Parasitism capacity of Trichogramma pretiosum Riley, 1879 and Telenomus remus Nixon, 1937 after ingestion of biological pesticides
DOI:
https://doi.org/10.5433/1679-0359.2022v43n4p1441Keywords:
Biological control, Egg parasitoids, Entomopathogens, Selectivity.Abstract
Augmentative biological control (ABC) of insect pests is an environmentally sustainable alternative to synthetic insecticides. By performing BC, more than one control agent can be used for the same insect pest that is in different stages of its life cycle or for pests that simultaneously occur in the area. However, this relationship requires biosecurity for the control agents employed. The aim of this study was to evaluate the parasitism capacity of Trichogramma pretiosum Riley, 1879 and Telenomus remus Nixon, 1937 after ingestion of biological pesticides. The entomopathogens, Baculovirus Anticarsia gemmatalis nucleopolyhedrovirus (AgMNPV), Bacillus thuringiensis (Bt) var. kurstaki, Bt var. aizawai, Beauveria bassiana, and Metarhizium anisopliae; the microbiological fungicide, Trichoderma harzianum, at concentrations recommended by the manufacturer; and a negative control (pure honey) were employed in this study. Further, forced ingestion was adopted, with the treatments mixed in honey and offered as food at two dilutions (one-part product: one-part honey and one-part product: nine parts honey). Each treatment consisted of 20 individual females for each parasitoid (T. pretiosum or T. remus). The following parameters were evaluated: female longevity, number of parasitized eggs, egg viability, and number of females and males to determine the sex ratio. For T. pretiosum, B. bassiana (1 × 1013 viable conidia 100 L H2O-1), and T. harzianum (5 × 1012 viable conidia 100 L H2O-1), the longevity of their females was reduced by the 1:1 mixture; however, this mixture did not interfere with other parameters and other biological pesticides compared to the respective controls of both dilutions. The biological pesticides did not negatively influence the parameters evaluated for T. remus. The tested products had low toxicity to the egg parasitoids, T. pretiosum and T. remus. Overall, more work is still required with parasitoids in other stages of development and with other exposure methods to confirm the selectivity of products for egg parasitoids to recommend its combined use in the field.References
Alves, S. B. (1998). Controle microbiano de insetos. FEALQ.
Amaro, J. T., Bueno, A. de F., Neves, P. M. O. J., Silva, D. M. da, Pomari-Fernandes, A., & Favetti, B. M. (2018). Selectivity of different biological products to the egg parasitoid Telenomus remus (Hymenoptera: Platygastridae). Revista Brasileira de Entomologia, 62(3), 195-197. doi: 10.1016/j.rbe.2018.04.003
Amaro, J. T., Bueno, A. F., Pomari-Fernandes, A. F., & Neves, P. M. O. J. (2015). Selectivity of organic products to Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). Neotropical Entomology, 44(5), 489-497. doi: 10.1007/s13744-015-0317-2
Aquino, M. F. de S., Sujii, E. R., Borges, M., Moraes, M. C. B., & Laumann, R. A. (2018). Diversity of stink bug adults and their parasitoids in soybean crops in Brazil: influence of a latitudinal gradient and insecticide application intensity. Environmental Entomology, 48(1), 105-113. doi: 10.1093/ee/nvy174
Araujo, E. S., Poltronieri, A. S., Poitevin, C. G., Mirás-Avalos, J. M., Zawadneak, M. A. C., & Pimentel, I. C. (2020). Compatibility between entomopathogenic fungi and EGG parasitoids (Trichogrammatidae): A laboratory study for their combined use to control Duponchelia fovealis. Insects, 11(9), 1-14. doi: 10.3390/insects11090630
Bortolotto, O. C., Pomari-Fernandes, A., Bueno, R. C. O. de F., Bueno, A. de F., Cruz, Y. K. S. da, Sanzovo, A., & Ferreira, R. B. (2015). The use of soybean integrated pest management in Brazil: a review. Agronomy Science and Biotechnology, 1(1), 25-32. doi: 10.33158/asb.2015v1i1p25
Boudh, S., & Singh, J. S. (2019). Pesticide contamination: problems and remediation strategies. In R. Bharagava, & P. Chowdary (Eds.), Emerging and eco-friendly approaches for waste management (pp. 245-269). Singapore.
