An overview of trends in pest management and the need for a paradigm shift in technologies for the progression of entomopathogenic nematodes in managing crop health

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Authors

  • ICAR-National Bureau of Agricultural Insect Resources (ICAR-NBAIR), Bengaluru – 560024, Karnataka ,IN
  • ICAR-National Bureau of Agricultural Insect Resources (ICAR-NBAIR), Bengaluru – 560024, Karnataka ,IN
  • CAR-National Bureau of Agricultural Insect Resources (ICAR-NBAIR), Bengaluru – 560024, Karnataka ,IN
  • CAR-National Bureau of Agricultural Insect Resources (ICAR-NBAIR), Bengaluru – 560024, Karnataka ,IN
  • CAR-National Bureau of Agricultural Insect Resources (ICAR-NBAIR), Bengaluru – 560024, Karnataka ,IN
  • CAR-National Bureau of Agricultural Insect Resources (ICAR-NBAIR), Bengaluru – 560024, Karnataka ,IN
  • CAR-National Bureau of Agricultural Insect Resources (ICAR-NBAIR), Bengaluru – 560024, Karnataka ,IN
  • CAR-National Bureau of Agricultural Insect Resources (ICAR-NBAIR), Bengaluru – 560024, Karnataka ,IN
  • CAR-National Bureau of Agricultural Insect Resources (ICAR-NBAIR), Bengaluru – 560024, Karnataka ,IN

DOI:

https://doi.org/10.18311/jbc/2024/36286

Keywords:

Biological control, entomopathogenic nematodes, innovations, paradigm shift, pest management

Abstract

Global pesticide usage is 3.5 million tonnes at an average of 1.81kg/ha, while Indian usage is at 55,000 metric tonnes (2023) with an average of 0.517kg/ha. Compared to the pesticide market, the Indian biopesticide market remains small- cumulative annual biopesticide production at 9000 metric tonnes and a growth rate of 3-5% in consumption which is projected to reach a CGR of 8-10% by 2030. The utilization of biopesticides amounts to approximately 9% of overall pesticide use and is projected to increase to 50% of the total pesticide market by 2050. Among several microbial biocontrol agents, Entomopathogenic Nematodes (EPN) has been realised to be dependable IPM component against several insect pests. EPNs are soil-inhabiting beneficial nematodes that parasitize and kill insect pests, with immense potential for ecological services making them valuable tools in IPM. Worldwide, the demand for the development of EPN-containing products is mounting with several companies involved in their production, distribution and sales. India’s estimated demand for EPN is 24,000 metric tonnes, while the current production is 1800 metric tonnes from 25-30 firms. In India and other developing countries, the current EPN production and supply chain are in their infancy and operate as a cottage industry. The market is flourishing with products that are spurious, expensive, and unregulated due to the wide gap between demand and availability of EPN products. The authors present an overview of the status and prospects of EPN as an IPM component, contemporary and futuristic issues for the transformation of the upcoming EPN industry to a self-reliant, self-sufficient and profitable enterprise and accomplish better uptake of EPN individually or in IPM.

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Published

2023-06-28

How to Cite

MANDADI, N., HUSSAINI, S. S., PATIL, J., AMALA, U., SREEDEVI, K., NAVIK, O., SUSHIL, S. N., MARUTHI, M., & BINDU SHREE, M. B. (2023). An overview of trends in pest management and the need for a paradigm shift in technologies for the progression of entomopathogenic nematodes in managing crop health. Journal of Biological Control, 38(2), 138–169. https://doi.org/10.18311/jbc/2024/36286

Issue

Section

Review Articles
Received 2024-01-17
Accepted 2024-03-21
Published 2023-06-28

 

References

Abe, Y. 1987. Culture of Steinernema feltiae (DD-136) on bran media. Japanese J Nematol, 17: 13-34.

Ansari, M.A., Abid Hussain and Moens, M. 2009. Formulation and application of entomopathogenic nematode-infected cadavers for control of Hoplia philanthus in turfgrass. Pest Manag Sci, 65: 367–374.

Banu, J. G., and Meena, K. S. 2015. Effect of different media and temperature on the multiplication and virulence of Heterorhabditis indica Poinar, Karunakar and David, 1992. Curr Biotechnol, 9(3): 239-246.

Bedding, R. A. 1981. Low-cost in vitro mass production of Neoaplectana and Heterorhabditis species (Nematoda) for field control of insect pests. Nematol, 27: 109-114. https://doi.org/10.1163/187529281X00115

Bedding, R. A. 1984. Large scale production, storage, and transport of the insect-parasitic nematode Neoaplectana spp. and Heterorhabditis spp. Ann Appl Biol, 104: 117-120. https://doi.org/10.1111/j.1744-7348.1984. tb05593.x

Bedding, R. A. 1988. Storage of entomopathogenic nematodes. Patent No. WO 88/08668.

Bedding, R. A., and Butler, K. L. 1994. Method for the storage of entomopathogenic nematodes. WIPO Patent No. WO 94/05150.

Bedding, R. A., Clark, S. D., Lacey, M. J., and Butler, K. L. 2000. Method and apparatus for the storage of entomopathogenic nematodes WIPO Patent No. WO 00/18887.

Biosys. 1993. Storage of nematodes in pseudoplastic layers. Patent No. AU2683692A.

Bouvier, J., Cuany, A., Monier, C., Brosse, V., and Sauphanor, B. 1998. Enzymatic diagnosis of resistance to deltamethrin in diapausing larvae of the codling moth, Cydia pomonella (L.). Arch. Insect Biochem Physiol Publ Collab Entomol Soc Am, 39: 55–64.

Broadbent, A. B., and Pree, D. J. 1997. Resistance to insecticides in populations of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae) from greenhouses in the Niagara region of Ontario. Can Entomol, 129: 907–913. https://doi.org/10.4039/ent129907-5.

