Evaluation of the Effectiveness of Entomopathogens for the Control of Colorado Potato Beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae)

Document Type : Original Research

Authors
A. Eski 1
Z. Bayramoglu 2
E. Sonmez 3
S. Biryol 4
I. Demir 4
1 Bilecik Şeyh Edebali University, Vocational School, Program of Biomedical Equipment Technology, Bilecik, Turkey.
2 Recep Tayyip Erdoğan University, Pazar Vocational School, Program of Medicinal and Aromatic Plants, Rize, Turkey.
3 Düzce University, Beekeeping Research Development and Application Center, Düzce, Turkey.
4 Karadeniz Technical University, Faculty of Sciences, Department of Biology, Trabzon, Turkey.
Abstract
Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) damages potato, tomato, and eggplant, and is one of the most serious agricultural pests all over the world. Due to its resistance against chemical insecticides and some biopesticides, new biocontrol agents compatible with different ecological conditions are needed urgently for the integrated pest management programs of this pest. For this purpose, we studied the insecticidal effects of thirteen indigenous microbial isolates including entomopathogenic bacteria, fungi, and nematodes from our culture collection against L. decemlineata with screening and dose-response tests under laboratory conditions. Bacillus thuringiensis strain Xd3 caused 83% and 73% mortality against larvae and adults of the pest at 109 CFU mL-1 concentration within 10 days, respectively. While fungal isolate Metarhizium anisopliae Gg-12 yielded 98% mortality with 107 conidia mL-1 concentration on larvae at 15 days, mortality provided by Gg-12 on adults reached 100% at the same concentration and period. Steinernema websteri AS1 was determined as the most effective entomopathogenic nematode with 92% mortality within seven days on larvae. Based on probit analysis, the LC50 values of B. thuringiensis Xd3 against larvae and adults were calculated as, respectively, 1.73×106 and 1.69×107 CFU mL-1, and that of M. anisopliae Gg12 were 1.18×104 and 6.2×103 conidia mL-1, and that of S. websteri AS1 was 117 IJs mL-1. Considering these results, the biopesticides developed from these isolates can be used safely and successfully in the pest management control programs of Colorado potato beetle.

Keywords

Subjects

Abbott, W. S. 1925. A method of computing the effectiveness of an insecticide. J. Econ. Entomol., 18: 265–267.
Adel, M. M. and Hussein, H. M. 2010. Effectiveness of entomopathogenic nematodes Steinernema feltiae and Heterorhabditis bacteriophora on the Colorado potato beetle Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae) under laboratory and greenhouse conditions. Arch. Phytopathology Plant Protect., 43: 1485–1494.
Akhanaev, Y. B., Tomilova, O. G., Yaroslavtseva, O. N., Duisembekov, B. A., Kryukov, V. Y. and Glupov, V. V. 2017. Combined action of the entomopathogenic fungus Metarhizium robertsii and Avermectins on the larvae of the Colorado Potato Beetle Leptinotarsa decemlineata (Say) (Coleoptera, Chrysomelidae). Entomol. Rev., 97: 25–35.
Alyokhin, A. V. and Ferro, D. N. 1999. Relative fitness of Colorado potato beetle (Coleoptera: Chrysomelidae) resistant and susceptible to the Bacillus thuringiensis Cry3A toxin. J. Econ. Entomol., 92(3): 510-515.
Alyokhin, A., Baker, M., Mota-Sanchez, D., Dively, G. and Grafius, E. 2008. Colorado potato beetle resistance to insecticides. Am. J. Potato Res., 85: 395–413.
Anderson, T. E., Hajek, A. E., Roberts, D. W., Preisler, H. K. and Robertson, J. L. 1989. Colorado Potato Beetle (Coleoptera: Chrysomelidae): Effects of combinations of Beauveria bassiana with insecticides. J. Econ. Entomol., 82: 83–89.
Armer, C. A., Berry, R. E., Reed, G.L. and Jepsen, S. J. 2004. Colorado potato beetle control by application of the entomopathogenic nematode Heterorhabditis marelata and potato plant alkaloid manipulation. Entomol. Exp. Appl., 111: 47–58.
Batta, Y. 2003. Production and testing of novel formulations of the entomopathogenic fungus Metarhizium anisopliae (Metschinkoff) Sorokin (Deuteromycotina: Hyphomycetes). Crop. Prot., 22: 415–422.
Ben-Dov, E., Boussiba, S. and Zaritsky, A. 1995. Mosquito larvicidal activity of Escherichia coli with combinations of genes from Bacillus thuringiensis subsp. israelensis. J. Bacteriol., 177: 2851–2857.
