THE SUBLETHAL EFFECTS OF FIVE COMMERCIAL INSECTICIDES ON THE AMYLOLYTIC AND PROTEOLYTIC ACTIVITY OF THE BIOCONTROL AGENT, HABROBRACON HEBETOR SAY (HYMENOPTERA: BRACONIDAE)
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Dec 12, 2022
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Abstract
Habrobracon hebetor Say is an important biological control agent that has a wide range of lepidopteran hosts, especially from the Noctuidae and Pyralidae families. Nutrition is a very important element in the efficiency of natural enemies in integrated pest management (IPM). In the presented research, the sublethal effects of five selected chemical and botanical insecticides, fenvalerate, propargite, buprofezin, dayabon and palizin, on the activity of amylase and protease enzymes in the midgut of this important ectoparasitoid wasp were studied under laboratory conditions. Changes in the activity of enzymes were investigated by LC30 treatment of the female wasps, which were 0.14, 7.01, 3.04, 9.58 and 2.53 mg a.i./mL, respectively. The obtained results showed that this parasitoid wasp has a long midgut in its digestive tract. Also, there were significant differences among the enzymatic treatments (F5,12 =14.695 and 99.278) except protein concentration (F5,12 = 0.670). Regarding the amylase enzyme, the highest and lowest activities were obtained in the control and fenvalerate treatment (0.0435±0.0023 mU/mg vs. 0.0277±0.0010 mU/mg). In addition, the highest proteolytic activity was observed in the control (4.9817±0.0268 U/mg) and the lowest in the propargite treatment (3.2231±0.0917 U/mg). By closely investigating the results, dayabon and palizin showed the lowest negative effects on the enzymes and could be applied together with this parasitoid wasp in IPM designs.
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Asadi, M., Rafiee-Dastjerdi, H., Nouri-Ganbalani, G., Vahedi, H., Naseri, B., & Hassanpour, M. (2022). THE SUBLETHAL EFFECTS OF FIVE COMMERCIAL INSECTICIDES ON THE AMYLOLYTIC AND PROTEOLYTIC ACTIVITY OF THE BIOCONTROL AGENT, HABROBRACON HEBETOR SAY (HYMENOPTERA: BRACONIDAE). Acta Entomologica Serbica, 27(2), 55-65. https://doi.org/10.5281/zenodo.7427630
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Copyright: © 2019 The ENTOMOLOGICAL SOCIETY OF SERBIA Staff. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
References
Abedi, Z., Saber, M., Gharekhani, G., Mehrvar, A., & Kamita, S. G. (2014). Lethal and sublethal effects of azadirachtin and cypermethrin on Habrobracon hebetor (Hymenoptera: Braconidae). Journal of Economic Entomology, 107, 638-645.
Abedi, Z., Saber, M., Gharekhani, G., Mehrvar, A., & Mahdavi, V. (2012). Effects of azadirachtin, cypermethrin, methoxyfenozide and pyridalil on functional response of Habrobracon hebetor Say (Hymenoptera: Braconidae). Journal of Plant Protection Research, 52(3), 353-358.
Altuntas, H., & Kilic, A. (2010.) The effects of parasitism by the ectoparasitoid wasp Bracon hebetor Say (Hymenoptera: Braconidae) on host hemolymph proteins in the Mediterranean flour moth, Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Turkish Journal of Zoology, 34, 409-416.
Asadi, M., Rafiee-Dastjerdi, H., Nouri-Ganbalani, G., Naseri, B., & Hassanpour, M. (2018). The effects of plant essential oils on the functional response of Habrobracon hebetor Say (Hymenoptera: Braconidae) to its host. Invertebrate Survival Journal, 15, 169-182.
Asadi, M., Rafiee-Dastjerdi, H., Nouri-Ganbalani, G., Naseri, B., & Hassanpour, M. (2019). Insecticidal activity of the isolated essential oils from three medicinal plants on the biological control agent, Habrobracon hebetor Say (Hymenoptera: Braconidae). Acta Biologica Szegediensis, 63(1), 63-68.