Bruck, D.J., Shapiro-Ilan, D. I. and Lewis, E. E. 2005 Evaluation of application technologies of entomopathogenic nematodes for control of the black

Buecher, E. J., and Hansen, E. L. 1971. Mass culture of axenic nematodes using continuous aeration. J Nematol, 3: 199-200.

Byrne, F. J., and Devonshire, A. L. 1993. Insensitive acetylcholinesterase and esterase polymorphism in susceptible and resistant populations of the tobacco whitefly Bemisia tabaci (Genn.). Pestic. Biochem. Physiol., 45: 34–42. https://doi.org/10.1006/pest.1993.1005.

Capinera, J. L., and Hibbard, B. E. 1987. Bait formulations of chemical and microbial insecticides for suppression of crop-feeding grasshoppers. J Agril Entomol, 4: 337-344.

Chavarría‐Hernández, N., Maciel‐Vergara, G., Chavarría‐ Hernández, J. C., Castro‐Rosas, J., Rodríguez‐Pastrana, B. R., de la Torre‐Martínez, M., and Rodríguez‐ Hernández, A. I. 2011. Mass production of the entomopathogenic nematode, Steinernema carpocapsae CABA01, through the submerged monoxenic culture in two internal‐loop airlift bioreactors with some geometric differences. Biochem. Eng. J., 55(3), 145–153. https://doi.org/10.1016/j.bej.2011.03.011

Chen, S. and Glazer, I. 2005. A novel method for long-term storage of the entomopathogenic nematode Steinernema feltiae at room temperature. BioControl, 32: 104-110. https://doi.org/10.1016/j.biocontrol.2004.08.006

Cho, C. H., Whang, K. S., Gaugler, R., and Yoo, S. K. 2011. Submerged monoxenic culture medium development for Heterorhabditis bacteriophora and its symbiotic bacterium Photorhabdus luminescens: Protein sources. J Microbiol Biotechn, 21(8), 869-873. https://doi.org/10.4014/jmb.1010.10055 PMid:21876379.

Connick, Jr., W. J., Nickle, W. R. and Vinyard, B. J. 1993. “Pesta”:new granular formulations for steinernema carpocapsae. J. Nematol., 25: 198–203.

Cortés‐Martínez, C. I., and Chavarría‐Hernández, N. 2020. Production of entomopathogenic nematodes in submerged monoxenic culture: A Review. Biotechnol Bioeng, 117(12): 3968-3985. https://doi.org/10.1002/ bit.27515 PMid:32710642.

Cutright, C. R. 1954. A codling moth population resistant to DDT. J Econ Entomol, 47: 189–190. https://doi.org/10.1093/ jee/47.1.189.

Del Valle, E. E., Dolinksi, C., Barreto, E. L. S. and Souza, R. M. 2009. Effect of cadaver coatings on emergence and infectivity of the entomopathogenic nematode Heterorhabditis baujardi LPP7 (Rhabditida: Heterorhabditidae) and the removal of cadavers by ants. BioControl., 50: 21–24.

Dunn, M.D., Belur, P. & Malan, A.P. 2019. In vitro liquid culture and optimization of Steinernema jeffreyense, using shake flasks. BioControl 65: 223- 233. https://doi.org/10.1007/s10526-019-09977-7.

Dutky, S. R., Thompson, J. V., and Cantwell, G. E. 1964. A technique for the mass propagation of the DD-136 nematode. J. Ins Pathol., 6: 417-422.

Ehlers, R. U. 1994. Liquid culture production of entomopathogenic nematodes Heterorhabditis and Steinernema spp. Proceedings of Annual Meeting of the Society of Invertebrate Pathology, 27: 75-81. Biocontrol. 43:77-86.

Ehlers, RU. 1994. Liquid culture production of entomopathogenic nematodes Heterorhabditis and Steinernema spp. Proceedings of Annual Meeting of the Society of Invertebrate Pathology, 27:75-81.

Ehlers, R. U. 1996. Current and future use of nematodes in biocontrol: Practice and commercial aspects with regard to regulatory policy issues. Biocont Sci Technol, 6: 303- 316. https://doi.org/10.1080/09583159631299

Ehlers, R. U. 2001. Mass production of entomopathogenic nematodes for plant protection. Appl Micro Biotech, 56(5-6): 623-633. https://doi.org/10.1007/s002530100711 PMid:11601608.

Ehlers, R. U., Niemann, I., Hollmer, S., Strauch, O., Jende, D., Shanmugasundaram, M., … Burnell, A. 2000. Mass Production Potential of the Bacto- Helminthic Biocontrol Complex Heterorhabditis indica - Photorhabdus luminescens. Biocontrol Science and Technology, 10(5), 607–616. https://doi.org/10.1080/095831500750016406.

Ehlers, R. U., Lunau, S., Krasomil‐Osterfeld, K. and Osterfeld, K. H. 1998. Liquid culture of the entomopathogenic nematode‐bacterium‐ complex Heterorhabditis megidis/ Photorhabdus luminescens. BioControl, 43: 77–86. https://doi.org/10.1023/A:1009965922794.

Ehlers, R. U., Osterfeld, K. H., Krasomil-Osterfeld, K., and Lunau, S. 1992. In vitro reproduction of Heterorhabditis megidis (strain HSH) in laboratory scale bioreactors. Proceedings of Annual Meeting of the Society of Invertebrate Pathology, 25: 100.

Ehlers, R. U., and Shapiro-Ilan, D. I. 2005. Mass production. In. Grewal PS, Ehlers R, Shapiro-Ilan DI (eds), Nematodes as biological control agents. Cambridge, MA: CABI Publishing. pp. 65-78. https://doi.org/10.1079/9780851990170.0065

Espinosa, P. J., Bielza, P., Contreras, J., and Lacasa, A. 2002. Insecticide resistance in field populations of Frankliniella occidentalis (Pergande) in Murcia (southeast Spain). Pest Manag Sci, 58: 967–971. https://doi.org/10.1002/ps.572

Shahina, F., Tabassum, A. K. and Manzoor H. S. 2011. Storage of entomopathogenic nematodes. US 2011/0197289 A1.

