Abstract
A total of 27 entomopathogenic nematode (EPN) strains originally isolated from different cotton fields were characterized in laboratory experiments for their virulence, reproductive potential and environmental tolerance. The EPN strain collections included 16 Steinernema carpocapsae (SC), three Steinernema siamkayai (SS), one Steinernema monticolum (SM), and seven Heterorhabditis bacteriophora (HB). Their virulence was tested against cotton bollworms such as the American bollworm Helicoverpa armigera, the spotted bollworm Earias vittella and the cotton leafworm Spodoptera litura. Larvae of H. armigera, E. vittella and S. litura were susceptible to all the tested EPN species/strains with significant differences among EPN species/strains. The most virulent strains were APKS2 (SC), TRYH1 (HB) KKMH1 (HB) and KKMH2 (HB) on H. armigera (91.9–93.5% mortality); KKMS1 (SC), APKS2 (SC), TRYH1 (HB), KKMH1 (HB), KKMH2 (HB) and APKH1 (HB) on E. vittella (92.7% mortality); and APKS2, TRYH1, KKMH1, KKMH2 and KKMH3 on S. litura (92.7% mortality). The results of the invasion rate assay indicated that the EPN strains more virulent against the target host had greater invasion rates. In the multiplication assay, KKMH1and OCMS1 (SC) produced a greater number of infective juveniles (IJs) (32.1–32.4 x 1000 IJs/ cadaver) in Carcyra cephalonica. Test for tolerance to heat at 40°C for 2 h revealed that KKMH1, TRYH1, KKMH2, KKMS1 and APKS2 were highly tolerant (>85% survival). IJs exposed to ambient room conditions (27–29°C; 65–70% r.h.) for 2 h showed that APKS2, OCMS1 and KKMS1 were more tolerant (68–69% survival) of rapid desiccation than others. APKS2, KKMS1 and KKMH1 showed better survival (70–73%) in slow desiccation assay when exposed to 25°C with 97% r.h. for 72 h, followed by 25°C with 93% r.h. for 48 h. The H. bacteriophora KKMH1 and S. carpocapsae APKS2 performed best in nine traits out of ten tested, followed by H. bacteriophora TRYH1, which performed best for six traits. It is suggested that the EPN strains KKMH1 and APKS2 could be deployed for a cotton bollworm management program after testing their performance under field conditions.
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References
Abbott, W. S. (1925). A method of computing the effectiveness of an insecticide. Journal of Economic Entomology, 18, 265–267.
Adiroubane, D., Tamilselvi, R., & Ramesh, V. (2010). Efficacy of Steinernema siamkayai against certain crop pests. Journal of Biopesticides, 3, 180–185.
Baweja, V., & Sehgal, S. S. (1997). Potential of Heterorhabditis bacteriophora Poinar (Nematoda; Heterorhabditidae) in parasitizing Spodoptera litura (F.) in response to malathion treatment. Acta Parasitologica, 42, 68–172.
Boemare, N., Givaudan, A., Brehelin, M., & Laumond, C. (1997). Symbiosis and pathogenicity of nematode–bacterium complexes. Symbiosis, 22, 21–45.
Dhaliwal, G. S., Jindal, V., & Dhawan, A. K. (2010). Insect pest problems and crop losses: changing trends. Indian Journal of Ecology, 37, 1–7.
Dillon, A. B., Rolston, A. N., Meade, C. V., Downes, M. J., & Griffin, C. T. (2008). Establishment, persistence and introgression of entomopathogenic nematodes in a forest ecosystem. Ecological Applications, 18, 735–747.
Dowds, B. C. A., & Peters, A. (2002). Virulence mechanisms, pp. 79–98. In: R. Gaugler (Ed.) Entomopathogenic nematology. New York, NY: CABI.
Ehlers, R. U. (2001). Mass production of entomopathogenic nematodes for plant protection. Applied Microbiology and Biotechnology, 56, 623–633.