Asadi, M., Nouri-Ganbalani, G., Rafiee-Dastjerdi, H., Hassanpour, M., & Naseri, B. (2020). Comparative study about the sublethal effects of chemical and botanical insecticides on the functional response of Habrobracon hebetor Say (Hym.: Braconidae) to larvae of Ephestia kuehniella Zeller (Lep.: Pyralidae). International Journal of Pest Management, 68(1), 80-88.
Asadi, M., Nouri-Ganbalani, G., Rafiee-Dastjerdi, H., Vahedi, H., Hassanpour, M., & Naseri, B. (2021). Effects of plant essential oils on the changes of digestive enzymes in the ectoparasitoid, Habrobracon hebetor Say, with description of its digestive tube. Arthropod-Plant Interactions, 15(6), 929-935.
Banks, J. E., & Stark, J. D. (1998). What is ecotoxicology? An ad-hoc grab bag or an interdisciplinary science? Integrative Biology, 1(5), 195-204.
Benham, G. S. (1972). Digestive and reproductive systems of Eriborus molestae Uchida (Hym.: Ichneumonidae). International Journal of Insect Morphology and Embryology, 1, 153-161.
Bernfeld, P. (1955). Amylases, a and b. Methods in Enzymology, 1, 149-154.
Borzoui, E., Naseri, B., & Mohammadzadeh-Bidarani, M. (2016). Adaptation of Habrobracon hebetor Say (Hymenoptera: Braconidae) rearing on Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) and Helicoverpa armigera Hübner (Lepidoptera: Noctuidae). Journal of Insect Science, 16, 1-7.
Bradford, M. A. (1976). Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248-254.
Croft, B. A. (1990). Arthropod biological control agents and pesticides. New York: John Wiley and Sons. 723 pp.
Dent, D. (1995). Integrated pest management. London: Chapman and Hall. 365 pp.
Desneux, N., Decourtye, A., & Delpuech, J. M. (2007). The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52, 81-106.
Elpidina, E. N., Vinokurov, K. S., Gromenko, V. A., Rudenshaya, Y. A., Dunaevsky, Y. E., & Zhuzhikov D. P. (2001). Compartmentalization of proteinases and amylases in Nauphoeta cinerea midgut. Archives of Insect Biochemistry and Physiology, 48, 206-216.
Faal-Mohammad Ali, H., Seraj, A. A., Talebi-Jahromi, Kh,. Shishebor, P., & Mosadegh. M. S. (2014). Effects of traditional insecticides on Habrobracon hebetor (Hymenoptera: Braconidae): bioassay and life-table assays. Archives of Phytopathology and Plant Protection, 47, 1089-1102.
Franco, O. L., Regden, D. J., Melo, F. R., & Grossi, M. F. (2000). Plant α amylase inhibitors and their interaction with insect α amylases; structure, function and potential for crop protection. European Journal of Biochemistry, 269, 397-412.
Galvan, T. L., Koch, R. L., & Hutchison, W. D. (2005). Effects of spinosad and indoxacarb on survival, development reproduction of the multicolored Asian lady beetle (Coleoptera: Coccinellidae). Biological Control, 34, 108-114.
Haseeb, M., Amano, H., & Liu, T. X. (2005). Effects of selected insecticides on Diadegma semiclausum (Hymenoptera: Ichneumonidae) and Oomyzus sokolowskii (Hymenoptera: Eulophidae), parasitoids of Plutella xylostella (Lepidoptera: Plutellidae). Insect Science, 12, 163-170.
Horie, Y., & Watanabe, H. (1980). Recent advances in sericulture. Annual Review of Entomology, 25, 49-71.
Jongsma, M. A., Bakker, P. L., Peters, J., Bosch, D., & Stiekema, W. J. (1995). Adaptation of Spodoptera exigua Hübner larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proceedings of National Academy of Sciences, 92, 8041-8045.