Ferreira, T. 2013. Characterisation of nematode symbiotic bacteria and the in vitro liquid culture of Heterorhabditis zealandica and Steinernema yirgalemense [Unpublished doctoral dissertation, University of Stellenbosch]. https://scholar.sun.ac.za/handle/10019.1/80294

Ferreira, T., Addison, M.F. and Malan, A.P. 2016. Development and population dynamics of Steinernema yirgalemense and growth characteristics of its associated Xenorhabdus symbiont in liquid culture. J Helminthol, 90: 364-71.

Ferreira, T., and Malan, A. P. 2014. Potential of entomopathogenic nematodes for the control of the banded fruit weevil, Phlyctinus callosus (Schönherr) (Coleoptera: Curculionidae). J Helminthol, 88(3): 293- 301.

FiBL Survey 2023. https://statistics.fibl.org/data.html

Fife, J. P., Decksen, R. C., Ozkan, H. E., and Grewal, P. S. 2003. Effects of pressure differentials on the viability and infectivity of entomopathogenic nematodes. BioControl., 27: 65-72. https://doi.org/10.1016/S1049-9644(02)00183-4

Finney, R., and Jean. 1981. Package for the transportation of nematodes. CA1165694A.USPTO.

Flanders, K. L., Miller, J. M., and Shields. E. J. 1996. In vivo production of Heterorhabditis bacteriophora ‘Oswego’ (Rhabditida: Heterorhabditidae), a potential biological control agent for soil-inhabiting insects in temperate regions. J Econ Entomol, 89: 373-380. https://doi. org/10.1093/jee/89.2.373

Friedman, M. J., Gaugler, R., and Kaya, H. K. 1990. Commercial production and development. In: Gaugler R, Kaya HK (eds), Entomopathogenic nematodes in biological control (pp. 153-172). CRC Press, Boca Raton, FL.

Friedman, M. J., Langston, S. L., and Pollit, S. 1989. Mass production in liquid culture of insect-killing nematodes. International Patent WO89/04602.

Garcia, L. C., Raetano, C. G., Wilcken S. R. S., Ramos, H. H., Leite, L. G., Filho, A. B., and Moscardi, F. 2005. Pressurização da calda de pulverização na viabilidade de microrganismos entomopatogênicos. Engenharia Agrícola, 25: 783-790. https://doi.org/10.1590/S0100- 69162005000300025.

Gaugler, R and Brown, I. 2001. LOTEK: an automated apparatus for production of insecticidal nematodes USSN 09/845, 816.

Gaugler, R., and Han, R. 2002. Production technology. In: Gaugler R (ed). Entomopathogenic nematology (pp. 289-310). CABI, Wallingford, UK. https://doi. org/10.1079/9780851995670.0289

Gaugler, R., Brown, I., Shapiro-Ilan, D. I., and Atwa, A. 2002. Automated technology for in vivo mass production of entomopathogenic nematodes. BioControl., 24: 199- 206. https://doi.org/10.1016/S1049-9644(02)00015-4

Georghiou, G. P. 1986. The magnitude of the resistance problem. Pesticide resistance: Strategies and tactics for management (pp.14-43). National Academy Press, Washington, D.C.

Georgis, R. 1990. Formulation and application technology. In: Gaugler R, Kaya HK (eds). Entomopathogenic nematodes in biological control (pp. 173-191). CRC Press, Boca Raton, Florida. https://doi. org/10.1201/9781351071741-12

Georgis, R. 1992. Present and future prospects for entomopathogenic nematode products. Biocontrol Sci Techn, 2(2): 83-99. https://doi. org/10.1080/09583159209355222

Georgis, R., Koppenhofer, A. M., Lacey, L. A., Belair, G., Duncan, L. W., Grewal, P. S., Samish, M., Tan, L., Torr, P., and Van Tol, R. W. H. M. 2006. Successes and failures in the use of parasitic nematodes for pest control. BioControl., 38: 103-123. https://doi.org/10.1016/j. biocontrol.2005.11.005

Gil, G., Choo, H., and Gaugler, R. 2002. Enhancement of entomopathogenic nematode production in in-vitro liquid culture of Heterorhabditis bacteriophora by fed-batch culture with glucose supplementation. Appl Microbiol Biotechnol, 58(6): 751-755. https://doi. org/10.1007/s00253-002-0956-1 PMid:12021794

Gitanjali, D. 2018. Mass production of entomopathogenic nematodes - A review. Int J Env Agric Biotechnol, 3(3): 1032-1043. https://doi.org/10.22161/ijeab/3.3.41

Glaser, R. W. 1932. Studies on Neoaplectana glaseri, a nematode parasite of the Japanese beetle (Popillia japonica). New Jersey Dep Agric Cir, 211: 3-34.

Glaser, R. W., and Farrell, C. C. 1935. Field experiments with the Japanese beetle and its nematode parasite. J New York Ent Soc, 43: 345-371.

Glazer I, Salame L, Segal D. 1997. Genetic enhancement of nematicide resistance in entomopathogenic nematodes. Biocontrol Sci. Technol. 7: 499–512.

Goud, S., Hugar P. S. and Prabhuraj. A. 2010. Effect of temperature, population density and shelf life of EPN Heterorhabditis indica (RCR) in sodium alginate gel formulation. J Biopesticides, 3(3): 627 – 632.

Götte, E., and Rybak, M. 2011. Pest control of the Western flower thrips Frankliniella occidentalis (Pergande) with proven insecticide resistance in cut flowers in greenhouses. Gesunde Pflanz. 62, 117–123. https://doi. org/10.1007/s10343-010-0229-3.

Grewal, P. S. 2000. Enhanced ambient storage stability of an entomopathogenic nematode through anhydrobiosis. Pest Manag Sci, 56 (5): 401-406.

Grewal, P. S. 2000a. Anhydrobiotic potential and long-term storage of entomopathogenic nematodes (Rhabditida: Steinernematidae). Interntl J Parasitol, 30: 995–1000.

