Individual and Combined Biological Effects of Bacillus thuringiensis and Multicapsid Nucleopolyhedrovirus on the Biological Stages of Egyptian Cotton Leafworm, Spodoptera littoralis (B.) (Lep.: Noctuidae)

Document Type : Original Research

Authors
1 Department of Plant Protection, Faculty of Agricultural Sciences, Fars Science and Research Branch, Islamic Azad University, Fars, Islamic Republic of Iran.
2 Department of Plant Protection, Faculty of Agricultural Sciences, Shiraz Branch, Islamic Azad University, Shiraz, Islamic Republic of Iran.
3 Iranian Research Institute of Plant Protection (IRIPP), Agricultural Research, Education and Extension Organization (AREEO), Tehran, Islamic Republic of Iran.
4 Department of Microbial Biotechnology and Biosaftey , Agricultural Biotechnology Research Institute of Iran (ABRII), Agricultural Research, Education and Extension Organization (AREEO), Karaj, Islamic Republic of Iran.
Abstract
The Egyptian cotton leafworm, Spodoptera littoralis (Boisduval) , is known as an important and highly polyphagous pest species worldwide. The objective of the present study was to evaluate synergistic effects of Bacillus thuringiensis subsp. kurstaki and NucleoPolyhedroVirus (SpliMNPV) on the 5-day-old larvae (2nd instars) of S. littoralis under laboratory conditions. To do this, the larvae of S. littoralis were fed on the treated artificial diet containing only one or combination of Bt (8.31×105, 2.78×107, 9.69×108 spore mL-1) and SpliMNPV (5.26×10, 7.03×102, 9.39×103 OB mL-1). According to the results, the mortality rate for most of the Bt-SpliMNPV combinations (different concentrations) was higher than that in the treatments containing only one of the studied biocontrol agents. The Bt-SpliMNPV combinations showed different types of interactions, including synergistic, additive, or antagonistic effects. The treatment containing 8.31×105 spore mL-1 of Bt and 5.26×10 OB mL-1 of the SpliMNPV was interpreted as synergism effect, as the real mortality (72.41±12.43%) was significantly more than the expected (48.28%). In addition, application of the Bt-SpliMNPV combinations could significantly increase larval and pupal periods, and reduce pupation, pupal weight and the adult emergence rate compared to the control and treatments containing only one of Bt or SpliMNPV. Finally, it could be concluded that co-application of Bt and SpliMNPV can enhance economic and efficient control of S. littoralis.

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Abbott, W. S. 1925. A method for computing the effectiveness of an insecticide. J. Econ. Entomol. 18, 265-267.
Alfazairy , A.A., El-Ahwany, A.M.D., Mohamed, E.A., Zaghloul, H.A.H. and El-Helow, E.R. 2013. Microbial control of the cotton leaf worm Spodoptera littoralis (Boisd.) by Egyption Bacillus thuringiensis isolates. Folia Microbiol. 58, 155-162.
Burges, H.D. and Thompson, E.M. 1971. Standardization and assay of microbial insecticides. In: Burges, H.D., Hussey, N.W. (eds.)., Microbial control of insects and mites. Academic., New York, p 709.
Chang, J.H., Choi, J.Y., Jin, B.R., Roh, J.K., Olszewski, J.A., Seo, S.J., O՚Reilly, D.R. and Je, Y.H. 2003. An improved baculovirus insecticide producing occlusing bodies that contains Bacillus thuringiensis insect toxin. J. Invertebr. Pathol. 84, 30-37.
Cook, S.P., Webb, R.E. and Thorpe, K.W. 1996. Potential enhancement of the gypsy moth (Lepiodoptera: Lymantriidae) nuclear polyhedrosis virus with triterpene azadirachtin. Biol. Control. 25(5), 1209-1214.
Duffield, S. and Jordan, S.L. 2000. Evaluation of insecticides for control of Helicoverpa armigera (Hübner) and Helicoverpa punctigera (Wallengren) (Lepidoptera: Noctuidae) on soybean, and the implications for field adoption. J. Aust. Entomol. Soci. 39, 322-327.
Duncan, D.B. 1955. Multiple range and multiple F tests. Biometrics. 11, l-42.
Duraimurugan, P., Regupathy, A. and Shanmugam, P. 2009. Effect of nucleopolyhedrovirus and Bacillus thuringiensis infection on the activity of insecticide detoxification enzyme in cotton bollworm, Helicoverpa armigera Hbn. Acta Phytopathol. Entomol. Ungarica. 44, 345-352.
Hatem, A.E., Aldebis, H.K. and Osuna, E.V. 2011. Effects of Spodoptera littoralis granulovirus on the development and reprpodution of cotton leafworm, S.littoralis. Biol. control. 59, 192-199.
Hatem, A.E., Reda, A.M. Amer and Vargas-Osuna, E. 2012a. Combination effects of Bacillus thuringiensis Cry1Ac toxin and nucleopolyhedrovirus or granulovirus of Spodoptera littoralis on cotton leafworm. Eypt J. Biol. Pest control. 22(2), 115-120.