Berry, R. E., Liu, J. and Reed, G. 1997. Comparison of endemic and exotic entomopathogenic nematode species for control of Colorado potato beetle (Coleoptera: Chrysomelidae). J. Econ. Entomol., 90: 1528–33.
Bruck, D. J. 2010. Fungal entomopathogens in the rhizosphere. BioControl, 55: 103–112.
Butt, T. M., Greenfield, B. P. J., Greig, C., Maffeis, T. G. G., Taylor, J. W. D., Piasecka, J., Dudley, E., Abdulla, A., Dubovskiy, I. M., Garrido-Jurado, I., et al. 2013. Metarhizium anisopliae pathogenesis of mosquito larvae: a verdict of accidental death. PLoS One, 8(12):e81686.
Çakıcı, F. Ö., Sevim, A., Demirbağ, Z. and Demir, İ. 2014. Investigating internal bacteria of Spodoptera littoralis (Boisd.) (Lepidoptera: Noctuidae) larvae and some Bacillus strains as biocontrol agents. Turk. J. Agric. For., 38: 99–110.
Demir, I., Sezen, K. and Demirbag, Z. 2002. The first study on bacterial flora and biological control agent of Anoplus roboris (Sufr., Coleoptera). J. Microbiol., 40: 104–108.
Duan, J. J., Head, G., Jensen, A. and Reed, G. 2004. Effects of transgenic Bacillus thuringiensis potato and conventional insecticides for Colorado potato beetle (Coleoptera: Chrysomelidae) management on the abundance of ground-dwelling arthropods in Oregon potato ecosystems. Environ. Entomol., 33: 275–281.
Ebrahimi, L., Niknam, G. and Lewis, E. E. 2011. Lethal and sublethal effects of Iranian isolates of Steinernema feltiae and Heterorhabditis bacteriophora on the Colorado potato beetle, Leptinotarsa decemlineata. BioControl, 56: 781–788.
Erbaş, Z., Gökçe, C., Hazir, S., Demirbağ, D. and Demir, İ. 2014. Isolation and identification of entomopathogenic nematodes (Nematoda: Rhabditida) from the Eastern Black Sea region and their biocontrol potential against Melolontha melolontha (Coleoptera: Scarabaeidae) larvae. Turk. J. Agric. For. 38: 187–197.
Erler, F. and Ates, A. O. 2015. Potential of two entomopathogenic fungi, Beauveria bassiana and Metarhizium anisopliae (Coleoptera: Scarabaeidae), as biological control agents against the June beetle. J. Insect Sci., 15(1): 44.
Eski, A., Demir, I., Sezen, K. and Demirbağ, Z. 2017. A new biopesticide from a local Bacillus thuringiensis var. tenebrionis (Xd3) against alder leaf beetle (Coleoptera: Chrysomelidae). World J. Microbiol. Biotechnol., 33(5): 95.
Ferro, D. N. and Gelernter, W. D. 1989. Toxicity of a new strain of Bacillus thuringiensis to Colorado potato beetle (Coleoptera: Chrysomelidae). J. Econ. Entomol., 82: 750–755.
Finney, D. J. 1971. Probit Analysis, Cambridge University Press. Wiley Subscription Services, Inc., A Wiley Company, London.
Gauthier, N., Hofmaster, R. and Semel, M. 1981. History of Colorado potato beetle control, pp. 13–33. Advances in Potato Pest Management, Hutchinson Ross Publishing Co., Stroudsburg,
Ghassemi-Kahrizeh, A. and Aramideh, S. 2015. Sub-lethal effects of Bacillus thuringiensis Berliner on larvae of Colorado potato beetle, Leptinotarsa decemlineata (Say) (Coleoptera: Chrysomelidae). Arch. Phytopathology and Plant Protect., 48: 259–267.
Gökçe, C., Erbaş, Z., Yılmaz, H., Demirbağ, Z. and Demir, İ. 2015. A new entomopathogenic nematode species from Turkey, Steinernema websteri (Rhabditida: Steinernematidae), and its virulence. Turk. J. Biol. 39: 167–174.
Guo, W., Yan, X., Zhao, G., Chen, J., Han, R. 2015. Efficacy of entomopathogenic Steinernema and Heterorhabditis nematodes against Holotrichia oblita. J. Pest. Sci., 88: 359–368.
Güven, Ö., Çayır, D., Baydar, R. ve Karaca, İ. 2015. Entomopatojen fungus Beauveria bassiana (Bals.) Vull. izolatlarının patates böceği [Leptinotarsa decemlineata Say. (Coleoptera: Chrysomelidae)] üzerindeki etkisi. Türk. Biyo. Mücadele Derg., 6(2): 107-116.
