 36: 55-67. https://doi.org/10.1007/BF02374636

Hassan SA, Halsall N, Gray AP, Abdelgader H, 2000. Laboratory method to evaluate the side effects of plant protection products on Trichogramma cacoeciae Marchal (Hym., Trichogrammatidae). In: Guidelines to evaluate side effects of plant protection products to non-target arthropod; Candolfi MP, Blumel S, Forster R (eds.). pp: 107-119. Dreier Druck, Reinheim, Germany.

Hewa-Kapuge S, McDougall S, Hoffmann AA, 2003. Effects of methoxyfenozide, indoxacarb, and other insecticides on the beneficial egg parasitoid Trichogramma nr. brassicae (Hym.: Trichogrammatidae) under laboratory and field conditions. J Econ Entomol 96: 1083-1090. https://doi.org/10.1093/jee/96.4.1083

IRAC, 2016. Mode of action classification: insecticide resistance management. Insecticide Resistance Action Committee. http://www.irac-online.org/documents/moa-classification/?ext=pdf. [19 Feb 2018].

Jalali SK, Mohanraj P, Lakshmi BL, 2016. Trichogrammatids. In: Ecofriendly pest management for food security; Omkar (ed.). pp: 139-181. Acad Press, San Diego, USA. https://doi.org/10.1016/B978-0-12-803265-7.00005-1

Jepson PC, 1998. Insects, spiders and mites. In: Handbook of ecotoxicology; Calow P (ed.). pp: 299-325. Blackwell, Oxford, UK. https://doi.org/10.1002/9781444313512.ch15

Kavitha J, Kuttalam S, Chandrasekaran S, Ramaraju, K, 2006. Effect of spiromesifen 240 SC on beneficial insects. Ann Plant Protect Sci 14: 343-345.

Ksentini I, Jardak T, Zeghal N, 2010. Bacillus thuringiensis, deltamethrin and spinosad side-effects on three Trichogramma species. Bull Insectol 63: 31-37.

Kumar P, Sekhar JC, Kaur J, 2013. Trichogrammatids: Integration with other methods of pest control. In: Biological control of insect pests using egg parasitoids; Sithanantham S et al. (eds.). pp: 191-208. Springer, New Delhi, India. https://doi.org/10.1007/978-81-322-1181-5_9

Lefebvre M, Langrell SRH, Gomez-y-Paloma S, 2015. Incentives and policies for integrated pest management in Europe: A review. Agron Sustain Dev 35: 27-45. https://doi.org/10.1007/s13593-014-0237-2

Leppla NC, Johnson MW, Merritt JL, Zalom FG, 2017. Applications and trends in commercial biological control for arthropod pest of tomato. In: Sustainable managements of arthropod pest of tomato; Wakil W, Brust GE, Perring TM (eds.). pp: 283-303. Acad Press, London. https://doi.org/10.1016/B978-0-12-802441-6.00013-9

Liu TX, Zhang Y, 2012. Side effects of two reduced-risk insecticides, indoxacarb and spinosad, on two species of Trichogramma (Hym.: Trichogrammatidae) on cabbage. Ecotoxicology 21: 2254-2263. https://doi.org/10.1007/s10646-012-0981-5

Maia JB, Carvalho GA, Leite MIS, Lopes-de-Oliveira R, Makyama L, 2010. Selectivity of insecticides used in corn crops to adult Trichogramma atopovirilia (Hym.: Trichogrammatidae). Rev Colomb Entomol 36: 202-206.

Martins TB; Pereira SM, Carneiro AV, Betetto MJ, Bueno AF, 2011. Seletividade de productos fitossanitários a pupas de Trichogramma pretiosum emovos de Anagasta kuehniella. In: VI Jornada Acadêmica da Embrapa Soja; Saraiva OF, Melo PGS (eds.). pp: 38-41. EmbrapaSoja, Londrina, Brazil.

