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Type: Article
Published: 2020-11-12
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Morphological and molecular characterization of Heterorhabditis bacteriophora isolated from Indian soils and their biocontrol potential

Nematology Laboratory, Department of Zoology, Chaudhary Charan Singh University, Meerut-250004, India
Nematology Laboratory, Department of Zoology, Chaudhary Charan Singh University, Meerut-250004, India Department of Zoology, Government Degree College, Billawar-184204, Kathua, Jammu and Kashmir, India.
Nematology Laboratory, Department of Zoology, Chaudhary Charan Singh University, Meerut-250004, India
Green Biotechnologies Research Centre of Excellence, University of Limpopo, Private Bag X1106, Sovenga 0727, Republic of South Africa
3Experimental Biology Research Group, Institute of Biology, University of Neuchatel, Neuchatel 2000, Switzerland.
Biocontrol nematode isolation nematode identification Helicoverpa armigera Heterorhabditis bacteriophora Holotrichia serrata Photorhabdus laumondii subsp. clarkei Spodoptera litura Nematoda

Abstract

Agricultural soils and open fields from Western Uttar Pradesh (India) were surveyed to determine the presence of entomopathogenic nematodes. From the entomopathogenic nematodes isolated, Heterorhabditis isolates were selected and further characterized using morphological, morphometrical and molecular approaches. The results showed that three isolated nematodes were Heterorhabditis bacteriophora and were associated with Photorhabdus laumondii subsp. clarkei bacteria, while the rests were identified as Heterorhabditis indica. The biocontrol potential of H. bacteriophora against three agricultural pests was evaluated. Nematode infectivity experiments showed that the nematode isolates DH7 and DH8 were highly pathogenic against cotton bollworm (Helicoverpa armigera) and tobacco cutworm (Spodoptera litura), and less pathogenic against white grub (Holotrichia serrata) larvae. This study sets the basis for establishing new biocontrol agents to be used in pest management programs in India.

References

  1. Aasha, Chaubey, A.K. & Bhat, A.H. (2019) Notes on Steinernema abbasi (Rhabditida: Steinernematidae) strains and virulence tests against lepidopteran and coleopteran pests. Journal of Entomology and Zoology Studies, 7, 954–964.

    Adams, B.J., Burnell, A.M. & Powers, T.O. (1998) A phylogenetic analysis of Heterorhabditis (Nemata: Rhabditidae) based on internal transcribed spacer 1 DNA sequence data. Journal of Nematology, 30, 22–39.

    Addinsoft, (2007) XLSTAT. Analyse de données et statistique avec MS Excel. Addinsoft, New York. [software]

    Ahmad, M., Arif, M.I. & Ahmad, M. (2007) Occurrence of insecticide resistance in field populations of Spodoptera litura (Lepidoptera: Noctuidae) in Pakistan. Crop Protection, 26, 809–817.

    https://doi.org/10.1016/j.cropro.2006.07.006

    Altschul, S.F., Gish, W., Miller, W., Myers, E.W. & Lipman, D.J. (1990) Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410.

    https://doi.org/10.1016/S0022-2836(05)80360-2

    Ansari, M.A., Tirry, L. & Moens, M. (2003) Entomopathogenic nematodes and their symbiotic bacteria for the biological control of Hoplia philanthus (Coleoptera: Scarabaeidae). Biological Control, 28, 111–117.

    https://doi.org/10.1016/S1049-9644(03)00032-X

    Achinelly, M.F., Eliceche, D.P., Belaich, M.N. & Ghiringhelli, P.D. (2017) Variability study of entomopathogenic nematode populations (Heterorhabditidae) from Argentina. Brazil Journal Biology, 77, 569–579.

    https://doi.org/10.1590/1519-6984.20015

    Bedding, R.A. & Akhurst, R.J. (1975) A simple technique for the detection of insect parasitic rhabditid nematodes in soil. Nematologica, 21, 109–110.

    https://doi.org/10.1163/187529275X00419

    Bale, J.S., van Lanteren, J.C. & Bigler, F. (2008) Biological Control and Sustainable food production. Philosophical Transactions of the Royal Society of London Biological Sciences, 363, 761–776.

    https://doi.org/10.1098/rstb.2007.2182

    Bellows, T.S. Jr. & Fisher, T.W. (1999) In: Handbook of Biological Control. Academic Press, San Diego, California, pp. 243–252.