Bueno, A. de F., Carvalho, G. A., Santos, A. C. dos, Sosa-Gómez, D. R., & Silva, D. M. da. (2017a). Pesticide selectivity to natural enemies: challenges and constraints for research and field recommendation. Ciência Rural, 47(6), 1-10. doi: 10.1590/0103-8478cr20160829
Bueno, A. F., Panizzi, A. R., Hunt, T. E., Dourado, P. M., Pitta, R. M., & Gonçalves, J. (2021). Challenges for adoption of Integrated Pest Management (IPM): the soybean example. Neotropical Entomology, 50(1), 5-20. doi: 10.1007/s13744-020-00792-9
Bueno, R. C. de O., Raetano, C. G., Dorneles, J. Jr., & Carvalho, F. K. (2017b). Integrated management of soybean pests: the example of Brazil. Outlooks on Pest Management, 28(5), 149-153. doi: 10.1564/v28
Bueno, R. C. O. de F., Parra, J. R. P., & Bueno, A. de F. (2012). Trichogramma pretiosum parasitism of Pseudoplusia includens and Anticarsia gemmatalis eggs at different temperatures. Biological Control, 60(2), 154-162. doi: 10.1016/j.biocontrol.2011.11.005
Burr, I. W., & Foster, L. A. (1972). A test for equality of variances. University of Purdue.
Carvalho, G. A., Moura, A. P., & Bueno, V. H. P. (2006). Side effects of pesticides on Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). In C. Castañé, & J. A. Sanchez (Eds.), IOBC/WPRS Bulletin (pp. 355-359). France.
Desneux, N., Decourtye, A., & Delpuech, J. M. (2007). The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52(1), 81-106. doi: 10.1146/annurev.ento.52.110405.091440
DiBartolomeis, M., Kegley, S., Mineau, P., Radford, R., & Klein, K. (2019). An assessment of acute insecticide toxicity loading (AITL) of chemical pesticides used on agricultural land in the United States. PLoS ONE, 14(8), 1-27. doi: 10.1371/journal.pone.0220029
Feltrin-Campos, E., Rigenberg, R., Carvalho, G. A., Glaeser, D. F., & Oliveira, H. N. de. (2018). Selectivity of insecticides against adult Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae) on Cassava. Journal of Agricultural Science, 11(1), 546. doi: 10.5539/jas.v11n1p546
Gomes, S. M. (1997). Comparação de três hospedeiros alternativos para criação e produção massal de Trichogramma pretiosum Riley, 1879 e T. galloi Zucchi, 1988. Tese de Doutorado, Universidade de São Paulo, Piracicaba, SP, Brasil.
Goulson, D. (2013). An overview of the environmental risks posed by neonicotinoid insecticides. Journal of Applied Ecology, 50(4), 977-987. doi: 10.1111/1365-2664.12111
Greene, G. L., Leppla, N. C., & Dickerson, W. A. (1976). Velvetbean caterpillar: a rearing procedure and artificial medium. Journal of Economic Entomology, 69(4), 487-488. doi: 10.1093/jee/69.4.487
Hardy, I. C. W. (1994). Sex ratio and mating structure in the parasitoid Hymenoptera. Oikos, 69(1), 3-20. doi: 10.2307/3545278
Hassan, S. A., Halsall, N., Gray, A. P., Kuehner, C., Moll, M., Bakker, F. M., Roembke, J., Yousef, A., Nasr, F., & Abdelgader, H. A. (2000). A laboratory method to evaluate the side effects of plant protection products on Trichogramma cacoeciae Marchal (Hymenoptera: Trichogrammatidae). In M. P Candolfi, S. Blümel, R. Forster, F. M. Bakker, C. Grimm, S. A. Hassan, U. Heimbach, M. A. Mead-Briggs, B. Raber, R. Schmuck, & H. Vogt (Eds.), Guidelines to evaluate side-effects of plant protection products to non-target arthropods (pp. 107-119). Gent, Belgium.
Hladik, M. L., Main, A. R., & Goulson, D. (2018). Environmental risks and challenges associated with neonicotinoid insecticides. Environmental Science and Technology, 52(6), 3329-3335. doi: 10.1021/acs. est.7b06388
Khan, M. A., & Ahmad, W. (2019). Synthetic chemical insecticides: environmental and agro contaminants. In M. A. Khan, & W. Ahmad (Eds.), Microbes for sustainable insect pest management: An eco-friendly approach (pp. 1-22). Switzerland.
Koch, R. L., Hodgson, E. W., Knodel, J. J., Varenhorst, A. J., & Potter, B. D. (2018). Management of insecticide-resistant soybean aphids in the upper midwest of the United States. Journal of Integrated Pest Management, 9(1), 1-7. doi: 10.1093/jipm/pmy014
Lacey, L. A. (Ed.). (2016). Microbial control of insect and mite pests: from theory to practice. Academic Press.