Moura AP, Carvalho GA, Pereira AE, Ricga KCD, 2006. Selectivity evaluation of insecticides used to control tomato pests to Trichogramma pretiosum. BioControl 51: 769-778. https://doi.org/10.1007/s10526-006-0001-x

Nornberg SD, Grützmacher AD, Kovaleski A, Camargo ES, Pasini RA, 2009. Toxicidade de agrotóxicos utilizados naprodução integrada de maçã a Trichogramma pretiosum Riley, 1879 (Hym.: Trichogrammatidae) em condições de laboratório. Curr Agric Sci Tech 15: 1-4.

Oliveira HN de, Antigo MR, de Carvalho GA, Glaeser DF, Pereira FF, 2013. Seletividade de inseticidas utilizados na cana-de-açúcar a adultos de Trichogramma galloi Zucchi (Hym.: Trichogrammatidae). Biosci J 29: 1267-1274.

Pinto JH, Stouthamer R, 1994. Systematics of the Trichogrammatidae with emphasis on Trichogramma. In: Biological control with egg parasitoids; Wajnberg E, Hassan SA (eds.). pp. 1-36. CAB Int, Wallingford, UK.

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: 209-215. https://doi.org/10.1007/s12600-009-0031-x

Querino RB, Zucchi RA, Pinto JD, 2010. Systematics of the Trichogrammatidae (Hym.: Chalcidoidea) with a focus on the genera attacking Lepidoptera. In: Egg parasitoids in agroecosystems with emphasis on Trichogramma; Cônsoli FL, Parra JRP, Zucchi RA (eds.). pp: 191-219. Springer, NY. https://doi.org/10.1007/978-1-4020-9110-0_7

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 (Hym.: Trichogrammatidae). Egg Parasitoid News, IOBC 17: 28.

Roditakis E, Vasakis E, Garcıa-Vidal L, Martınez-Aguirre MR, Rison JL, Haxaire-Lutun MO, Nauen R, Tsagkarakou A, Bielza P, 2018. A four-year survey on insecticide resistance and likelihood of chemical control failure for tomato leaf miner Tuta absoluta in the European/Asian region. J Pest Sci 91: 421-435. https://doi.org/10.1007/s10340-017-0900-x

Rodriguez JR, Pintureau B, Galan M, 1994. Déterminisme de la couleur des hôtes parasités par Trichogramma fuentesi. Entomol Exp Appl 70: 121-128. https://doi.org/10.1111/j.1570-7458.1994.tb00740.x

Romeis J, Shanower TG, Zebitz CPW, 1998. Response of Trichogramma egg parasitoids to colored sticky traps. BioControl 43: 17-27. https://doi.org/10.1023/A:1009905722193

Saber M, Hejazi MJ, Hassan SA, 2004. Effects of azadirachtin/neemazal on different stages and adult life table parameters of Trichogramma cacoeciae (Hym.: Trichogrammatidae). J Econ Entomol 97: 905-910. https://doi.org/10.1093/jee/97.3.905

Saelices RM, López A, Amor F, Benchochea P, Fernandez MM, Garzon A, Morales I, Velazquez E, Medina P, Adaan A, et al., 2012. Ecotoxicidad de insecticidas de uso frecuente en el cultivo del tomate, en el enemigo natural Trichogramma achaeae (Hym.: Trichogrammatidae). Bol San Veg Plagas 38: 95-108.

Saljoqi AUR, Nawaz M, Farid A, Khan IA, 2012. Compatibility of spinosad with Trichogramma chilonis (Hym.: Trichogrammatidae) in integrated pest management of Sitotroga cerealella. Pak J Zool 44: 133-139.

Sanchez C, Gallego JR, Gamez M, Cabello T, 2014. Intensive biological control in Spanish greenhouses: problems of the success. Int J Biol Biomol Agric Food Biotechnol Eng 8: 1128-1132.

