Hostname: page-component-586b7cd67f-vdxz6 Total loading time: 0 Render date: 2024-11-24T23:09:05.008Z Has data issue: false hasContentIssue false

Behavioral response and adaptive cost in resistant and susceptible Plutella xylostella to Chlorantraniliprole

Published online by Cambridge University Press:  13 June 2019

D.A. Passos
Affiliation:
Departamento de Agronomia – Entomologia, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros, s/n, Dois Irmãos 52171-900, Recife – PE, Brazil
C.S.A. Silva-Torres*
Affiliation:
Departamento de Agronomia – Entomologia, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros, s/n, Dois Irmãos 52171-900, Recife – PE, Brazil
H.A.A. Siqueira
Affiliation:
Departamento de Agronomia – Entomologia, Universidade Federal Rural de Pernambuco, Rua Dom Manoel de Medeiros, s/n, Dois Irmãos 52171-900, Recife – PE, Brazil
*
*Author for correspondence Phone: +55 81 3320-6218 Fax: +55 81 3320-6214 E-mail: christian.silva@ufrpe.br

Abstract

Diamides have been used worldwide to manage the diamondback moth (DBM), Plutella xylostella L. (Lepidoptera: Plutellidae), however some strains showed resistance to these molecules. Also, pheromone traps could be used to manage this pest, hence reducing the use of insecticides in the field. Resistant DBM strains may have biological disadvantages in comparison to susceptible strains in areas without sprays, including reduction in fitness or behavioral changes. Therefore, the aim of this study was to investigate whether DBM strains resistant to chlorantraniliprole showed adaptive costs that could alter male attraction to the sex pheromone, in comparison to susceptible strains in the laboratory and semi-field conditions. First, the LC1, LC10, LC25, and LC50 of DBM to chlorantraniliprole were established, which were 0.003, 0.005, 0.007, and 0.011 mg a.i. liter−1, and 5.88, 24.80, 57.22, and 144.87 mg a.i. liter−1 for the susceptible and resistant strains, respectively. Development and reproduction of DBM strains subjected to those concentrations were compared. Later, male response to the sex pheromone was investigated in a Y-tube in the laboratory and in a greenhouse to pheromone traps. Resistant DBM strain showed an adaptive cost in comparison to the susceptible strain that can result in a delay in population growth in the field when selection pressure is absent. Conversely, resistant males have no olfactory response alteration in comparison to susceptible males, consistently at 3 (P = 0.6848) and 7 days (P = 0.9140) after release, suggesting that pheromone traps continue to be a viable alternative to manage DBM in an IPM system.

Type
Research Paper
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Abbott, W.S. (1925) A method of computing the effectiveness of an insecticide. Journal of Economic Entomology 18, 265266.Google Scholar
Arnaud, L. & Haubruge, E. (2002) Insecticide resistance enhances male reproductive success in a beetle. Evolution 56, 24352444.Google Scholar
Baker, P.B., Shelton, A.M. & Andaloro, J.T. (1982) Monitoring of diamondback moth (Lepidoptera: Yponomeutidae) in cabbage with pheromones. Journal of Economic Entomology 75, 10251028.Google Scholar
Barros, R., Albert-Junior, I.B., Oliveira, A.J., Souza, A.C. & Lopes, V. (1993) Controle químico da traçadas-crucíferas, Plutella xylostella (L.) (Lepidoptera: Plutellidae) em repolho. Anais da Sociedade Entomológica do Brasil 22, 463469.Google Scholar
Beukeboom, L.W. (2018) Size matters in insects – an introduction. Entomologia Experimentalis et Applicata 166, 23.Google Scholar
Cardoso, M.O., Pamplona, A.M.S.R. & Michereff Filho, M. (2010) Recomendações técnicas para o controle de lepidópteros pragas em couve e repolho no Amazonas. p.15. Manaus, EMBRAPA, Circular Técnica 35.Google Scholar