Lacey, L. A., Grzywacz, D., Shapiro-Ilan, D. I., Frutos, R., Brownbridge, M., & Goettel, M. S. (2015). Insect pathogens as biological control agents: Back to the future. Journal of Invertebrate Pathology, 132(1), 1-41. doi: 10.1016/j.jip.2015.07.009
Lima, J. A. M. de C., Labanowski, J., Bastos, M. C., Zanella, R., Prestes, O. D., Vargas, J. P. R. de, Mondamert, L., Granado, E., Tiecher, T., Zafar, M., Troian, A., Le Guet, T., & Santos, D. R. dos. (2020). “Modern agriculture” transfers many pesticides to watercourses: a case study of a representative rural catchment of southern Brazil. Environmental Science and Pollution Research, 27(10), 10581-10598. doi: 10.1007/s11 356-019-06550-8
Mannino, M. C., Huarte-Bonnet, C., Davyt-Colo, B., & Pedrini, N. (2019). Is the insect cuticle the only entry gate for fungal infection? Insights into alternative modes of action of entomopathogenic fungi. Journal of Fungi, 5(2), 1-9. doi: 10.3390/jof5020033
Mills, N. J., & Kuhlmann, U. (2000). The relationship between egg load and fecundity among Trichogramma parasitoids. Ecological Entomology, 25(3), 315-324. doi: 10.1046/j.1365-2311.2000.00260.x
Nascimento, P. T., Fadini, M. A. M., Valicente, F. H., & Ribeiro, P. E. A. (2018). Does Bacillus thuringiensis have adverse effects on the host egg location by parasitoid wasps? Revista Brasileira de Entomologia, 62(4), 260-266. doi: 10.1016/j.rbe.2018.09.006
Parra, J. (2014). Biological control in Brazil: an overview. Scientia Agricola, 71(5), 420-429. doi: 10.1590/01 03-9016-2014-0167
Parra, J. R. P., Lopes, J. R. S., Serra, H. J. P., & Sales, O., Jr. (1989). Metodologia de criação de Anagasta kuehniella (Zeller, 1879) para produção massal de Trichogramma spp. Anais da Sociedade Entomológica Brasileira, 18(2), 403-415. doi: 10.37486/0301-8059.v18i2.603
Pinto, L. M. N., & Fiuza, L. M. (2003). Distribuição de genes cry de Bacillus thuringiensis isolados de solos do Estado do Rio Grande do Sul, Brasil. Ciência Rural, 33(4), 699-702. doi: 10.1590/s0103-8478200300 0400018
Pomari, A. F., Bueno, A. D. F., Freitas Bueno, R. C. O. de, & Oliveira Menezes, A. de. (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). Annals of the Entomological Society of America, 105(1), 73-81. doi: 10.1603/AN11115
Potrich, M., Alves, L. F. A, Haas, J., Silva, E. R. L. da, Daros, A., Pietrowski, V., & Neves, P. M. O. J. (2009). Selectivity of Beauveria bassiana and Metarhizium anisopliae to Trichogramma pretiosum Riley (Hymenoptera: Trichogrammatidae). Neotropical Entomology, 38(6), 822-826. doi: 10.1590/s1519-566x 2009000600016
Potrich, M., Alves, L. F. A., Lozano, E., Roman, J. C., Pietrowski, V., & Neves, P. M. O. J. (2015). Interactions between Beauveria bassiana and Trichogramma pretiosum under laboratory conditions. Entomologia Experimentalis et Applicata, 154(3), 213-221. doi: 10.1111/eea.12272
Qu, S., & Wang, S. (2018). Interaction of entomopathogenic fungi with the host immune system. Developmental and Comparative Immunology, 83(1), 96-103. doi: 10.1016/j.dci.2018.01.010
Queiroz, A. P., Bueno, A. de F., Pomari-Fernandes, A., Grande, M. L. M., Bortolotto, O. C., & Silva, D. M. (2016). Low temperature storage of Telenomus remus (Nixon) (Hymenoptera: Platygastridae) and its factitious host Corcyra cephalonica (Stainton) (Lepidoptera: Pyralidae). Neotropical Entomology, 46(2), 182-192. doi: 10.1007/s13744-016-0442-6
Shakeri, J., & Foster, H. A. (2007). Proteolytic activity and antibiotic production by Trichoderma harzianum in relation to pathogenicity to insects. Enzyme and Microbial Technology, 40(1), 961-968. doi: 10.1016/ j.enzmictec.2006.07.041
Shapiro, S., & Wilk, M. B. (1965). An analysis of variance test for normality. Biometrika, 52(3/4), 591-611. doi: 10.2307/2333709
Silva, D. M. da, & Bueno, A. de F. (2015). Organic products selectivity for Trichogramma pretiosum (Hymenoptera: Trichogrammatidae). Arquivos do Instituto Biológico, 82(1), 1-8. doi: 10.1590/1808-165 7000422013
Silva, D. M. da, Freitas Bueno, A. de, Andrade, K., Santos Stecca, C. dos, Neves, P. M. O. J., & Moscardi, F. (2016). Selectivity of organic compounds to the egg parasitoid Telenomus remus Nixon (Hymenoptera: Plastygastridae). Semina:Ciencias Agrárias, 37(1), 55-66. doi: 10.5433/1679-0359.2016v37n1p55
Song, J., Wang, X., Hou, D., Huang, H., Liu, X., Deng, F., Wang, H., Arif, B. M., Hu, Z., & Wang, M. (2016). The host specificities of baculovirus per os infectivity factors. PLoS ONE, 11(7), 1-12. doi: 10.1371/ journal.pone.0159862
Sosa-Gómez, D. R., Corrêa-Ferreira, B. S., Kraemer, B., Pasini, A., Husch, P. E., Vieira, C. E. D., Martinez, C. B. R., & Lopes, I. O. L. (2020). Prevalence, damage, management and insecticide resistance of stink bug populations (Hemiptera: Pentatomidae) in commodity crops. Agricultural and Forest Entomology, 22(2), 99-118. doi: 10.1111/afe.12366
Sosa-Gómez, D. R., & D’Alessandro, C. (2019). Hongos entomopatógenos del phylum Ascomycota. In C. C. López Lastra, & R. E. Lecuona (Eds.), Micopatología de artrópodos: hongos entomopatógenos para ser usados como bioinsumos en el control microbiano de plagas (pp. 47-78). Castelar, Buenos Aires.