Sattar S, Farmanullah, Saljoqi AR, Arif M, Sattar H, Qazi JI, 2011. Toxicity of some new insecticides against Trichogramma chilonis (Hym.: Trichogrammatidae) under laboratory and extended laboratory conditions. Pak J Zool 43: 1117-1125.

Schindelin J, Arganda-Carreras I, Frise E, Aynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, et al., 2012. Fiji: an open-source platform for biological-image analysis. Nat Methods 9: 676-682. https://doi.org/10.1038/nmeth.2019

Scholz BCG, Zalucki MP, 2000. The effects of two new insecticides on the survival of adult Trichogramma pretiosum Riley in sweet corn. In: Hymenoptera: evolution, biodiversity and biological control; Austin A, Dowton M (eds.). pp: 381-388. CSIRO Publ, Clayton, AU.

Smith SM, 1996. Biological control with Trichogramma: advances, successes, and potential of their use. Annu Rev Entomol 41: 375-406. https://doi.org/10.1146/annurev.en.41.010196.002111

Stanley J, Preetha G, 2016. Pesticide toxicity to non-target organisms: exposure, toxicity and risk assessment methodologies. Springer Science+Business Media, Dordrecht: 502 pp. https://doi.org/10.1007/978-94-017-7752-0

Stark J, Jepson PC, Mayer DF, 1995. Limitations to use of topical toxicity data for predictions of pesticide side effects in the field. J Econ Entomol 88: 1081-1088. https://doi.org/10.1093/jee/88.5.1081

Sterk G, Hassan SA, Baillod M, Bakker F, Bigler F, Blümel S, Bogenschütz H, Boller E, Bromand B, Brun J, et al., 1999. Results of the seventh joint pesticide testing programme carried out by the IOBC/WPRS-Working Group "Pesticides and Beneficial Organisms". BioControl 44: 99-117.

Suh CPC, Orr DB, Van Duyn JW, 2000. Effect of insecticides on Trichogramma exiguum (Hym.: Trichogrammatidae) preimaginal development and adult survival. J Econ Entomol 93: 577-583. https://doi.org/10.1603/0022-0493-93.3.577

Takada Y, Kawamura S, Tanaka T, 2001. Effects of various insecticides on the development of the egg parasitoid Trichogramma dendrolimi (Hym.: Trichogrammatidae). J Econ Entomol 94: 1340-1343. https://doi.org/10.1603/0022-0493-94.6.1340

Tipping PW, Burbutis PP, 1983. Some effects of pesticide residues on Trichogramma nubilale (Hym.: Trichogrammatidae). J Econ Entomol 76: 892-896. https://doi.org/10.1093/jee/76.4.892

van Lenteren JC, Bolckmans K, Kohl J, Ravensberg WJ, Urbaneja A, 2018. Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl 63: 63-59. https://doi.org/10.1007/s10526-017-9801-4

Vianna UR, Pratissoli JD, Zanuncio C, Serrao JE, 2009. Insecticide toxicity to Trichogramma pretiosum (Hym.: Trichogrammatidae) females and effect on descendant generation. Ecotoxicology 18: 180-186. https://doi.org/10.1007/s10646-008-0270-5

Vila E, Cabello T, 2014. Biosystems engineering applied to greenhouse pest control. In: Biosystems engineering: biofactories for food production in the Century XXI; Guevara-Gonzalez R, Torres-Pacheco I (eds.). pp: 99-128. Springer, Cham, CH. https://doi.org/10.1007/978-3-319-03880-3_4

Williams T, Valle J, Viñuela E, 2003. Is the naturally derived insecticide spinosad compatible with insect natural enemies? Biocontrol Sci Technol 13: 459-475. https://doi.org/10.1080/0958315031000140956

Yong TH, Hoffmann MP, 2006. Habitat selection by the introduced biological control agent Trichogramma ostriniae (Hym.: Trichogrammatidae) and implications for nontarget effects. Environ Entomol 35: 725-732. https://doi.org/10.1603/0046-225X-35.3.725




DOI: 10.5424/sjar/2019172-14413