Grewal, P. S. 2000b. Enhanced ambient storage stability of an entomopathogenic nematode through anhydrobiosis. Pest Manag Sci, 56: 401–40.

Grewal, P. S. 2002. Formulation and application technology. Pp. 265–288 In R. Gaugler, ed. Entomopathogenic Nematology. Wallingford, UK: CABI Publishing.

Grewal, P. S., and Georgis, R. 1999. Entomopathogenic nematodes. In: Hall FR, Menn JJ (eds). Methods in biotechnology, vol. 5: Biopesticides: Use and delivery (pp. 271-299). Totowa, NJ, Humana Press. https://doi. org/10.1385/0-89603-515-8:271

Grewal, P. S., Bornstein-Forst, S., Burnell, A. M., Glazer, I., and Jagdale, G. B. 2006. Physiological, genetic, and molecular mechanisms of chemoreception, thermobiosis, and anhydrobiosis in entomopathogenic nematodes. BioControl, 38: 54-65. https://doi. org/10.1016/j.biocontrol.2005.09.004

Guangdong Entomological Institute (GSI). 2001. Storing method of entomopathogenic nematode. Patent No. CN1335061A.

Gumus, A., Karagoz, M., Shapiro-Ilan, D., and Hazir, S. 2015. A novel approach to biocontrol: Release of live insect hosts pre-infected with entomopathogenic nematodes. J Inv Pathol, 130: 56-60. https://doi.org/10.1016/j. jip.2015.07.002 PMid:26149819.

Gutiérrez-Moreno, R., Mota-Sanchez, D., Blanco, C. A., Whalon, M. E., Terán Santofimio, H., Rodriguez- Maciel, J. C., et al. 2019. Field-evolved resistance of the fall armyworm (Lepidoptera: Noctuidae) to synthetic insecticides in Puerto Rico and Mexico. J Econ Entomol, 112: 792–802. https://doi.org/10.1093/jee/toy372.

Han, R., Cao, L., and Liu, X. 1992. Relationship between medium composition, inoculums size, temperature and culture time in the yields of Steinernema and Heterorhabditis nematodes. Fundamental Applied Nematol, 15: 223-229.

Han R, Cao L, Liu X. 1993. Effects of inoculum size, temperature, and time on in vitro production of Steinernema carpocapsae Agriotis. Nematologica, 39: 366–375.

Han, R., Pang, X. and Li, L. 1995. Optimization of the medium components for the solid culture of entomopathogenic Steinernema and Heterorhabditis nematodes. Natural Enemies of Insects. 17:153–164.

Hara, A. H., Lindegren, J. E., and Kaya, H. K. 1981. Monoxenic mass production of the entomogenous nematode Neoplectana carpocapsae Weiser on dog food/agar medium. USDA Advances in Agriculture, 8.

Harris, C. R., and Svec, H. J. 1981. Colorado potato beetle resistance to carbofuran and several other insecticides in Quebec. J Econ Entomol, 74: 421–424. https://doi. org/10.1093/jee/74.4.421.

Hatab, M. A., and Gaugler, R. 2001. Diet Composition and lipids of in vitro-produced Heterorhabditis bacteriophora. Biological Control. 20: 1-7. https://doi. org/10.1006/bcon.2000.0870.

Hayes A. E., Fitzpatrick, S. M., Webster, J. M. 1999. Infectivity, distribution, and persistence of the entomopathogenic nematode Steinernema carpocapsae all strain (Rhabditida: Steinernematidae) applied by sprinklers or boom sprayer to dry-pick cranberries. J Econ Entomol, 92(3):539-46. https://doi.org/10.1093/ jee/92.3.539. PMID: 10407620.

Hazir, S., Kaya, H. K., Stock, S. P., and Keskün, N. 2003. Entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) for biological control of soil pests. Turk J Biol, 27: 181-202.

Herron, G. A., and James, T. M. 2005. Monitoring insecticide resistance in Australian Frankliniella occidentalis Pergande (Thysanoptera: Thripidae) detects fipronil and spinosad resistance. Aust J Entomol, 44: 299–303. https://doi.org/10..1111/j.1440-6055.2005.00478.x

Hough, W. S. 1928. Relative resistance to arsenical poisoning of two codling moth strains. J Econ Entomol, 21: 325– 329. https://doi.org/10..1093/jee/21.2.325

House, H. L., Welch, H. E., and Cleugh, T. R. 1965. Food medium of prepared dog biscuit for the mass production of the nematode DD-136 (Nematoda: Steinernematidae). Nature, 206: 847. https://doi.org/10.1038/206847a0 PMid:5891411.

Hsu, J.-C., Feng, H.-T., and Wu, W.-J. 2004. Resistance and synergistic effects of insecticides in Bactrocera dorsalis (Diptera: Tephritidae) in Taiwan. J Econ Entomol, 97: 1682–1688. https://doi.org/10.1603/0022-0493- 97.5.1682

Hussaini, S. S., Satya, J. K., and Hussaini, M. A. 2000. Mass production of a native Steinernema sp. (SSL2) PDBC EN 13.21 (Nematode: Steinernematidae) on different artificial media. Indian J Plant Protec, 28: 94-96.

Hussaini, S. S., Nagesh, M., Rajeshwari, R. and Manzoor, H. 2007. Effect of protein and lipid sources in the Wout’s medium on the yield and pathogenicity of Steinernema carpocapsae and S. tami. Indian J Plant Protec, 35: 93-96.

Hussaini, S. S., Singh, S. P. Parthasarathy, R. and Shakeela, V. 2002. In vitro production of entomopathogenic nematodes in different artificial media. Indian J Nematol, 32(1): 44-46.

Hussein, M. A. and Abdel-Aty, M. A. 2012. Formulation of two native entomopathogenic nematodes at room temperature. J Biopest, 5 (Supplementary): 23-27.