Castañeda, L.E., Barrientos, K., Cortes, P.A., Figueroa, C.C., Fuentes-Contreras, E., Luna-Rudloff, M., Silva, A.X. & Bacigalupe, L.D. (2011) Evaluating reproductive fitness and metabolic costs for insecticide resistance in Myzus persicae from Chile. Physiological Entomology 36, 253260.Google Scholar
Castelo-Branco, M., Villas-Boas, G.L. & Franca, F.H. (1996) Nível de dano de traça-das-crucíferas em repolho. Horticultura Brasileira 14, 154157.Google Scholar
Chow, Y.S., Lin, Y.M., Lee, N.S. & Teng, H.J. (1984) The disruption effect of the synthetic sex pheromone and its analogues on diamondback moth, Plutella xylostella L. in the field. Academia Sinica Institute of Zoology Bulletin 23, 119122.Google Scholar
Colares, F., Silva-Torres, C.S.A., Torres, J.B., Barros, E.M. & Pallini, A. (2013) Influence of cabbage resistance and col our upon the diamondback moth and its parasitoid Oomyzus sokolowskii. Entomololia Experimentalis et Applicata 148, 8493.Google Scholar
Coustau, C., Chevillon, C. & Ffrench-Constant, R. (2000) Resistance to xenobiotics and parasites: can we count the cost? Trends ecolology and Evolution 15, 378383.Google Scholar
Crow, J.F. (1957) Genetics of insect resistance to chemicals. Annual Review of Entomology 1, 227246.Google Scholar
Ferreira, E.S., Santos, A.R., Silva-Torres, C.S.A. & Torres, J.B. (2013) Life-history costs associated with resistance to lambda-cyhalothrin in the predatory ladybird beetle Eriopis connexa. Agriculture and Forest Entomology 15, 168177.Google Scholar
Finney, D.J. (1971) Probit Analysis. London, England, Cambridge University Press.Google Scholar
French-Constant, R.H. & Bass, C. (2017) Does resistance really carry a fitness cost? Current Opinion in Insect Science 21, 3946.Google Scholar
Furlong, M.J., Wright, D.J. & Dosdall, L.M. (2013) Diamondback mothecology and management: problems, progress, and prospects. Annual Review of Entomology 58, 517541.Google Scholar
Hallett, R.H., Angerilli, N.P.D. & Borden, J.H. (1995) Potential for a sticky trap monitoring system for the diamondback moth (Lepidoptera: Yponomeutidae) on cabbages in Indonesia. International Journal of Pest Management 41, 205207.Google Scholar
Han, W., Zhang, S., Shen, F., Liu, M., Ren, C. & Gao, X. (2012) Residual toxicity and sublethal effects of chlorantraniliprole on Plutella xylostella (lepidoptera: plutellidae). Pest Management Science 68, 11841190.Google Scholar
Hirooka, T., Nishimatsu, T., Kodama, H., Reckmann, U. & Nauen, R. (2007) The biological profile of flubendiamide, a new benzenedicarboxamide insecticide. Pflanzenschutz-Nachrichten Bayer 60, 183202.Google Scholar
Hollingsworth, R.G., Tabashnik, B.E., Johnson, M.W., Messing, R.H. & Ullman, D.E. (1997) Relationship between susceptibility to insecticides and fecundity across populations of cotton aphid (Homoptera: Aphididae). Journal of Economic Entomology 90, 5558.Google Scholar
Honek, A. (1993) Intraspecifi c variation in body size and fecundity in insects: a general relationship. Oikos 66, 483492.Google Scholar
Imenes, S.D.L., Campos, T.B., Rodrigues Netto, S.M. & Bergmann, E.C. (2002) Avaliação da atratividade de feromônio sexual sintético da traça das crucíferas, Plutella xylostella (L.) (Lepidoptera: Plutellidae), em cultivo orgânico de repolho. Arquivos do Instituto Biológico 69, 8184.Google Scholar
IRAC (2018) Arthropod pesticide resistance database. https://www.pesticideresistance.org/display.php?page=species&arId=571. Accessed 16 October 2018.Google Scholar
Jia, B., Liu, Y., Zhu, Y.C., Liu, X., Gao, C. & Shen, J. (2009) Inheritance, fitness cost and mechanism of resistance to tebufenozide in Spodoptera exigua (Hübner) (Lepidoptera: Noctuidae). Pest management science 65, 9961002.Google Scholar