Keever, D. W., Arbogast, R. T. & Mullen, M. A. (1985). Population trends and distributions of Bracon hebetor Say (Hymenoptera: Braconidae) and lepidopterous pests in commercially stored peanuts. Environmental Entomology, 14, 722-725.
Magro, S. R., & Parra, J. R. P. (2001). Biologia do ectoparasitoide Bracon hebetor Say (Hymenoptera: Braconidae) em sete especies de lepidopteros. Science of Agriculture, 58, 693-698.
Mahdavi, V., & Saber, M. (2013). Functional response of Habrobracon hebetor Say (Hymenoptera: Braconidae) to Mediterranean flour moth (Anagasta Kuehniella Zeller) in response to pesticides. Journal of Economic Entomology, 53, 399-403.
Mahdavi, V. (2013). Residual toxicity of some pesticides on the larval ectoparasitoid Habrobracon hebetor Say (Hymenoptera: Braconidae). Journal of Plant Protection Research, 53, 27-32.
Maia, A. H. N., Alferdo, J. B. L., & Campanhola, C. (2000). Statistical inference on associated fecundity life table parameters using jackknife technique: computational aspects. Journal of Economic Entomology, 93, 511-518.
Meyer, J. S., Ingersoll, C. G., Mac Donald, L. L., & Boyce, M. S. (1986). Estimating uncertainty in population growth: jackknifes vs. bootstrap techniques. Ecology, 67, 1156-1166.
Parsia Aref, S., & Valizadegan, O. (2015). Fumigant toxicity and repellent effect of three Iranian eucalyptus species against the lesser grain beetle, Rhyzopertha dominica (F.) (Col.: Bostrychidae). Journal of Entomology and Zoology Studies, 3(2), 198-202.
Paust, A., Reichmuth, C., Büttner, C., Prozell, S., Adler, C. S., & Schöller, M. (2006). Spatial effects on competition between the larval parasitoids Habrobracon hebetor (Say) (Hymenoptera: Braconidae) and Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae) parasitising the Mediterranean flour moth, Ephestia kuehniella Zeller. 9th International working conference on stored product protection. Sao Paulo, Brazil, 7-17.
Rafiee-Dastjerdi, H., Hejazi, M. J., Nouri-Ganbalani, G., & Saber, M. (2008). Toxicity of some biorational and conventional insecticides to cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae) and its ectoparasitoid, Habrobracon hebetor Say (Hymenoptera: Braconidae). Journal of the Entomological Society of Iran, 28(1), 27-37.
Rafiee-Dastjerdi, H., Khorrami, F., Razmjou, J., Golizadeh, A., & Hassanpour, M. (2013). The efficacy of some medicinal plant extracts and essential oils against potato tuber moth, Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae). Journal of Crop Protection, 2, 93-99.
Razmjou, J., Mahdavi, V., Rafiee-Dastjerdi, H., Farhoomand, A., & Molapour, S. (2018). Insecticidal activities of some essential oils against larval ectoparasitoid, Habrobracon hebetor (Hymenoptera: Braconidae). Journal of Crop Protection, 7(2), 151-159.
Saadat, D., Bandani, A. R., & Dastranj. M. (2014). Comparison of the developmental time of Bracon hebetor Say (Hymenoptera: Braconidae) reared on five different lepidopteron host species and its relationship with digestive enzymes. European Journal of Entomology, 111, 495-500.
Slansky, F., & Scriber, J. (1981). The nutritional ecology of immature insects. Annual Review of Entomology, 26, 183-211.
Stroble, S., Maskos, K., Wiegand, G., Huber, R., Gomis-Ruth, F., & Glockshuber, R. (1998). A novel strategy for inhibition of α-amylase: yellow meal worm α-amylase in complex with Ragi bifunctional inhibitor at 2.5 resolutions. Structure, 6, 911-921.
