Hostname: page-component-cd9895bd7-lnqnp Total loading time: 0 Render date: 2024-12-27T07:53:13.891Z Has data issue: false hasContentIssue false
  • English
  • Français

Characterization of the pyrethroid resistance mechanisms in a Blattella germanica (Dictyoptera: Blattellidae) strain from Buenos Aires (Argentina)

Published online by Cambridge University Press:  07 July 2021

Emiliano Boné Open the ORCID record for Emiliano Boné [Opens in a new window] ,
Gonzalo Roca Acevedo ,
Marcos Sterkel ,
Sheila Ons ,
Paola González-Audino  and
Valeria Sfara
Emiliano Boné*
Affiliation:
Instituto de Investigación e Ingeniería Ambiental (IIIA), CONICET-UNSAM, Universidad Nacional de San Martín, San Martín, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
Gonzalo Roca Acevedo
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina Centro de Investigaciones de Plagas e Insecticidas (CIPEIN-UNIDEF-CITEDEF-CONICET), Buenos Aires, Argentina
Marcos Sterkel
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina Laboratorio de Neurobiología de Insectos, Centro Regional de Estudios Genómicos, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, Buenos Aires, Argentina
Sheila Ons
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina Laboratorio de Neurobiología de Insectos, Centro Regional de Estudios Genómicos, Facultad de Ciencias Exactas, Universidad Nacional de La Plata, Buenos Aires, Argentina
Paola González-Audino
Affiliation:
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina Centro de Investigaciones de Plagas e Insecticidas (CIPEIN-UNIDEF-CITEDEF-CONICET), Buenos Aires, Argentina
Valeria Sfara
Affiliation:
Instituto de Investigación e Ingeniería Ambiental (IIIA), CONICET-UNSAM, Universidad Nacional de San Martín, San Martín, Argentina Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Buenos Aires, Argentina
*
Author for correspondence: Emiliano Boné, Email: ebone@unsam.edu.ar
Get access Rights & Permissions [Opens in a new window]

Abstract

The use of chemical insecticides is the main control method for Blattella germanica worldwide. The prolonged and frequent use of insecticides produced the selection of insecticide-resistant individuals. The German cockroach is one of the most widespread urban pests in Argentina. In the last decades, resistance monitoring studies in this country demonstrated that there is a high prevalence of pyrethroid-resistant populations of B. germanica in the field. In this work, we studied the resistance mechanisms of a field-collected strain of B. germanica at toxicological, enzymatic, and molecular levels. A resistance ratio of 100 was obtained for the resistant strain when it was exposed to β-cypermethrin. The pretreatment with specific synergists (piperonyl butoxide and triphenyl phosphate) led to a significant increase in the toxicity of the pyrethroid, suggesting an involvement of oxidases and esterases in the detoxification of this insecticide. Moreover, esterase and oxidase activities in the resistant strain were 1.5-fold and 2-fold higher respectively, compared to the susceptible individuals. On the other hand, the voltage-gated sodium channel gene of the resistant cockroaches did not show nucleotidic substitutions in the domain II which are associated to knockdown resistance in this species. These results suggest that the main mechanism of resistance of the studied cockroaches' strain is metabolic, mainly due to an increase in the activity of oxidase and esterase enzymes. The results of this work in addition to other reports found in literature show that the extended use of a single active principle for cockroach control promotes the development of resistance leading to control failure in the field. In contrast, integrated pest management strategies include the use of different control tools in addition to chemical insecticides, which delay the appearance of resistance increasing the efficacy of pest control.