Jiang, T., Wu, S., Yang, T., Zhu, C. & Gao, C. (2015) Monitoring field populations of Plutella xylostella (Lepidoptera: Plutellidae) for resistance to eight insecticides in China. Florida Entomologist 98, 6573.Google Scholar
Jutsum, A.R. & Gordon, R.F.S. (1989) Pheromones: importance to insects and role in pest management. pp. 116 in Jutsum, A.R. & Gordon, R.F.S. (Eds) Insect Pheromones in Plant Protection. New York, J. Wiley.Google Scholar
Kang, W.J., Koo, H.-N., Jeong, D.-H., Kim, H.K., Kim, J. & Kim, G.-H. (2017) Functional and genetic characteristics of chlorantraniliprole resistance in the diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Entomological Research 47, 394403.Google Scholar
Koshihara, P. (1986) Diamondback moth management. pp. 43–53 in Proceedings of the First International Workshop of Diamondback Moth Management, Asian Vegetable Research and Development Center. Shanhua, Taiwan.Google Scholar
LeOra Software (2005) POLO-Plus, POLO for Windows Computer Program, v. 2.0. Petaluma, CA, LeOra-Software.Google Scholar
Li, J., Guo, Q., Han, S. & Jiang, L. (2013) Types, morphologies and distributions of antennal sensilla of Quadrastichus erythrinae (Hymenptera: Eulophidae). Florida Entomologist 96, 12881297.Google Scholar
Maa, C.J.W. (1986) Ecological approach to male diamondback moth response to sex pheromone. pp. 109–123 in Proceedings of the First International Workshop of Diamondback Moth Management, Asian Vegetable Research and Development Center. Shanhua, Taiwan.Google Scholar
Magalhães, D.M., Borges, M., Laumann, R.A., Sujii, E.R., Mayon, P., Caulfield, J.C., Midega, C.A., Khan, Z.R., Pickett, J.A., Birkett, M.A., Blassioli-Moraes, M.C. (2012) Semiochemicals from herbivory induced cotton plants enhance the foraging behavior of the cotton boll weevil, Anthonomus grandis. Journal of Chemical Ecology 38, 15281538.Google Scholar
Martins, A.J., Bellinato, D.F., Peixoto, A.A., Valle, D. & Lima, J.B.P. (2012) Effect of insecticide resistance on development, longevity and reproduction of field or laboratory selected Aedes aegypti populations. PLoS ONE 7, e31889, doi.org/10.1371/journal.pone.0031889.Google Scholar
Matthews, R.W. & Matthews, J.R. (2010) Insect Behavior, 514p. London, Springer.Google Scholar
Michereff, M.F.F., Vilella, E.F., Michereff Filho, M. & Mafra-Neto, A. (2000) Uso Do feromônio sexual sintético para captura de machos da traça-das-crucíferas. Pesquisa Agropecuária Brasileira 35, 19191926.Google Scholar
Miluch, C.E., Dosdall, L.M. & Evenden, M.L. (2013) The potential for pheromone-based monitoring to predict larval populations of diamondback moth, Plutella xylostella (L.), in canola (Brassica napus L.). Crop Protection 45, 8997.Google Scholar
Miluch, C.E., Dosdall, L.M. & Evenden, M.L. (2014) Factors influencing male Plutella xylostella (Lepidoptera: Plutellidae) capture rates in sex pheromone-baited traps on canola in western Canada. Journal of Economic Entomology 107, 20672076.Google Scholar
Nauen, R. (2006) Insecticide mode of action: return of the ryanodine receptor. Pest Management Science 62, 690692.Google Scholar
Nauen, R. & Steinbach, D. (2016) Resistance to diamide insecticides in lepidopteran pests. pp. 219240 in Horowitz, A.R. & Ishaaya, I. (Eds) Advances in Insect Control and Resistance Management. Basel, Switzerland, Springer.Google Scholar
Onstad, D.W. (2014) Insect Resistance Management. Biology, Economics, and Prediction. 2nd edn. London, UK, Academic Press.Google Scholar
Paris, M., David, J.P. & Despres, L. (2011) Fitness costs of resistance to Bti toxins in the dengue vector Aedes aegypti. Ecotoxicology 20, 11841194.Google Scholar