Telang, M. A., Giri, A. P., Sainani, M. N., & Gupta, V. S. (2005). Characterization of two midgut proteinases of Helicoverpa armigera Hübner and their interaction with proteinase inhibitors. Journal of Insect Physiology, 51, 513-522.
Valencia, A., Arboleda, J. W., Lopez-Avila, A. & Grossi, M. F. (2008). Digestive α-amylases from Tecia solanivora (Povolny) larvae (Lepidoptera: Gelechiidae): response to pH, temperature and plant amylase inhibitors. Bulletin of Entomological Research, 98, 575-579.
Vinson, S. B. (1969). General morphology of the digestive and internal reproductive systems of adult Cardiochiles nigriceps (Hymenoptera: Braconidae). Annals of the Entomological Society of America, 62, 1414-1419.
Youm, O., & Gilstrap, F. E. (1993). Life-fertility tables of Bracon hebetor Say (Hymenoptera: Braconidae) reared on Heliocheilus albipunctella de Joannis (Lepidoptera: Noctuidae). Insect Science and its Applications, 14, 455-459.
Abedi, Z., Saber, M., Gharekhani, G., Mehrvar, A., & Mahdavi, V. (2012). Effects of azadirachtin, cypermethrin, methoxyfenozide and pyridalil on functional response of Habrobracon hebetor Say (Hymenoptera: Braconidae). Journal of Plant Protection Research, 52(3), 353-358.
Altuntas, H., & Kilic, A. (2010.) The effects of parasitism by the ectoparasitoid wasp Bracon hebetor Say (Hymenoptera: Braconidae) on host hemolymph proteins in the Mediterranean flour moth, Ephestia kuehniella Zeller (Lepidoptera: Pyralidae). Turkish Journal of Zoology, 34, 409-416.
Asadi, M., Rafiee-Dastjerdi, H., Nouri-Ganbalani, G., Naseri, B., & Hassanpour, M. (2018). The effects of plant essential oils on the functional response of Habrobracon hebetor Say (Hymenoptera: Braconidae) to its host. Invertebrate Survival Journal, 15, 169-182.
Asadi, M., Rafiee-Dastjerdi, H., Nouri-Ganbalani, G., Naseri, B., & Hassanpour, M. (2019). Insecticidal activity of the isolated essential oils from three medicinal plants on the biological control agent, Habrobracon hebetor Say (Hymenoptera: Braconidae). Acta Biologica Szegediensis, 63(1), 63-68.
Asadi, M., Nouri-Ganbalani, G., Rafiee-Dastjerdi, H., Hassanpour, M., & Naseri, B. (2020). Comparative study about the sublethal effects of chemical and botanical insecticides on the functional response of Habrobracon hebetor Say (Hym.: Braconidae) to larvae of Ephestia kuehniella Zeller (Lep.: Pyralidae). International Journal of Pest Management, 68(1), 80-88.
Asadi, M., Nouri-Ganbalani, G., Rafiee-Dastjerdi, H., Vahedi, H., Hassanpour, M., & Naseri, B. (2021). Effects of plant essential oils on the changes of digestive enzymes in the ectoparasitoid, Habrobracon hebetor Say, with description of its digestive tube. Arthropod-Plant Interactions, 15(6), 929-935.
Banks, J. E., & Stark, J. D. (1998). What is ecotoxicology? An ad-hoc grab bag or an interdisciplinary science? Integrative Biology, 1(5), 195-204.
Benham, G. S. (1972). Digestive and reproductive systems of Eriborus molestae Uchida (Hym.: Ichneumonidae). International Journal of Insect Morphology and Embryology, 1, 153-161.
Bernfeld, P. (1955). Amylases, a and b. Methods in Enzymology, 1, 149-154.