Keywords

Enzymatic activityGerman cockroachknockdown resistancepyrethroids
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 112 , Issue 1 , February 2022 , pp. 21 - 28
Check for updates
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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

Alzogaray, RA and Zerba, EN (2001) Third instar nymphs of Rhodnius prolixus exposed to α-cyano pyrethroids: from hyperactivity to death. Archives of Insect Biochemistry and Physiology: Published in Collaboration with the Entomological Society of America 46, 119–126.CrossRefGoogle Scholar
Anspaugh, DD, Rose, RL, Koehler, PG, Hodgson, E and Roe, RM (1994) Multiple mechanisms of pyrethroid resistance in the German cockroach, Blattella germanica (L.). Pesticide Biochemistry and Physiology, 50, 138–148.CrossRefGoogle Scholar
Brown, D, Zhang, L, Wen, Z and Scott, JG (2003) Induction of P450 monooxygenases in the German cockroach, Blattella germanica L. Archives of Insect Biochemistry and Physiology: Published in Collaboration with the Entomological Society of America 53, 119–124.CrossRefGoogle ScholarPubMed
Casida, JE (1970) Mixed-function oxidase involvement in the biochemistry of insecticide synergists. Journal of Agricultural and Food Chemistry 18, 753–772.CrossRefGoogle ScholarPubMed
Chen, N, Pei, XJ, Li, S, Fan, YL and Liu, TX (2020) Involvement of integument-rich CYP4G19 in hydrocarbon biosynthesis and cuticular penetration resistance in Blattella germanica (L.). Pest Management Science 76, 215–226.CrossRefGoogle Scholar
Cochran, DG (1989) Monitoring of insecticide resistance in field-collected strains of German cockroach. Journal of Economic Entomology 82, 336–341.CrossRefGoogle ScholarPubMed
Cornwell, PB (1968) The cockroach. Volume 1. A laboratory insect and an industrial pest.Google Scholar
Crespo, FA and Valverde, AC (2008) Orden Blattaria. In Claps, LR, Debandi, G and Juñet, R (eds), Biodiversidad de Artrópodos Argentinos, vol. 2. La Plata, Argentina: Sociedad Entomológica Argentina, pp. 167–179.Google Scholar
Desousa, G, Cuany, A, Brun, A, Amichot, M, Rahmani, R and Bergé, JB (1995) A microfluorometric method for measuring ethoxycoumarin-O-deethylase activity on individual Drosophila melanogaster abdomens: interest for screening resistance in insect populations. Analytical Biochemistry 229, 86–91.CrossRefGoogle Scholar
Dong, KE (1997) A single amino acid change in the para sodium channel protein is associated with knockdown-resistance (kdr) to pyrethroid insecticides in German cockroach. Insect Biochemistry and Molecular Biology 27, 93–100.CrossRefGoogle ScholarPubMed
Dong, K and Scott, JG (1991) Neuropharmacology and genetics of kdr-type resistance in the German cockroach, Blattella germanica (L.). Pesticide Biochemistry and Physiology 41, 159–169.CrossRefGoogle Scholar
Dong, K, Valles, SM, Scharf, ME, Zeichner, B and Bennett, GW (1998) The knockdown resistance (kdr) mutation in pyrethroid-resistant German cockroaches. Pesticide Biochemistry and Physiology 60, 195–204.CrossRefGoogle Scholar
Enayati, AA and Motevali, HF (2007) Biochemistry of pyrethroid resistance in German cockroach (Dictyoptera, Blatellidae) from hospitals of Sari, Iran. Iranian Biomedical Journal 11, 251–258.Google ScholarPubMed
Fardisi, M, Gondhalekar, AD and Scharf, ME (2017) Development of diagnostic insecticide concentrations and assessment of insecticide susceptibility in German cockroach (Dictyoptera: Blattellidae) field strains collected from public housing. Journal of Economic Entomology 110, 1210–1217.CrossRefGoogle ScholarPubMed