Hatem, A.E., Faragalla, F.H. and Vargas-Osuna, E. 2012b. Combination effects of Spodoptera littoralis nuclear polyhedrosis and granulous virus against larvae of the cotton leafworm. World Rural Observations. 4(4): 10-16.
Hesketh, H. and Hails, R. 2008. The influence of Bacillus thuringiensis on Baculovirus transmission dynamics in the cabbage moth, Mamestra brassicae. [Speech]. In: Fortyoneth Annual General Meeting of the Society for Invertebrate Pathology and 9th International Conference on Bacillus thuringiensis (incorporating COST862 Action Bacterial Toxins for Insect Control), Warwick, UK, Soc. Invertebr. Pathol. 44.
Kalantari, M., Marzban, R., Imani, S. and Askari, H. 2013. Effect of Bacillus thuringiensis isolate and single nuclear polyhedrosis virus in combination and alone on Helicoverpa armigera. Arch. Phytopathology. Plant Prot.
http:// dx.doi.org/10.1080/03235408.2013.802460.
Khedr, M.A., Al-Shannaf, H.M., Mead, H.M. and Abd El-Aziz Shaker, Sh. 2015. Comparative study to determinefood consumption of cotton leafworm, Spodoptera littoralis, on some cotton genotypes. J. Plant Prot. Res. 55(3), 312-321.
Knaak, N. and Fiuza, L.M. 2005. Histopathology of Anticarsia gemmatalis Hübner (Lepidoptera: Noctuidae) treated with nucleopolyhedrovirus and Bacillus thuringiensis sorovar kurstaki. Braz. J. Microbiol. 36, 196-200.
Lacey, L.A., Frutos, R., Kaya, H.K. and Vail, P. 2001. Insect pathogens as biological control agents: do they have a future? Biol. Control. 21, 230-248.
Lacey, L. A., Grzywacz, D., Shapiro-Ilan, D. I., Frutos, R., Brownbridge, M. and Goettel, M. S. 2015. Insect pathogens as biological control agents: Back to the future. J. Invertebr. pathol. 132, 1-41.
Liu, X.X., Zhang, Q.W., Xu, B. and Li, J. 2006. Effects of Cry1Ac toxin of Bacillus thuringiensis and nuclear polyhedrosis virus of Helicoverpa armigera Hubner (Lepidoptera: Noctuidae) on larval mortality and pupation. Pest Manage. Sci. 62, 729-737.
Magholli, Z., Marzban, R., Abbasipour, H., Shikhi, A. and Karimi, J. 2013. Interaction effects of Bacillus thuringiensis subsp. kurstaki and single nuclear polyhedrosis virus on Plutella xylostella. J. Plant Dis. protect. 120(4), 173-178.
Magholi, Z., Abbasipour, H. and Marzban, R. 2014. Effect of Helicoverpa armigera Nucleopolyhedrosis Virus (HaNPV) on the larvae of the Diamondback Moth, Plutella xylostella (L.) (Lepidoptera: Plutellidae). Plant Prot. Sci. 4, 184-189.
Mahmoud, D.M., Abd El-Bar, M.M. and Abdul Aziz Radi, M.H. 2012. Combined effect local isolate Spodoptera littoralis nucleopolyhedrosis virus and Bacillus thuringiensis on Culex pipiens L. larvae (Culicidae: Diptera). J. Basic Appl. Zool. 65, 74-78.
Mansour, N.A., Eldefrawi, M.E., Toppozada, A. and Zeid, M. 1966. Toxicological studies on the Egyptian ctton leafworm, Prodenia litura V1 potentiation and antagonism of carbamate insecticide. J. Econ. Entomol. 59, 307-311.
Mansour, S.A., Foda, M.S. and Aly, A.R. 2012. Mosquitocidal activity of two Bacillus bacterial endotoxins combined with plant oila and conventional insecticides. Ind. Crops. Prod. 35, 44-52.
Marzban, R. 2002. Comparison bioassay of several native strains of Bt and kurstaki serotype on Plodia interpunctella. J. Pest. Plant Dis. 70, 29-36.
Marzban, R. and Salehi Jouzani, G. 2006. Isolation of native Bacillus thuringiensis Berliner isolates from the agricultural soils of Iran. J. New Agri. Sci. 1(2), 47-54.
Marzban, R., He, Q., Liu, X. and Zhang, Q. 2009. Effects of Bacillus thuringiensis toxin Cry1AC and cytoplasmic polyhedrosis virus of Helicoverpa armigera (Hübner) (HaCPV) on cotton bollworm (Lepidoptera: Noctuidae). J. Invertebr. Pathol. 101, 71-76.
Marzban, R. 2012. Midgut pH profile and energy differences in lipid, protein and glycogen metabolism of Bacillus thuringiensis Cry 1Ac and cypovirus-infected Helicoverpa armigera (Hübner) (Lepidoptera: Noctuidae). J. Entomol. Res. Soc. 14, 45-53.