Borzoui, E., Naseri, B., & Mohammadzadeh-Bidarani, M. (2016). Adaptation of Habrobracon hebetor Say (Hymenoptera: Braconidae) rearing on Ephestia kuehniella Zeller (Lepidoptera: Pyralidae) and Helicoverpa armigera Hübner (Lepidoptera: Noctuidae). Journal of Insect Science, 16, 1-7.
Bradford, M. A. (1976). Rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248-254.
Croft, B. A. (1990). Arthropod biological control agents and pesticides. New York: John Wiley and Sons. 723 pp.
Dent, D. (1995). Integrated pest management. London: Chapman and Hall. 365 pp.
Desneux, N., Decourtye, A., & Delpuech, J. M. (2007). The sublethal effects of pesticides on beneficial arthropods. Annual Review of Entomology, 52, 81-106.
Elpidina, E. N., Vinokurov, K. S., Gromenko, V. A., Rudenshaya, Y. A., Dunaevsky, Y. E., & Zhuzhikov D. P. (2001). Compartmentalization of proteinases and amylases in Nauphoeta cinerea midgut. Archives of Insect Biochemistry and Physiology, 48, 206-216.
Faal-Mohammad Ali, H., Seraj, A. A., Talebi-Jahromi, Kh,. Shishebor, P., & Mosadegh. M. S. (2014). Effects of traditional insecticides on Habrobracon hebetor (Hymenoptera: Braconidae): bioassay and life-table assays. Archives of Phytopathology and Plant Protection, 47, 1089-1102.
Franco, O. L., Regden, D. J., Melo, F. R., & Grossi, M. F. (2000). Plant α amylase inhibitors and their interaction with insect α amylases; structure, function and potential for crop protection. European Journal of Biochemistry, 269, 397-412.
Galvan, T. L., Koch, R. L., & Hutchison, W. D. (2005). Effects of spinosad and indoxacarb on survival, development reproduction of the multicolored Asian lady beetle (Coleoptera: Coccinellidae). Biological Control, 34, 108-114.
Haseeb, M., Amano, H., & Liu, T. X. (2005). Effects of selected insecticides on Diadegma semiclausum (Hymenoptera: Ichneumonidae) and Oomyzus sokolowskii (Hymenoptera: Eulophidae), parasitoids of Plutella xylostella (Lepidoptera: Plutellidae). Insect Science, 12, 163-170.
Horie, Y., & Watanabe, H. (1980). Recent advances in sericulture. Annual Review of Entomology, 25, 49-71.
Jongsma, M. A., Bakker, P. L., Peters, J., Bosch, D., & Stiekema, W. J. (1995). Adaptation of Spodoptera exigua Hübner larvae to plant proteinase inhibitors by induction of gut proteinase activity insensitive to inhibition. Proceedings of National Academy of Sciences, 92, 8041-8045.
Keever, D. W., Arbogast, R. T. & Mullen, M. A. (1985). Population trends and distributions of Bracon hebetor Say (Hymenoptera: Braconidae) and lepidopterous pests in commercially stored peanuts. Environmental Entomology, 14, 722-725.
Magro, S. R., & Parra, J. R. P. (2001). Biologia do ectoparasitoide Bracon hebetor Say (Hymenoptera: Braconidae) em sete especies de lepidopteros. Science of Agriculture, 58, 693-698.
Mahdavi, V., & Saber, M. (2013). Functional response of Habrobracon hebetor Say (Hymenoptera: Braconidae) to Mediterranean flour moth (Anagasta Kuehniella Zeller) in response to pesticides. Journal of Economic Entomology, 53, 399-403.
Mahdavi, V. (2013). Residual toxicity of some pesticides on the larval ectoparasitoid Habrobracon hebetor Say (Hymenoptera: Braconidae). Journal of Plant Protection Research, 53, 27-32.
Maia, A. H. N., Alferdo, J. B. L., & Campanhola, C. (2000). Statistical inference on associated fecundity life table parameters using jackknife technique: computational aspects. Journal of Economic Entomology, 93, 511-518.