Fardisi, M, Gondhalekar, AD, Ashbrook, AR and Scharf, ME (2019) Rapid evolutionary responses to insecticide resistance management interventions by the German cockroach (Blattella germanica L.). Scientific Reports 9, 1–10.CrossRefGoogle Scholar
Fronza, G, Roca-Acevedo, G, Mougabure-Cueto, GA, Sierra, I, Capriotti, N and Toloza, AC (2020) Insecticide resistance mechanisms in Triatoma infestans (Reduviidae: Triatominae): the putative role of enhanced detoxification and knockdown resistance (kdr) allele in a resistant hotspot from the Argentine Chaco. Journal of Medical Entomology 57, 837–844.CrossRefGoogle Scholar
Hall, TA (1999) BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. In Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hemingway, J and Karunaratne, SH (1998) Mosquito carboxyl esterases: a review of the molecular biology and biochemistry of a major insecticide resistance mechanism. Medical and Veterinary Entomology 12, 1–12.CrossRefGoogle Scholar
Hemingway, J and Ranson, H (2000) Insecticide resistance in insect vectors of human disease. Annual Review of Entomology 45, 371–391.CrossRefGoogle ScholarPubMed
Hemingway, J, Dunbar, SJ, Monro, AG and Small, GJ (1993) Pyrethroid resistance in German cockroaches (Dictyoptera: Blattelidae): resistance levels and underlying mechanisms. Journal of Economic Entomology 86, 1931–1938.CrossRefGoogle ScholarPubMed
Hodgson, E and Levi, PE (1999) Interactions of piperonyl butoxide with cytochrome P450. In Jones, DG (ed.), Piperonyl Butoxide the Insecticide Synergist. London: Academic Press, pp. 41–53.CrossRefGoogle Scholar
Keller, JC, Clark, PH and Lofgren, CS (1956) Susceptibility of insecticide-resistant cockroaches to pyrethrins, I. Pest Control 24, 14–15.Google Scholar
Khan, MAQ and Matsumura, F (1972) Induction of mixed-function oxidase and protein synthesis by DDT and dieldrin in German and American cockroaches. Pesticide Biochemistry and Physiology 2, 236–243.CrossRefGoogle Scholar
Ladonni, H (1997) Susceptibility of different field strains of Blattella germanica to four pyrethroids (Orthoptera: Blattellidae). Iranian Journal of Public Health 26, 35–40.Google Scholar
Ladonni, H (2001) Evaluation of three methods for detecting permethrin resistance in adult and nymphal Blattella germanica (Dictyoptera: Blattellidae). Journal of economic entomology 94, 694–697.CrossRefGoogle Scholar
Limoee, M, Enayati, AA, Khassi, K, Salimi, M and Ladonni, H (2011) Insecticide resistance and synergism of three field-collected strains of the German cockroach Blattella germanica (L.) (Dictyoptera: Blattellidae) from hospitals in Kermanshah, Iran. Tropical Biomedicine 28, 111–118.Google ScholarPubMed
Liu, Z, Valles, SM and Dong, K (2000) Novel point mutations in the German cockroach para sodium channel gene are associated with knockdown resistance (kdr) to pyrethroid insecticides. Insect Biochemistry and Molecular Biology 30, 991–997.CrossRefGoogle Scholar
Mallis, K (1969) Handbook of Pest Control, 5th Edn. NY: MacNair-Dorland Co, pp. 1158.Google Scholar
Metcalf, RLA (1967) Mode of action of insecticide synergists. Annual Review of Entomology 12, 229–256.CrossRefGoogle ScholarPubMed
Miyazaki, M, Ohyama, K, Dunlap, DY and Matsumura, F (1996) Cloning and sequencing of the para-type sodium channel gene from susceptible and kdr-resistant German cockroaches (Blattella germanica) and house fly (Musca domestica). Molecular and General Genetics MGG 252, 61–68.Google Scholar