Haffani, Y. Z., Cloutier, C. and Belzile, F. J. 2001. Bacillus thuringiensis Cry3Ca1 protein is toxic to the Colorado potato beetle, Leptinotarsa decemlineata (Say). Biotechnol. Prog., 17: 211–216.
Harcourt, D. G. 1971. Population dynamics of Leptinotarsa decemlineata (say) in Eastern Ontario: III. Major population processes. Can. Entomol., 103: 1049–1061.
Hare, J. D. and Andreadis, T. G. 1983. Variation in the susceptibility of Leptinotarsa decemlineata (Coleoptera: Chrysomelidae) when reared on different host plants to the fungal pathogen, Beauveria bassiana in the field and laboratory. Environ. Entomol., 12(6): 1892-1897.
Hongyi, W., Ling, W. and Feng, L. 2000. Sensitivity of vegetable beetle, Colaphellus bowringi Baly to entomopathogenic nematoda, Steinernema carpocapsae. Acta Agric. Univ. Jiangxi., 22: 243–245.
Hussein, H. M., Habustova, O. S., Puza, V. and Zemek, R. 2016. Laboratory Evaluation of Isaria fumosorosea CCM 8367 and Steinernema feltiae Ustinov against Immature Stages of the Colorado Potato Beetle. PLoS ONE, 11(3): e0152399.
Kati, H., Sezen, K., Belduz, A. O. and Demirbağ, Z. 2005. Characterization of a Bacillus thuringiensis subsp. kurstaki strain isolated from Malacosoma neustria L. (Lepidoptera: Lasiocampidae). Biologia Bratisl., 60(3): 301–305.
Kaplan, E. L. & Meier, P. 1958. Nonparametric estimation from incomplete observations. J. Am. Stat. Assoc., 53(282): 457-481.
Kepenekçi, İ., Atay, T. and Alkan, M. 2016. Biological control potential of Turkish entomopathogenic nematodes against the Colorado potato beetle, Leptinotarsa decemlineata. Biocontrol Sci. Technol., 26(1): 141-144.
Kocacevik, S., Sevim, A., Eroglu, M., Demirbag, Z. and Demir, I. 2015. Molecular characterization, virulence and horizontal transmission of Beauveria pseudobassiana from Dendroctonus micans (Kug.) (Coleoptera: Curculionidae). J. Appl. Entomol., 139(5): 381–389.
Kryukov, V. Y., Khodyrev, V. P., Yaroslavtseva, O. N., Kamenova, A. S., Duisembekov, B. A. and
Glupov, V. V. 2009. Synergistic action of entomopathogenic Hyphomycetes and the bacteria Bacillus thuringiensis ssp. morrisoni in the infection of Colorado potato beetle Leptinotarsa decemlineata. Prikl. Biokhim. Mikrobiol., 45(5): 511–516.
Mascarin, G. M. and Jaronski, S. T. 2016. The production and uses of Beauveria bassiana as a microbial insecticide. World J. Microbiol. Biotechnol., 32(11): 177.
Öztürk, H.E., Güven, Ö, Karaca, İ. 2015. Effects of some bioinsecticides and entomopathogenic fungi on colorado potato beetle (Leptinotarsa decemlineata L.). Comm. Appl. Biol. Sci., 80(2): 205-211.
Patil, J., Rangasamy, V. and Lakshmi, L. 2017. Efficacy of entomopathogenic Heterorhabditis and Steinernema nematodes against the white grub, Leucopholis lepidophora Blanchard (Coleoptera: Scarabaeidae). Crop Protect., 101: 84–89.
Pérez, M. P., Sauka, D. H., Onco, M. I., Berretta, M. F. and Benintende, G. B. 2017. Selection of Bacillus thuringiensis strains toxic to cotton boll weevil (Anthonomus grandis, Coleoptera: Curculionidae) larvae. Rev. Argent. Microbiol., 49(3): 264–272.
Ropek, D. and Kolodziejczyk, M. 2019. Efficacy of selected insecticides and natural preparations against Leptinotarsa decemlineata. Potato Res., 62: 85-95.
Secil, E. S., Sevim, A., Demirbag, Z. and Demir, I. 2012. Isolation, characterization and virulence of bacteria from Ostrinia nubilalis (Lepidoptera: Pyralidae). Biologia Bratisl., 67(4): 767–776.
Sezen, K., Demir, I. and Demirbağ, Z. 2007. Identification and pathogenicity of entomopathogenic bacteria from common cockchafer, Melolontha melolontha (Coleoptera: Scarabaeidae). New Zeal. J. Crop. Hort., 35(1), 79–85.