Immaraju, J. A., Paine, T. D., Bethke, J. A., Robb, K. L. and Newman, J. P. 1992. Western flower thrips (Thysanoptera: Thripidae) resistance to insecticides in coastal California greenhouses. J Econ Entomol, 85: 9–14. https://doi.org/10.1093/jee/85.1.9.

Kaur, A. 2023. Organic farming in India: The present scenario. J Emerg Technol Innov Res, 6(2). Kaya, H. K., and Gaugler, R. 1993. Entomopathogenic nematodes. Ann Rev Ent, 38: 181-206. https://doi. org/10.1146/annurev.en.38.010193.001145

Kaya, H. K., and Stock S. P. 1997. Techniques in insect nematology. In: Lacey LA (ed.). Manual of techniques in insect pathology (pp. 281-324). Academic Press, San Diego, CA. https://doi.org/10.1016/B978-012432555- 5/50016-6

Khan, H. A. A., and Akram, W. 2018. Trichlorfon and spinosad resistance survey and preliminary determination of the resistance mechanism in Pakistani field strains of Bactrocera dorsalis. Sci Rep, 8: 11223–11225. https:// doi.org/10.1038/s41598-018-29622-0

Kim, Y. H. 2015. Predatory nematodes as biocontrol agents of phytonematodes. In: Askary, TH, Martinelli PRP (eds). Biocontrol Agents of Phytonematodes (pp. 393- 420). CAB International, Wallingford, UK. https:// www.researchgate.net/publication/319261010_ Beneficial_Nematodes_in_Agroecosystems_A_ Global_Perspective.

Kim, T. W., Kim, T. H., Yasunaga‐Aoki, C., and Yu, Y. M. (2014). Mass production of entomopathogenic nematode, Heterorhabditits megidis by using micorosparger of gandong strain. J Faculty Agric, Kyushu Univ, 59 (2): 283–288.

Ko, A. E., Bieman, D. N., Schal, C. and Silverman. J. 2016. Insecticide resistance and diminished secondary kill performance of bait formulations against German cockroaches (Dictyoptera: Blattellidae). Pest Manag. Sci. 72(9):1778-84. https://doi.org/10.1002/ps.4211 PMID: 26689433; PMCID: PMC4917477.

Lacey, L. A., and Shapiro-Ilan, D. I. 2008. Microbial control of insect pests in temperate orchard systems: Potential for incorporation into IPM. Ann Rev Ent, 53: 121-144. https://doi.org/10.1146/annurev.ento.53.103106.093419 PMid:17803454

Leite, L. G., Shapiro-Ilan, D. I., Hazir, S., and Jackson, M. A. 2016. The effects of nutrient concentration, addition of thickeners, and agitation speed on liquid fermentation of Steinernema feltiae. J Nematol, 48(2): 126-133. https:// doi.org/10.21307/jofnem-2017-018 PMid:27418706 PMCid:PMC4930316.

Lindegren, J. E., Hoffman, D. F., Collier, S. S. and Fries, R.D. 1979. Propagation and storage of Neoaplectana carpocapsae Weiser using Amyelois transitella (Walker) adults. USDA Advances in Agriculture. 3: 1–5.

Lindegren, J. E., Valero, K. A., and Mackey, B. E. 1993. Simple in vivo production and storage methods for Steinernema carpocapsae infective juveniles. J. Nematol, 25: 193-197.

Lunau, S., Stoessel, S., Schmidt-Peisker, A. J., and Ehlers, R. 1993. Establishment of monoxenic innocula for scaling up in vitro cultures of the entomopathogenic Nematodes Steinernema spp. and Heterorhabditis spp. Nematologica, 39(1-4): 385-399. https://doi. org/10.1163/187529293X00330.

Martin, N. A., and Workman, P. J. 1994. “Confirmation of a pesticide-resistant strain of Western flower thrips in New Zealand,” in Proceedings of the Forty Seventh New Zealand Plant Protection Conference (New Zealand: Waitangi Hotel New Zealand Plant Protection Society), 144–148.

McCoy, E. E., and Glaser. R. W. 1936. Nemalode culture for Japanese beetle control. N J Dept Agric Circ. 265: 1-10. Mishra, J., Dutta, V., and Arora N. K. 2020. Biopesticides in India: Technology and sustainability linkages. 3 Biotech, 10(5). https://doi.org/10.1007/s13205-020- 02192-7 PMid:32351868 PMCid:PMC7181464.

Moffit, H. R., Westigard, P. H., Mantey, K. D., and Van de Baan, H. E. 1988. Resistance to diflubenzuron in the codling moth (Lepidoptera: Tortricidae). J Econ Entomol, 81: 1511–1515. https://doi.org/10.1093/jee/81.6.1511

Mukuka, J., Strauch, O., Hoppe, C., and Ehlers, R. U. 2010. Improvement of heat and desiccation tolerance in Heterorhabditis bacteriophora through cross-breeding of tolerant strains and successive genetic selection. Biocontrol, 55(4): 511-521. https://doi.org/10.1007/s10526-010-9271-4

Murray, D., Dunn, Belur, P. D., and Malan, A. P. 2021. A review of the in vitro liquid mass culture of entomopathogenic nematodes, Biocontrol Sci Technol, 31(1): 1-21. https://doi.org/10.1080/09583157.2020.1837072

Nagesh, M., Askary, T. H., Balachander, M., Arkalgud, S. N. and Rajan R. 2017. Strategies for making entomopathogenic nematodes cost-effective biocontrol agents. In: Biocontrol Agents: Entomopathogenic and Slug Parasitic Nematodes. Eds. Mahfouz M.M. Abd- Elgawad, Tarique Hassan Askary, James Coupland. CAB International, Wallingford, UK. https://doi.org/10.1079/9781786390004.0596

Nagesh, M., Haldhar, S. M., Saha, R. K., and Sindhu. 2022. Possibility of agri-entrepreneurships in promotion of biological control for crop and soil health with special reference to entomopathogenic nematodes. In: Haldhar SM, Sharma PT, Sarangthem, Singh SB (eds). Entrepreneurship Opportunities in Agriculture (pp. 34-45). Bhavya Books, New Delhi.