Narahashi, T (1996) Neuronal ion channels as the target sites of insecticides. Pharmacology & Toxicology 79, 1–14.CrossRefGoogle ScholarPubMed
Narahashi, T (2002) Nerve membrane ion channels as the target site of insecticides. Mini Reviews in Medicinal Chemistry 2, 419–432.CrossRefGoogle ScholarPubMed
Prabhakaran, SK and Kamble, ST (1993) Activity and electrophoretic characterization of esterases in insecticide-resistant and susceptible strains of German cockroach (Dictyoptera: Blattellidae). Journal of Economic Entomology 86, 1009–1013.CrossRefGoogle Scholar
Prabhakaran, SK and Kamble, ST (1994) Subcellular distribution and characterization of esterase isozymes from insecticide-resistant and-susceptible strains of German cockroach (Dictyoptera: Blattellidae). Journal of Economic Entomology 87, 541–545.CrossRefGoogle Scholar
Prabhakaran, SK and Kamble, ST (1995) Purification and characterization of an esterase isozyme from insecticide resistant and susceptible strains of German cockroach, Blattella germanica (L.). Insect Biochemistry and Molecular Biology 25, 519–524.CrossRefGoogle Scholar
Prevec, JS, Okoampah, ND and Morton, RA (1992) Organ phosphorus insecticide resistance in Drosophila melanogaster populations. Journal of Genetics 71, 121–134.CrossRefGoogle Scholar
Pridgeon, JW, Appel, AG, Moar, WJ and Liu, N (2002) Variability of resistance mechanisms in pyrethroid resistant German cockroaches (Dictyoptera: Blattellidae). Pesticide Biochemistry and Physiology 73, 149–156.CrossRefGoogle Scholar
Rehn, JAG (1945) Man's uninvited fellow traveler: the cockroach. The Scientific Monthly 61, 265–276.Google Scholar
Roca-Acevedo, G (2015) Análisis toxicológico, bioquímico y molecular de la resistencia a insecticidas en estados embrionarios y post-embrionarios de Triatoma infestans, vector de la enfermedad de Chagas (tesis doctoral). Universidad de Buenos Aires. Facultad de Farmacia y Bioquímica. [consultado: 13/4/2021] Disponible en el Repositorio Digital Institucional de la Universidad de Buenos Aires. Available at http://repositoriouba.sisbi.uba.ar/gsdl/collect/posgraafa/index/assoc/HWA_1135.dir/1135.PDF.Google Scholar
Roca-Acevedo, G, Picollo, MI, Capriotti, N, Sierra, I and Santo-Orihuela, PL (2015) Examining mechanism of pyrethroid resistance in eggs of two populations of the Chaga's disease vector Triatoma infestans (Hemiptera: Reduviidae). Journal of Medical Entomology 52, 987–1002.CrossRefGoogle Scholar
Russell, RM, Preisler, HK and Savin, NE (2007) Bioassays with arthropods. 2nd. Boca Ratón, Binary quantal response, Florida, USA: CRC Press. pp. 35–54.Google Scholar
Santo-Orihuela, Pablo L, Vassena, Claudia V, Zerba, Eduardo N, and Picollo, Maria I (2008) Relative contribution of monooxygenaseand esterase to pyrethroid resistance in Triatoma infestans(Hemiptera: Reduviidae) from Argentina and Bolivia. Journal of medical entomology, 45, 298–306.CrossRefGoogle Scholar
Santo-Orihuela, PL, Vassena, CV, Carvajal, G, Clark, E, Menacho, S, Bozo, R and Marcet, PL (2017) Toxicological, enzymatic, and molecular assessment of the insecticide susceptibility profile of Triatoma infestans (Hemiptera: Reduviidae, Triatominae) populations from rural communities of Santa Cruz, Bolivia. Journal of Medical Entomology 54, 187–195.CrossRefGoogle ScholarPubMed
Santo Orihuela, PL, Picollo, MI, Audino, PG, Barrios, S, Zerba, E and Masuh, H (2006) 7-Coumaryl permethrate and its cis and trans isomers as new fluorescent substrates for examining pyrethroid cleaving enzymes. Pest Management Science: formerly Pesticide Science 62, 1039–1044.CrossRefGoogle Scholar