Stacke, R. F., Godoy, D. N., Halberstadt, S. A., Bronzatto, E. S., Giacomelli, T., Hettwer, B. L., Guedes, J. V. C., & Bernardi, O. (2020). Inheritance of lambda-cyhalothrin resistance, fitness costs and cross-resistance to other pyrethroids in soybean looper, Chrysodeixis includens (Lepidoptera: Noctuidae). Crop Protection, 131(1), 1-8. doi: 10.1016/j.cropro.2020.105096
Stanley, J., & Preetha, G. (2016). Pesticide toxicity to non-target organisms: exposure, toxicity and risk assessment methodologies. In S. Johnson, & P. Gnanadhas (Eds.), Pesticide toxicity to non-target organisms (pp. 99-152). Dordrecht.
Stark, J. D., & Banks, J. E. (2003). Population-level effects of pesticides and other toxicants on arthropods. Annual Review of Entomology, 48(1), 505-519. doi: 10.1146/annurev.ento.48.091801.112621
Stein, C. P., & Parra, J. R. P. (1987). Uso da radiação ultra-violeta para inviabilizar ovos de Anagasta kuehniella (Zeller, 1879) visando estudos com Trichogramma spp. Anais da Sociedade Entomológica do Brasil, 16(1), 229-231. doi: 10.37486/0301-8059.v16i1.477
Takada, Y., Kawamura, S., & Tanaka, T. (2001). Effects of various insecticides on the development of the egg parasitoid Trichogramma dendrolimi (Hymenoptera: Trichogrammatidae). Journal of Economic Entomology, 94(6), 1340-1343. doi: 10.1603/0022-0493-94.6.1340
Torres, J. B., & Bueno, A. de F. (2018). Conservation biological control using selective insecticides - A valuable tool for IPM. Biological Control, 126(1), 53-64. doi: 10.1016/j.biocontrol.2018.07.012
Valicente, F. H., & Tuelher, E. D. E. S. (2009). Controle Biológico da lagarta do cartucho, Spodoptera frugiperda, com Baculovírus. (Circular Técnica). EMBRAPA Milho e Sorgo.
Van Lenteren, J. C. (2012). The state of commercial augmentative biological control: plenty of natural enemies, but a frustrating lack of uptake. BioControl, 57(1), 1-20. doi: 10.1007/s10526-011-9395-1
Van Lenteren, J. C., Bolckmans, K., Köhl, J., Ravensberg, W. J., & Urbaneja, A. (2018). Biological control using invertebrates and microorganisms: plenty of new opportunities. BioControl, 63(1), 39-59. doi: 10.10 07/s10526-017-9801-4
Vianna, U. R., Pratissoli, D., Zanuncio, J. C., Lima, E. R., Brunner, J., Pereira, F. F., & Serrão, J. E. (2009). Insecticide toxicity to Trichogramma pretiosum (Hymenoptera: Trichogrammatidae) females and effect on descendant generation. Ecotoxicology, 18(2), 180-186. doi: 10.1007/s10646-008-0270-5
Xu, Y. Y., Liu, T. X., Leibee, G. L., & Jones, W. A. (2004). Effects of selected insecticides on Diadegma insulare (Hymenoptera: Ichneumonidae), a parasitoid of Plutella xylostella (Lepidoptera: Plutellidae). Biocontrol Science and Technology, 14(7), 713-723. doi: 10.1080/09583150410001682395
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