Nagesh, M., Hussaini, S. S., Prasad, J. S., Gururaj, K., Sindhu, M., and Bindu, S. 2023. Status and the way forward – Innovations for commercialization and promotion of entomopathogenic nematodes in IPM for PHM. International Conference on Plant Health Management, 2023 Nov 15-17, PJTSAU, Hyderabad, Telangana State, India.

Nagesh, M., Hussaini, S. S., Rabindra, R. J., and Salim, J. 2010. Indian Patent No. 295748/3490/CHE/2010. Amorphous formulation of entomopathogenic nematodes as biopesticide.

Navon, A., Keren, S., Salame, L., and Glazer, I. 1998. An edible-to-insects calcium alginate gel as a carrier for entomopathogenic nematodes. Biocontrol Sci Technol, 8(3): 429–437. https://doi. org/10.1080/09583159830225

Neves, J. M., Teixeira, J. A., Simoes, N., and Mota, M. 2001. Effect of airflow rate on yield of Steinernema carpocapsae Az 20 in liquid culture in an external-loop airlift bioreactor. Biotechnol Bioeng, 72: 369-373. https://doi.org/10.1002/1097-0290(20010205)72:3<369::AIDBIT15>3.0.CO;2-F PMid:11135208

Nguyen, N. C., Anh, L. T., Vu, N. H., and Phuc, H. K. 2022. The reproduction potentials of four entomopathogenic nematode strains related to cost-effective production for biological control. J Asia-Pacific Entomol, 25(3): 1-7. https://doi.org/10.1016/j.aspen.2022.101880

Nickle, W. R., Connick, Jr. W. J., and Cantelo, W. W. 1994. Effects of pesta-pelletized Steinernema carpocapsae (All) on western corn rootworms and Colorado potato beetles. J Nematol, 26: 249–250. https://www.researchgate.net/publication/309765035_ Formulation_of_Entomopathogenic_Nematodes_for_ Crop_Pest_Control_a_Review

Nilsson, U., and Gripwall, E. 1999. Influence of application technique on the viability of the biological control agents Verticillium lecanii and Steinernema feltiae. Crop Protec, 18: 53-59. https://doi.org/10.1016/S0261-2194(98)00095-7

Pace, W. G., Grote, W., Pitt D. E., and Pitt J. M. 1986. Liquid culture of nematodes. International Patent WO 86/01074.

Perry, R. N., Ehlers, R. U., and Glazer I. 2012. A realistic appraisal of methods to enhance desiccation tolerance of entomopathogenic nematodes. J Nematol, 44: 185-190.

Pérez-Campos, S. J., Rodríguez-Hernández, A. I., del- Rocío López-Cuellar, M., Zepeda-Bastida, A., and Chavarría-Hernández, N. 2018. In-vitro liquid culture of the entomopathogenic nematode, Steinernema colombiense, in orbitally shaken flasks. Biocontrol Sci and Technology, 28(9): 901-911.

Poinar, G. O. 1979. Nematodes for biological control of insects. Boca Raton, CRC Press, Fl. Poinar, G., and Grewal, P. S. 2012. History of Entomopathogenic Nematology. J Nematol, 44(2): 153- 161.

Poinar, G. O. 1990. Taxonomy and biology of Steinernematidae and Heterorhabditidae. In: Gaugler R, Kaya HK (eds.). Entomopathogenic nematodes in biological control (pp. 23-61). CRC Press, Boca Raton.

Poinar, G. O., and Thomas, G. M. 1966. Significance of Achromobacter nematophilus Poinar and Thomas (Achromobacteraceae: Eubacteriales) in the development of the nematode, DD-136 (Neoaplectana sp. Steinernematidae). Parasitol, 56(2): 385-90. https://doi.org/10.1017/S0031182000070980 PMid:4960247

Poinar, G. O. J. 1975. Description and biology of a new species Rhabditida heterorhabditidae new family. Nematologica, 21: 463-470. https://doi.org/10.1163/187529275X00239

Prabhu, S., Rajendran, G., and Subramanian, S. 2006. In vitro mass production technology for the entomopathogenic nematode, Steinernema glaseri. Indian J Nematol, 36(1): 142-144.

Raja, R. K., Hazir, C., Gümüş, A., Asan, C., Karagöz, M. and Hazir, S. 2015. Efficacy of the entomopathogenic nematode Heterorhabditis bacteriophora using different application methods in the presence or absence of a natural enemy. Turkish J Agric Forestry, 39(2). https:// doi.org/10.3906/tar-1410-33 Available at: https://journals.tubitak.gov.tr/agriculture/vol39/iss2/12

Ramakuwela, T., Hatting, J., Laing, M.D., Hazir, S., and Thiebaut, N. 2016. In vitro solid-state production of Steinernema innovationi with cost analysis. Biocontrol Sci Technol, 26: 792-808. https://doi.org/10.1080/09583157.2016.1159284

Reyes, M., and Sauphanor, B. 2008. Resistance monitoring in codling moth: A need for standardization. Pest Manag Sci Former Pestic Sci, 64: 945–953. https://doi.org/10.1002/ps.1588

Rodríguez, M. A., Bosch, D., Sauphanor, B., and Avilla, J. 2010 Susceptibility to organophosphate insecticides and activity of detoxifying enzymes in Spanish populations of Cydia pomonella Lepidoptera: Tortricidae. J Econ Entomol, 103: 482–491.

San-Blas, E., Campos-Herrera, R., Dolinski, C., Monteiro, C., Andaló, V., Leite, L., Rodríguez, M., Montero, P. M., Saenz, A., Cedano, C., López, J. C., Valle, E. D., Doucet, M., Lax, P., Navarro, P., Báez, F., Llumiquinga, P., Ruiz-Vega, J., Guerra-Moreno, A., and Stock, S. P. 2013. Entomopathogenic nematology in Latin America: A brief history, current research and future prospects. J Inv Pathol, 165: 22-45. https://doi.org/10.1016/j. jip.2019.03.010 PMid:30940472.