Meyer, J. S., Ingersoll, C. G., Mac Donald, L. L., & Boyce, M. S. (1986). Estimating uncertainty in population growth: jackknifes vs. bootstrap techniques. Ecology, 67, 1156-1166.
Parsia Aref, S., & Valizadegan, O. (2015). Fumigant toxicity and repellent effect of three Iranian eucalyptus species against the lesser grain beetle, Rhyzopertha dominica (F.) (Col.: Bostrychidae). Journal of Entomology and Zoology Studies, 3(2), 198-202.
Paust, A., Reichmuth, C., Büttner, C., Prozell, S., Adler, C. S., & Schöller, M. (2006). Spatial effects on competition between the larval parasitoids Habrobracon hebetor (Say) (Hymenoptera: Braconidae) and Venturia canescens (Gravenhorst) (Hymenoptera: Ichneumonidae) parasitising the Mediterranean flour moth, Ephestia kuehniella Zeller. 9th International working conference on stored product protection. Sao Paulo, Brazil, 7-17.
Rafiee-Dastjerdi, H., Hejazi, M. J., Nouri-Ganbalani, G., & Saber, M. (2008). Toxicity of some biorational and conventional insecticides to cotton bollworm, Helicoverpa armigera (Lepidoptera: Noctuidae) and its ectoparasitoid, Habrobracon hebetor Say (Hymenoptera: Braconidae). Journal of the Entomological Society of Iran, 28(1), 27-37.
Rafiee-Dastjerdi, H., Khorrami, F., Razmjou, J., Golizadeh, A., & Hassanpour, M. (2013). The efficacy of some medicinal plant extracts and essential oils against potato tuber moth, Phthorimaea operculella (Zeller) (Lepidoptera: Gelechiidae). Journal of Crop Protection, 2, 93-99.
Razmjou, J., Mahdavi, V., Rafiee-Dastjerdi, H., Farhoomand, A., & Molapour, S. (2018). Insecticidal activities of some essential oils against larval ectoparasitoid, Habrobracon hebetor (Hymenoptera: Braconidae). Journal of Crop Protection, 7(2), 151-159.
Saadat, D., Bandani, A. R., & Dastranj. M. (2014). Comparison of the developmental time of Bracon hebetor Say (Hymenoptera: Braconidae) reared on five different lepidopteron host species and its relationship with digestive enzymes. European Journal of Entomology, 111, 495-500.
Slansky, F., & Scriber, J. (1981). The nutritional ecology of immature insects. Annual Review of Entomology, 26, 183-211.
Stroble, S., Maskos, K., Wiegand, G., Huber, R., Gomis-Ruth, F., & Glockshuber, R. (1998). A novel strategy for inhibition of α-amylase: yellow meal worm α-amylase in complex with Ragi bifunctional inhibitor at 2.5 resolutions. Structure, 6, 911-921.
Telang, M. A., Giri, A. P., Sainani, M. N., & Gupta, V. S. (2005). Characterization of two midgut proteinases of Helicoverpa armigera Hübner and their interaction with proteinase inhibitors. Journal of Insect Physiology, 51, 513-522.
Valencia, A., Arboleda, J. W., Lopez-Avila, A. & Grossi, M. F. (2008). Digestive α-amylases from Tecia solanivora (Povolny) larvae (Lepidoptera: Gelechiidae): response to pH, temperature and plant amylase inhibitors. Bulletin of Entomological Research, 98, 575-579.
Vinson, S. B. (1969). General morphology of the digestive and internal reproductive systems of adult Cardiochiles nigriceps (Hymenoptera: Braconidae). Annals of the Entomological Society of America, 62, 1414-1419.
Youm, O., & Gilstrap, F. E. (1993). Life-fertility tables of Bracon hebetor Say (Hymenoptera: Braconidae) reared on Heliocheilus albipunctella de Joannis (Lepidoptera: Noctuidae). Insect Science and its Applications, 14, 455-459.