Qi, S. & Casida, J.E. (2013) Species differences in chlorantraniliprole and flubendiamide insecticide binding sites in the ryanodine receptor. Pesticide Biochemistry and Physiology 107, 321326.Google Scholar
Qin, C., Wang, C., Wang, Y., Sun, S., Wang, H. & Xue, C. (2018) Resistance to diamide insecticides in Plutella xylostella (Lepidoptera: Plutellidae): comparison between lab-selected strains and field-collected populations. Journal of Economic Entomology 20, 17.Google Scholar
Ribeiro, L.M.S., Wanderley-Teixeira, V., Ferreira, H.N., Teixeira, A.A. & Siqueira, H.A. (2014) Fitness costs associated with field-evolved resistance to chlorantraniliprole in Plutella xylostella (Lepidoptera: Plutellidae). Bulletin of Entomological Research 104, 8896.Google Scholar
Ribeiro, L.M.S., Siqueira, H.A.A., Wanderley-Teixeira, V., Ferreira, H.N., Silva, W.M., Silva, J.E. & Teixeira, A.A.C. (2017) Field resistance of Brazilian Plutella xylostella to diamides is not metabolism-mediated. Crop Protection 93, 8288.Google Scholar
Robertson, J.L., Russell, R.M., Preisler, H.K. & Savin, N.E. (2007) Bioassays with Arthropods. Boca Raton, FL, CRC Press.Google Scholar
Roditakis, E., Vasakis, E., Grispou, M., Stavrakaki, M., Nauen, R., Gravouil, M. & Bassi, A. (2015) First report of Tuta absoluta resistance to diamide insecticides. Journal of Pest Science 88, 916.Google Scholar
Roush, R.T. & Mckenzie, J.A. (1987) Ecological genetics of insecticide and acaricide resistance. Annual Review of Entomology 32, 361380.Google Scholar
Saeed, S., Jaleel, W., Sarwar, Z.M., Naqqash, M.N., Saeed, Q., Zaka, S.M., Ishtiaq, Q.M., Qayyum, M.A., Sial, M.U., Ansari, M.J., Batool, M., Khan, K.A., Ghramh, H.A., Hafeez, M. & Sharma, G.K. (2018) Fitness parameters of Plutella xylostella (L.) (Lepidoptera; Plutellidae) at four constant temperatures by using age-stage, two-sex life tables. Saudi Journal of Biological Sciences, doi.org/10.1016/j.sjbs.2018.08.026.Google Scholar
Sanil, D. & Shetty, N.J. (2012) The effect of sublethal exposure to temephos and propoxur on reproductive fitness and its influence on circadian rhythms of pupation and adult emergence in Anopheles stephensi Liston-a malaria vector. Parasitology Research 111, 423432.Google Scholar
SAS Institute (2002) SAS/STAT 9.2, User's Guide. Cary, NC, USA, SAS Institute.Google Scholar
Shakeel, M., Farooq, M., Nasim, W., Akram, W., Khan, F.Z.A., Jaleel, W., Zhu, X., Yin, H., Li, S., Fahad, S., Hussain, S., Chauhan, B.S. & Jin, F. (2017) Environment polluting conventional chemical control compared to an environmentally friendly IPM approach for control of diamondback moth, Plutella xylostella (L.), in China: a review. Environmental Science and Pollution Research International 24, 1453714550.Google Scholar
Silva, J.E., Assis, C.P.O., Ribeiro, L.M.S. & Siqueira, H.A.A. (2016) Field-evolved resistance and cross-resistance of Brazilian Tuta absoluta (Lepidoptera: Gelechiidae) populations to diamide insecticides. Journal of Economic Entomology 109, 21902195.Google Scholar
Silva-Torres, C.S.A., Torres, J.B., Barros, R. & Pallini, A. (2010) Parasitismo de traça-das-cruciferas por Oomyzus sokolowskii. Pesquisa Agropecuária Brasileira 45, 638645.Google Scholar
Sparks, T.C. & Nauen, R. (2015) IRAC: mode of action classification and insecticide resistance management. Pesticide Biochemistry and Physiology 121, 122128.Google Scholar
Steinbach, D., Gutbrod, O., Lümmen, P., Matthiesen, S., Schorn, C. & Nauen, R. (2015) Geographic spread, genetics and functional characteristics of ryanodine receptor based target-site resistance to diamide insecticides in diamondback moth, Plutella xylostella. Insect Biochemistry and Molecular Biology 63, 1422.Google Scholar
Steinbach, D., Moritz, G. & Nauen, R. (2017) Fitness costs and life table parameters of highly insecticide-resistant strains of Plutella xylostella (L.) (Lepidoptera: Plutellidae) at different temperatures. Pest Management Science 73, 17891797.Google Scholar