Sezen, K. and Demirbag, Z. 1999. Isolation and insecticidal activity of some bacteria from the hazelnut beetle (Balaninus nucum L. [Curculionidae]). Appl. Entomol. Zool., 34: 85–89.
Sezen, K., Kati, H., Nalcacioĝlu, R., Muratoğlu, H. and Demirbağ, Z. 2008. Identification and pathogenicity of bacteria from European shot-hole borer, Xyleborus dispar Fabricius (Coleoptera: Scolytidae). Ann. Microbiol., 58(2): 173–179.
Shapiro-Ilan, D. I., Han, R. and Dolinksi, C. 2012. Entomopathogenic nematode production and application technology. J. Nematol., 44: 206–17.
Sönmez, E., Sevim, A., Demirbağ, Z. and Demir, İ. 2016. Isolation, characterization and virulence of entomopathogenic fungi from Gryllotalpa gryllotalpa (Orthoptera: Gryllotalpidae). Appl. Entomol. Zool., 51, 213–223.
Stewart, J. G., Boiteau, G. and Kimpinski, J. 1998. Management of late-season adults of the Colorado potato beetle (Coleoptera: Chrysomelidae) with entomopathogenic nematodes. Can. Entomol., 130: 509–514.
Tatar, D. M. 2008. Cloning, characterization and expression of cry3Aa gene of Bacillus thuringiensis Xd3. Unpublished master thesis, Karadeniz Technical University, Trabzon.
Teixeira, M. L. F. and Franco, A.A. 2007. Susceptibility of Cerotoma arcuata Olivier (Coleoptera: Chrysomelidae) larvae to Beauveria bassiana (Bals.) Vuillemin, Metarhizium anisopliae (Metsch.) Sorokin and Bacillus thuringiensis Berliner. Ciênc. Rural, 37: 19–25.
Toepfer, S., Gueldenzoph, C., Ehlers, R. U., Kuhlmann, U. 2005. Screening of entomopathogenic nematodes for virulence against the invasive western corn rootworm, Diabrotica virgifera (Coleoptera: Chrysomelidae) in Europe. Bull. Entomol. Res., 95(5): 473–482.
Trdan, S., Vidrih, M., Andjus, L. and Laznik, Z. 2009. Activity of four entomopathogenic nematode species against different developmental stages of Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera, Chrysomelidae). Helminthologia, 46(1): 14–20.
Tripathi, M. and Gujar, G. 2017. Formulation for optimizing Bacillus thuringiensis production, J. Biol. Control., 31(1): 38-49.
Unruh, T. R. and Lacey, L. A. 2001. Control of Codling Moth, Cydia pomonella (Lepidoptera: Tortricidae), with Steinernema carpocapsae: Effects of supplemental wetting and pupation site on infection rate. Biol. Control, 20(1): 48–56.
Vega, F. E., Goettel, M. S., Blackwell, M., Chandler, D., Jackson, M. A., Keller, S., Koike, M., Maniania, N. K., Monzon, A., Ownley, B. H., et al. 2009. Fungal entomopathogens: New insights on their ecology. Fungal Ecol., 2(4): 149–159.
Whalon, M. E., Miller, D. L., Hollingworth, R. M., Grafius, E. J., Miller, J. R. 1993. Selection of a Colorado potato beetle (Coleoptera: Chrysomelidae) strain resistant to Bacillus thuringiensis. J. Econ. Entomol., 86(2): 226-233.
White, G. F. 1927. A method for obtaining infective nematode larvae from cultures. Science, 66(1709): 302-303.
Wraight, S. P. P. and Ramos, M. E. E. 2005. Synergistic interaction between Beauveria bassiana and Bacillus thuringiensis tenebrionis-based biopesticides applied against field populations of Colorado potato beetle larvae. J. Invertebr. Pathol., 90(3): 139–150.
Yaroslavtseva, O. N., Dubovskiy, I. M., Khodyrev, V. P., Duisembekov, B. A., Kryukov, V. Y. and Glupov, V. V. 2017. Immunological mechanisms of synergy between fungus Metarhizium robertsii and bacteria Bacillus thuringiensis ssp. morrisoni on Colorado potato beetle larvae. J. Insect Physiol., 96: 14–20.
Zehnder, G. and Gelernter, W. 1989. Activity of the M-ONE Formulation of a new strain of Bacillus thuringiensis against the Colorado potato beetle (Coleoptera: Chrysomelidae): Relationship between susceptibility and insect life stage. J. Econ. Entomol., 82: 756–761.
Journal of Agricultural Science and Technology
Volume 24, Issue 2
March and April 2022
Pages 393-405