Santo Orihuela, PL, Vassena, CV, Zerba, EN and Picollo, MI (2014) Relative contribution of monooxygenase and esterase to pyrethroid resistance in Triatoma infestans (Hemiptera: Reduviidae) from Argentina and Bolivia. Journal of Medical Entomology 45, 298–306.CrossRefGoogle Scholar
Scharf, ME, Neal, JJ, Marcus, CB and Bennett, GW (1998) Cytochrome P450 purification and immunological detection in an insecticide resistant strain of German cockroach (Blattella germanica, L.). Insect Biochemistry and Molecular Biology 28, 1–9.CrossRefGoogle Scholar
Schneider, CA, Rasband, WS and Eliceiri, KW (2012) NIH Image to Image J: 25 years of image analysis. Nature Methods 9, 671–675.CrossRefGoogle Scholar
Scott, JG (1990) Investigating mechanisms of insecticide resistance: methods, strategies, and pitfalls In Roush RT and Tabashink BE (eds), Pesticide Resistance in Arthropods, New York, Chapman & Hall, pp. 39–57.CrossRefGoogle Scholar
Soderlund, DM (2008) Pyrethroids, knockdown resistance and sodium channels. Pest Management Science: formerly Pesticide Science 64, 610–616.CrossRefGoogle ScholarPubMed
Soderlund, DM and Bloomquist, JR (1990) Molecular mechanisms of insecticide resistance. In Roush RT and Tabashink BE (eds), Pesticide Resistance in Artrhopods, New York, Chapman & Hall, pp. 58–96.Google Scholar
Tan, J, Liu, Z, Nomura, Y, Goldin, AL and Dong, K (2002) Alternative splicing of an insect sodium channel gene generates pharmacologically distinct sodium channels. Journal of Neuroscience 22, 5300–5309.CrossRefGoogle ScholarPubMed
Tang, Q, Bourguignon, T, Willenmse, L, De Coninck, E and Evans, T (2019) Global spread of the German cockroach, Blattella germanica. Biological Invasions 21, 693–707.CrossRefGoogle Scholar
Umeda, K, Yano, T and Hirano, M (1988) Pyrethroid-resistance mechanism in German cockroach, Blattella germanica (Orthoptera: Blattellidae). Applied Entomology and Zoology 23, 373–380.CrossRefGoogle Scholar
Valles, SM (1998) Toxicological and biochemical studies with field population of the German cockroach, Blattella germanica. Pesticide Biochemistry and Physiology 62, 190–200.CrossRefGoogle Scholar
Valles, SM and Yu, SJ (1996) Detection and biochemical characterization of insecticide resistance in the German cockroach (Dictyoptera Blattellidae). Journal of Economic Entomology 89, 21–26.CrossRefGoogle Scholar
Valles, SM, Dong, K and Brenner, RJ (2000) Mechanisms responsible for cypermethrin resistance in a strain of German cockroach, Blattella germanica (L.). Pesticide Biochemistry and Physiology 66, 195–205.CrossRefGoogle Scholar
Von Santos Veloso, R, Pereira, EJG, Guedes, RNC and Oliveira, MGA (2013) Does cypermethrin affect enzyme activity, respiration rate and walking behavior of the maize weevil (Sitophilus zeamais)? Insect Science 20, 358–366.CrossRefGoogle ScholarPubMed
Wei, Y, Appel, AG, Moar, WJ and Liu, N (2001) Pyrethroid resistance and cross-resistance in the German cockroach, Blattella germanica (L). Pest Management Science: formerly Pesticide Science 57, 1055–1059.CrossRefGoogle Scholar
Wu, X and Appel, AG (2017) Insecticide resistance of several field-collected German cockroach (Dictyoptera: Blattellidae) strains. Journal of Economic Entomology 110, 1203–1209.CrossRefGoogle ScholarPubMed
Wu, D, Scharf, ME, Neal, JJ, Suiter, DR and Bennett, GW (1998) Mechanisms of fenvalerate resistance in the German cockroach, Blattella germanica (L.). Pesticide Biochemistry and Physiology 61, 53–62, was added to reference list.CrossRefGoogle Scholar