Marzban R., Saberi F. and Shirazi M.M. 2016. Microfiltration and Ultrafiltration of Bacillus thuringiensis Fermentation broth: Membrane performance and spore-crystal recovery approaches. Braz. J. Chem. Eng. 33 (4), 783-791.
Masetti, A. DeLuigi, V. and Burgio, G. 2008. Effect of nucleopolyhedrovirus based product on Spodoptera littoralis. Bull. Insect. 61(2), 299-302.
Matter, M.M. and Zohy, N.M. 1981. Biotic efficiency of Bacillus thuringiensis Berl. and a nuclear-polyhedrosis virus on larvae of the american bollworm, Heliothis armigera Hbn. (Lep: Noctuidae). J. Appl. Entomol. 92, 336-343.
Mosallanejad, H. and Smagghe, G. 2009. Biochemical mechanisms of methoxyfenozide resistance in the cotton leafworm Spodoptera littoralis. Pest Manage. Sci. 65, 732-736.
Nouri-Ganbalani, G., Borzoui, E., Abdolmaleki, A., Abedi., Z. and Kamita, Sh. G. 2016. Individual and Combined Effects of Bacillus thuringiensis and Azadirachtin on Plodia interpunctella Hübner (Lepidoptera: Pyralidae). J. Insect Sci. 16(1): 95; 1-8.
Novan, A. 1985. Spodoptera littoralis. In: Singh, P. and Moore, R. F. (Eds.), Handbook of insect rearing. Elsivire., Amesterdam, pp. 469-475.
Qayyum, M.A., Wakil, W., Arif, M.J. and Sahi, Sh.T. 2015. Bacillus thuringiensis and Nuclear Polyhedrosis Virus for the Enhanced Bio-cotrol of Helicoverpa armigera. Int. J. Agric. Biol. 17(5), 1043-1048.
Robinson, G.S., Ackery., P.R., Kitching, I.J., Beccaloni, G.W. and Hernández, L.M. 2010. Hosts a database of the world Lepidopteran hostplants. Natural History Museum, London. http://www. nhm.ac.uk/hosts [ accessed on 14 January 2012].
Salama, H.S., Sharaby, A. and Eldin, M.M. 1993. Mode mof action of Bacillus thuringiensis and nuclear polyhedrosis virus in the larvae of Spodoptera littoralis (Boisd). Insect Sci. Appl. 14, 483-488.
Salehi Jouzani, G., Valijanian, E. and Sharafi, R. 2017. Bacillus thuringiensis: a successful insecticide with new environmental features and tidings. Appl. Microbiol. Biotechnol. 101(7), 2691-2711.
SAS Institute., 1999. SAS Online Doc®. Version 8. Cary, NC.
Seufi, A.M. 2008. Characterization of an Egyption Spodoptera littoralis nucleopolyhedrovirus and a possible use of a highly conserved region from polyhedrin gene for nucleopolyhedrovirus detection. J.Virol. 5-13.
Shaurub, E. H., El-Meguid, A. A. and El-Aziz, N. M. 2014. Effect of individual and combined treatment with Azadirachtin and Spodoptera littoralis Multicapsid Nucleopolyhedrovirus (SpliMNPV, Baculoviridae) on the Egyptian Cotton Leafworm Spodoptera littoralis (Boisduval) (Lepidoptera: Noctuidae). Ecol. Balk. 6(2), 93-100.
SPSS, 1998. SPSS User’s Guide. SPSS, Inc., Chicago, IL.
Theilmann, D.A., Blissard, G.W., Bonning, B., Jehle, J.A, O՚Reilly, D.R., Rohrmann, G.F., Thiem, S. and Valk, J.M. 2005. Baculoviridae. In virus Taxonomy. Classification and nomenclature of viruses. 8th report of the international committee on the taxonomy of viruses. In: Fauquet, C.X., Mayo, M.A., Maniloff, J., Desselberger, M. & Ball. L.A. (Eds.), Elsevier. Amesterdam, pp. 177-185
Toprak, U., Gurkan, M. O. and Bayram, S. 2007. Impact of a turkish isolate and a plaque-purified variant of SpliNPV-B on Larval stage development of Spodoptera lituralis (Lep: Noctuidae) Boisd . Pest Manage. Sci. 63, 564-568.
Ullah, L., Asif, M., Arslan, M. and Ashfaq, M. 2014. Temporal expression of Cry1Ab/c protein in Bt-cotton varieties, their efficacy against Helicoverpa armigera (Lepidoptera: Noctuidae) and population dynamics of suckingarthropods on them. Int. J. Agric. Biol. 16, 879-885.
Xiaoxia, L., Qingwen, Z., Baoliang, X. and Jianecheng, L. 2006. Effects of Cry1Ac toxin of Bacillus thuringiensis and nuclear polyhedrosis virus of Helicoverpa armigera (Hübner) (Lepidoptera:Noctuidae) on larval mortality and pupation . Pest Manag. Sci. 62, 729-737.