Shapiro-Ilan, D., and Dolinski, C. 2015. Entomopathogenic nematode application technology. In: Campos-Herrera, R. (eds). Nematode pathogenesis of insects and other pests (pp. 231-254). Sustainability in Plant and Crop Protection, Springer. https://doi.org/10.1007/978-3- 319-18266-7_9

Shapiro-Ilan, D. I., Gaugler, R., Tedders, W. L., Brown, I., and Lewis, E. E. 2002. Optimization of inoculation for in vivo production of entomopathogenic nematodes. J Nematol, 34: 343-350.

Shapiro-Ilan, D. I., Gouge, D. H., Piggott, S. J. and Patterson, F. J. 2006. Application technology and environmental considerations for use of entomopathogenic nematodes in biological control. BioControl, 38: 124–133.

Shapiro-Ilan, D., Han, R., and Dolinksi, C. 2012. Entomopathogenic Nematode Production and Application Technology. J Nematol, 44(2): 206-217.

Shapiro-Ilan, D. I., Lewis, E.E., Behle, R. W. and McGuire, M. R. 2001. Formulation of entomopathogenic nematodeinfected- cadavers. J Invertebrate Pathol, 78: 17–23.

Shapiro-Ilan, D., Lewis, E. E., and Schliekelman, P. 2014. Aggregative group behavior in insect parasitic nematode dispersal. Intl J Parasitol, 44: 49-54. https://doi.org/10.1016/j.ijpara.2013.10.002 PMid:24184157.

Shapiro-Ilan, D.I., Lewis, E. E., Tedders, W.L., and Son, Y. 2003. Superior efficacy observed in entomopathogenic nematodes applied in infected-host cadavers compared with application in aqueous suspension. J Invertebrate Pathol, 83: 270–272.

Shapiro-Ilan, D. I. and McCoy, C. W. 2000. Effect of culture method and formulation on the virulence of Steinernema riobrave (Rhabditida: Steinernematidae) to Diaprepes abbreviatus (Curculionidae). J Nematol., 32: 281–288.

Siddiqui, J. A., Fan, R., Naz, H., Bamisile, B. S., Hafeez, M., Ghani, M. I., Wei, Y., Xu, Y., and Chen X. 2023. Insights into insecticide-resistance mechanisms in invasive species: Challenges and control strategies. Front Physiol, 13: Article 1112278. https://doi.org/10.3389/fphys.2022.1112278 PMid:36699674 PMCid:PMC9868318.

Silver, S. C., Dunlop, D. B. and Grove, D. I. 1995. Granular formulation of entities with improved storage stability. WIPOPatent No. WO 95/0577.

Somwong, P., and Petcharat, J. 2012. Culture of the entomopathogenic nematode Steinernema carpocapsae (Weiser) on artificial media. ARPN J Agric Biol Sci, 7(4): 229-232.

Spence, K. O., Stevens, G. N., Arimoto, H., Ruiz-Vega, J., Kaya, H. K., and Lewis, E. E. 2011. Effect of insect cadaver desiccation and soil water potential during rehydration on entomopathogenic nematode (Rhabditida: Steinernematidae and Heterorhabditidae) production and virulence. J. Inv. Pathol., 106: 268-273. https://doi.org/10.1016/j.jip.2010.10.009 PMid:21047513

Spier, M. R., Vandenberghe, L. P. d., Medeiros, A. B. P., and Soccol, C. R. 2011. Application of different types of bioreactors in bioprocesses. In. Antolli PG, Liu Z (eds). Bioreactors: Design, properties and applications (pp. 55-90). New York, Nova Science Publishers.

Strauch, O., Oestergaard, J., Hollmer S., and Ehlers, R. U. 2004. Genetic improvement of the desiccation tolerance of the entomopathogenic nematode Heterorhabditis bacteriophora through selective breeding. BioCont., 31: 218-226. https://doi.org/10.1016/j.biocontrol.2004.03.009

Sunanda, B. S., and Siddiqui, A. U. 2013. In vitro production of Steinernema carpocapsae in different artificial media. Indian J Nematol, 43(1): 40-42.

Surrey, R. M., and Davies, R. J. 1996. Pilot scale liquid culture and harvesting of an entomopathogenic nematode, Heterorhabditis bacteriophora. J Inv Pathol, 67: 92-99. https://doi.org/10.1006/jipa.1996.0013

Tabassum, K. A., and Shahina, F. 2004. In vitro mass rearing of different species of entomopathogenic nematodes in monoxenic solid culture. Pakistan J Nematol, 22: 167- 175.

Toepfer, S., Hatala-Zseller, I., Ehlers, R. U., Peters, A., and Kuhlmann, U. 2010. The effect of application techniques on field-scale efficacy: Can the use of entomopathogenic nematodes reduce damage by western corn rootworm larvae? Agric Forest Entomol, 12: 389-402. https://doi. org/10.1111/j.1461-9563.2010.00487.x

Tofangsazi, N., Cherry, R. H., and Arthurs, S. P. 2014. Efficacy of commercial formulations of entomopathogenic nematodes against tropical sod webworm, Herpetogramma phaeopteralis (Lepidoptera: Crambidae). J Appl Entomol, 138: 656-661. https://doi.org/10.1111/jen.12125

Tumialis, D., Mazurkiewicz, A., and Skrzecz, I. 2021. Effect of agitation speed on the density of bacteria Photorhabdus luminescens and the population dynamics of nematodes Heterorhabditis megidis in liquid culture. J Helminthol, 95. https://doi.org/10.1017/S0022149X21000493 PMid:34505559

Upadhyay, D., Kooliyottil, R., Mandjiny, S., Inman, F., and Holmes, L. 2013. Mass production of the beneficial nematode Steinernema carpocapsae utilizing a fedbatch culturing process. Sci J Plant Pathol, 2(01): 52-58. https://doi.org/10.33687/phytopath.002.01.0076

Van Zyl, C., and Malan, A. 2014. The role of entomopathogenic nematodes as biological control agents of insect pests, with emphasis on the history of their mass culturing and in vivo production. African Entomol, 22(2): 235-249. https://doi.org/10.4001/003.022.0222

Vontas, J., Hernández-Crespo, P., Margaritopoulos, J. T., Ortego, F., Feng, H.-T., Mathiopoulos, K. D., et al. 2011. Insecticide resistance in Tephritid flies. Pestic. Biochem Physiol, 100: 199–205. https://doi.org/10.1016/j.pestbp.2011.04.004

Vyas, R. V., Patel, N. B., Patel, P., and Patel, D. J. 2002. Efficacy of entomopathogenic nematodes against Helicoverpa armigera on pigeon pea. Intl Chickpea Pigeon Pea Newsl, 9: 43-44.