Ganguly, S., & Singh, L. K. (2000). Steinernema thermophilum (Rhabditida: Steinernematidae) from India. International Journal of Nematology, 10, 183–191.
Gaugler, R., Glazer, I., Campbell, J., & Liran, N. (1994). Laboratory and field evaluation of an entomopathogenic nematode genetically selected for host finding. Journal of Invertebrate Pathology, 63, 68–73.
Glazer, I. (2002). Survival biology, pp. 169–187. In: R. Gaugler (Ed.) Entomopathogenic nematology. New York, NY: CABI Publishing.
Glazer, I., Klein, A., Navon, A., & Nakache, Y. (1992). Comparison of efficacy of entomopathogenic nematodes combined with antidesiccants applied by canopy sprays against three cotton pests (Lepidoptera: Noctuidae). Journal of Economic Entomology, 85, 1636–1641.
Gouge, D. H., Lee, L. L., & Henneberry, T. J. (1999). Parasitism of diapausing pink bollworm Pectinophora gossypiella Lepidoptera: Gelechiidae) larvae by entomopathogenic nematodes (Nematoda: Steinernematidae, Heterorhabditidae). Crop Protection, 18, 531–537.
Gouge, D. H., Reaves, L. L., Stoltman, M. M., Van Berkum, J. R., Burke, R. A., Forlow Jech, L. J., et al. (1996). Control of pink bollworm Pectinophora gossypiella (Saunders) (Lepidoptera: Gelechiidae) larvae in Arizona and Texas cotton fields using the entomopathogenic nematode Steinernema riobrave (Rhabditida: Steinernematidae). Proceedings of the Beltwide Cotton Conference (Memphis, TN, USA), Vol. 2, pp. 1078-1082.
Gouge, D. H., & Shapiro-Ilan, D. I. (2003). Case studies in cotton and citrus: Use of entomopathogenic nematodes. Indian Journal of Nematology, 33, 91–102.
Gupta, M., Desai, P., & Pawar, A. D. (1987). The feasibility of using DD 136 strain of Neoaplectana carpocapsae Weiser for the control of insect pests. Plant Protection Bulletin, 39, 16–19.
Kary, N. E., Golizadeh, A., Dastjerdi, H. R., Mohammadi, D., Afghahi, S., Omrani, M., et al. (2012). A laboratory study of susceptibility of Helicoverpa armigera (Hübner) to three species of entomopathogenic nematodes. Munis Entomology & Zoology, 7(1), 372–379.
Kaya, H. K., & Stock, S. P. (1997). Techniques in insect nematology, pp. 281–324. In: L. A. Lacey (Ed.) Manual of techniques in insect pathology. San Diego, CA, USA: Academic Press.
Kim, H. H., Cho, S. R., Choo, H. Y., Lee, S. M., Jeon, H. Y., & Lee, D. W. (2008). Biological control of tobacco cutworm, Spodoptera litura (Lepidoptera: Noctuidae) by Steinernematid and Heterorhabditid entomopathogenic nematodes. Korean Journal of Applied Entomology, 47, 447–456.
Lewis, E. E. (2002). Behavioral ecology, pp. 205–224. In: R. Gaugler (Ed.) Entomopathogenic nematology. New York, NY: CABI.
Liu, A., & Glazer, I. (2000). Desiccation survival of entomopathogenic nematodes of the genus Heterorhabditis. Phytoparasitica, 28, 331–340.
Mracek, Z. (2003). Use of entomopathogenic nematodes (EPNs) in biological control, pp. 235–264. In: R. K. Upadhyay (Ed.) Advances in microbial control of insect pests. New York, NY: Kluwer Academic / Plenum Publishers.
Mukuka, J., Strauch, O., Hoppe, K., & Ehlers, R. (2010). Fitness of heat and desiccation tolerant hybrid strains of Heterorhabditis bacteriophora (Rhabditidomorpha: Heterorhabditidae). Journal of Pest Science, 83, 281–287.