Steinbrecht, R.A. (1996) Structure and function of insect olfactory sensilla. Ciba Foundation Symposium 200, 158174, discussion 174–177.Google Scholar
Sun, J., Liang, P. & Gao, X. (2012) Cross resistance patterns and fitness in fufenozide resistant diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae). Pest Management Science 68, 285289.Google Scholar
Tabashnik, B.E., Finson, N., Groeters, F.R., Moar, W.J., Johnson, M.W., Luo, K. & Adang, M.J. (1994) Reversal of resistance to Bacillus thuringiensis in Plutella xylostella. Proceeding of the National Academy of Science 91, 41204124.Google Scholar
Talekar, N.S. & Shelton, A.M. (1993) Biology, ecology and management of the diamondback moth. Annual Review of Entomology 38, 275301.Google Scholar
Tanaka, A., Horikiri, M., Takemura, K. & Matsumoto, K. (1990) Possibility of the application of synthetic sex pheromone in a small field against the diamondback moth, Plutella xylostella. Proceedings of the Association for Plant Protection of Kyushu 36, 139142.Google Scholar
Trimble, R.M., El-Sayed, A.M. & Pree, D.J. (2004) Impact of sub-lethal residues of azinphos-methyl on the pheromone-communication systems of insecticide-susceptible and insecticide-resistant obliquebanded leafrollers Choristoneura rosaceana (Lepidoptera: Tortricidae). Pest Management Science 60, 660668.Google Scholar
Troczka, B.J., Williamson, M.S., Field, L.M. & Davies, T.G.E. (2017) Rapid selection for resistance to diamide insecticides in Plutella xylostella via specific amino acid polymorphisms in the ryanodine receptor. Neurotoxicology 60, 224233.Google Scholar
Troczka, B., Zimmer, C.T., Elias, J., Schorn, C., Davies, G.E., Field, L.M., Williamson, M.S., Slater, R. & Nauen, R. (2012) Resistance to diamide insecticides in diamondback moth, Plutella xylostella (Lepidoptera: Plutellidae) is associated with a mutation in the membrane-spanning domain of the ryanodine receptor. Insect Biochemistry and Molecular Biology 42, 873880.Google Scholar
Uchiyama, T. & Ozawa, A. (2014) Rapid development of resistance to diamide insecticides in the smaller tea tortrix, Adoxophyes honmai (Lepidoptera: Tortricidae), in the tea fields of Shizuoka Prefecture, Japan. Applied Entomology and Zoology 49, 529534.Google Scholar
Wang, X.L. & Wu, Y.D. (2012) High levels of resistance to chlorantraniliprole evolved in field populations of Plutella xylostella. Journal of Economic Entomology 105, 10191023.Google Scholar
Wang, J., Wu, Y., Wang, X., Lansdell, S.J., Zhang, J. & Millar, N.S. (2016) A three amino acid deletion in the transmembrane domain of the nicotinic acetylcholine receptor α6 subunit confers high-level resistance to spinosad in Plutella xylostella. Insect Biochemistry and Molecular Biology 71, 2936.Google Scholar
Yamanda, H. & Koshihara, T. (1980) Flying time of diamondback moth, Plutella xylostella L., to light trap e sex pheromone trap. Japanese Journal of Applied Entomology and Zoology 24, 3032.Google Scholar
Yi, Z., Liu, D., Cui, X. & Shang, Z. (2016) Morphology and ultrastructure of antennal sensilla in male and female Agrilus mali (Coleoptera: Buprestidae). Journal of Insect Science 16, 116.Google Scholar
Yipeng, L., Liu, Y., Xingchuan, J. & Guirong, W. (2018) Cloning and functional characterization of three new pheromone receptors from the diamondback moth, Plutella xylostella. Journal of Insect Physiology 107, 1422.Google Scholar
Zilahi-Balogh, G.M.G., Angerilli, N.P.D., Borden, J.H., Meray, M., Tulung, M. & Sembel, D. (1995) Regional differences in pheromone response of diamondback moth in Indonesia. International Journal of Pest Management 41, 201204.Google Scholar