Vyas, R. V., Patel, N. S., and Patel, D. J. 1999. Mass production technology for entomopathogenic nematodes, Steinernema spp. Indian J Nematol, 29(2): 178-181.

Vyas, R. V., Yadav, P., Gheelani, Y. H., Chaudhary, R. K., Patel, N. B. and Patel, D. J. 2001. In vitro mass production of native Steinernema sp. Annals Plant Protection Sciences, 9: 77-80.

Wang, J. X., and Bedding, R. A. 1998. Population dynamics of Heterorhabditis bacteriophora and Steinernema carpocapsae in in vitro solid culture. Fund Appl Nematol, 21: 165-171.

Wang, Y., Bilgrami, A. L., Shapiro-Ilan, D. and Gaugler, R. 2007. Stability of entomopathogenic bacteria, Xenorhabdus nematophila and Photorhabdus luminescens, during in vitro culture. Journal of Industrial Microbiol and Biotechnol, 34:73-81.

Wang, Z. H., Hou, W. J., Hao, C. Y., Wu, Q. J., Xu, B. Y., and Zhang, Y. J. 2011. Monitoring the insecticide resistance of the field populations of Western flower thrips, Frankliniella occidentalis in Beijing area. J Appl Entomol, 48(3): 542–547.

Wang, C., Scharf, M. E. and Bennett, G. W. 2004. Behavioral and physiological resistance of the German cockroach to gel baits (Dictyoptera:Blattellidae). J Econ Entomol, 97: 2067-2072.

Wang, C., Scharf, M.E. and Bennett, G.W. 2006. Genetic Basis for Resistance to Gel Baits, Fipronil, and Sugar- Based Attractants in German Cockroaches (Dictyoptera: Blattellidae). J Econ Entomol, 99(5): 1761-1767.

Welter, S. C., Varela, L., and Freeman, R. 1991. Codling moth resistance to azinphosmethyl in California. Resist. Pest Manag Newslett, 3: 12.

Wennemann, L., Cone, W. W., Wright, L. C., Perez, J., and Conant, M. M. 2003. Distribution patterns of entomopathogenic nematodes applied through drip irrigation systems. J Econ Ent, 96(2): 287-291. https://doi.org/10.1093/jee/96.2.287 PMid:14994792.

White, G. F. 1927. A method for obtaining infective nematode larvae from cultures. Science, 66: 302-303. https://doi.org/10.1126/science.66.1709.302.b PMid:17749713.

Wilson, M. J., Glen, D. M., and George, S. K. 1993. The rhabditid nematode Phasmarhabditis hermaphrodita as a potential biological control agent for slugs. Biocont Sci Technol, 3: 503-511. https://doi.org/10.1080/09583159309355306

Woodring, J. L., and Kaya, H. K. 1988. Steinernematid and Heterorhabditid nematodes: A handbook of biology and techniques. Southern Cooperative Series Bulletin, Vol. 331, Arkansas Agricultural Experiment Station, Fayetteville, AR.

Wouts, W. M. 1981. Mass production of the entomogenous nematode, Heterorhabditis heliothidis (Nematoda: Heterorhabditidae) on artificial media. J Nematol, 13: 467-469.

Yadav, S., Sharma, H. K., Siddiqui, A. U., and Sharma, S. K. 2015. In vitro mass production of Steinernema carpocapsae on different artificial media. Indian J Nematol, 45(1): 123-124.

Yoo, S., Brown, I., and Gaugler, R. 2000. Liquid media development for Heterorhabditis bacteriophora: Lipid source and concentration. Applied Microbiol Biotechnol., 54: 759-763. https://doi.org/10.1007/ s002530000478 PMid:11152066.

Young, J. M., Dunnill, P., and Pearce, J. D. 2002. Separation characteristics of liquid nematode cultures and the design of recovery operations. Biotechnol Progr, 18: 29-35. https://doi.org/10.1021/bp010122a PMid:11822896.

Yukawa, T., and Pitt, J. M. 1985. Nematode storage and transport. Int. Patent WO85/03412.

Yu, S. J. 1991. Insecticide resistance in the fall armyworm, Spodoptera frugiperda (JE Smith). Pestic Biochem Physiol, 39: 84–91. https://doi.org/10.1016/0048-3575(91)90216-9

Zervos, S., Johnson, S. C., and Webster, J. M. 1991. Effect of temperature and inoculum size on reproduction and development of Heterorhabditis heliothidis and Steinernema glaseri (Nematoda: Rhabditoidea) in Galleria mellonella. Canadian J Zool, 69: 1261-1264. https://doi.org/10.1139/z91-177.

Zhao, G., Liu, W. E. I., Brown, J. M., and Knowles, C. O. 1995. Insecticide resistance in field and laboratory strains of Western flower thrips (Thysanoptera: Thripidae). J Econ Entomol, 88: 1164–1170. https://doi.org/10.1093/jee/88.5.1164

Zhu, H., Grewal, P. S., and Reding, M. E. 2011. Development of a desiccated cadaver delivery system to apply entomopathogenic nematodes for control of soil pests. Appl Eng Agric, 27: 317-324. https://doi.org/10.13031/2013.37065

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