Navon, A., Nagalakshmi, V. K., Levski, S., Salame, L., & Glazer, I. (2002). Effectiveness of entomopathogenic nematodes in an alginate gel formulation against lepidopterous pests. Biocontrol Science and Technology, 12, 737–746.
Patel, M. N., Stolinski, M., & Wright, D. J. (1997). Neutral lipids and the assessment of infectivity in entomopathogenic nematodes: observations on four Steinernema species. Parasitology, 114, 489–496.
Salame, L., Glazer, I., Miqaia, N., & Chkhubianishvili, T. (2010). Characterization of populations of entomopathogenic nematodes isolated at diverse sites across Israel. Phytoparasitica, 38, 39–52.
Seenivasan, N., Prabhu, S., Makesh, S., & Sivakumar, M. (2012). Natural occurrence of entomopathogenic nematode species (Rhabditida: Steinernematidae and Heterorhabditidae) in cotton fields of Tamil Nadu, India. Journal of Natural History, 46, 2829–2843.
Shahina, F., Anis, M., Maqbool, M. A., & Soomro, M. H. (1999). Mortality response of some insects by entomopathogenic nematode Steinernema BS266. Pakistan Journal of Nematology, 17, 125–128.
Shapiro, D. I., Glazer, I., & Segal, D. (1996). Trait stability and fitness of the heat tolerant entomopathogenic nematode Heterorhabditis bacteriophora IS5 strain. Biological Control, 6, 238–244.
Shapiro, D. I., Glazer, I., & Segal, D. (1997). Genetic improvement of heat tolerance in Heterorhabditis bacteriophora through hybridization. Biological Control, 8, 153–159.
Shapiro-Ilan, D. I., Stuart, R. J., & McCoy, C. W. (2003). Comparison of beneficial traits among strains of the entomopathogenic nematode, Steinernema carpocapsae, for control of Curculio caryae (Coleoptera: Curculionidae). Biological Control, 28, 129–136.
Singh, J., & Bardhan, A. K. (1974). Effectiveness of DD 136, an entomophilic nematode against insect pests of agricultural importance. Current Science, 43, 662.
Solomon, A., Paperna, I., & Glazer, I. (1999). Desiccation survival of the entomopathogenic nematode Steinernema feltiae: induction of anhydrobiosis. Nematology, 1, 61–68.
Strauch, O., Oestergaard, J., Hollmer, S., & Ehlers, R. U. (2004). Genetic improvement of the desiccation tolerance of the entomopathogenic nematode Heterorhabditis bacteriophora through selective breeding. Biological Control, 31, 218–226.
Tabashnik, B. E., & Carriere, Y. (2010). Field-evolved resistance to Bt cotton: Bollworm in the U.S. and pink bollworm in India. Southwestern Entomologist, 35, 417–424.
Wahab, S. (2009). Biotechnological approaches in the management of plant pests, diseases and weeds for sustainable agriculture. Journal of Biopesticides, 2, 115–134.
Walia, K. K., Bajaj, H. K., Walia, R. K., & Nandal, S. N. (2008). Host range, pathogenicity and foraging behaviour of Heterorhabditis indica, Steinernema asiaticum and Steinernema siamkayai strains indigenous to Haryana. Journal of Biological Control, 22, 7–12.
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The senior author is grateful to Life Science Research Board, Defense Research and Development Organization, New Delhi, India, for the financial support through a grant (No. DLS/81/48222/LSRB-136/FSB/2007).
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Seenivasan, N., Sivakumar, M. Screening for environmental stress-tolerant entomopathogenic nematodes virulent against cotton bollworms. Phytoparasitica 42, 165–177 (2014). https://doi.org/10.1007/s12600-013-0348-3
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DOI: https://doi.org/10.1007/s12600-013-0348-3