    Bhat, A.H., Chaubey, A.K. & Askary, T.A. (2020a) Global distribution of entomopathogenic nematode, Steinernema and Heterorhabditis. Egyptian Journal of Biological Pest Control, 30. [in press]

    https://doi.org/10.1186/s41938-020-0212-y

    Bhat, A.H., Chaubey, A.K., Shokoohi, E. & Machado, R.A.R. (2020b) Molecular and phenotypic characterization of Heterorhabditis indica (Nematoda: Rhabditida) nematodes isolated during a survey of agricultural soils in Western Uttar Pradesh, India. Acta Parasitologica, 65. [in press]

    https://doi.org/10.1007/s11686-020-00279-y

    Bhat, A.H., Askary, T.H., Ahmad, M.J., Suman, Aasha, & Chaubey, A.K. (2020c) Description of Heterorhabditis bacteriophora (Nematoda: Heterorhabditidae) isolated from hilly areas of Kashmir Valley. Egyptian Journal of Biological Pest Control, 30. [in press]

    https://doi.org/10.1186/s41938-019-0197-6

    Bharti, L., Bhat, A.H., Chaubey, A.K. & Abolafia, J. (2020) Morphological and molecular characterization of Merlinius brevidens (Allen, 1955) Siddiqi, 1970 (Nematoda, Rhabditida, Merlinidae) from India. Journal of Natural History, 54. [in press]

    https://doi.org/10.1080/00222933.2020.1810352

    Bhat, A.H., Sharma, L. & Chaubey, A.K. (2020d) Characterisation of Xenrorhabdus stockiae associated symbiont of Steinernema surkhetense with a note on its geographical distribution and virulence. Egyptian Academic Journal of Biological Sciences A, Entomology, 13, 105–122.

    https://doi.org/10.21608/eajbsa.2020.75906

    Bhat, A.H., Chaubey, A.K., Shokoohi, E. & Mashela, P.W. (2019) Study of Steinernema hermaphroditum (Nematoda, Rhabditida) from the West Uttar Pradesh, India. Acta Parasitologica, 64, 720–737.

    https://doi.org/10.2478/s11686-019-00061-9

    Bhat, A.H., Chaubey, A.K. & Půža, V. (2018) The first report of Xenorhabdus indica from Steinernema pakistanense: co-phylogenetic study suggests co-speciation between X. indica and its steinernematid nematodes. Journal of Helminthology, 92, 1–10.

    https://doi.org/10.1017/S0022149X17001171

    Bhat, A.H., Istkhar, Chaubey, A.K., Půža, V. & San-Blas, E. (2017) First report and comparative study of Steinernema surkhetense (Rhabditida: Steinernematidae) and its symbiont bacteria from sub-continental India. Journal of Nematology, 49, 92–102.

    https://doi.org/10.21307/jofnem-2017-049

    Bhat, A.H., Bharti, L., Istkhar & Chaubey, A.K. (2016) Phylogenic, pathogenic and reproductive characterization of Heterorhabditis indica from district Meerut, India. Journal of Pharmacy and Biological Science, 6, 60–73.

    https://doi.org/10.21276/ijpbs.2016.6.3.7

    Bruno, P., Machado, R.A.R., Glauser, G., Köhler, A., Campos-Herrera, R., Bernal, J., Toepfer, S., Erb, M., Robert, C.A.M., Arce, C.C.M. & Turlings, T.C.J. (2020) Entomopathogenic nematodes from Mexico that can overcome the resistance mechanisms of the western corn rootworm. Scientific Reports, 10. [in press]

    https://doi.org/10.1038/s41598-020-64945-x

    Calvert, G.M., Karnik, J., Mehler, L., Beckman, J., Morrissey, B., Sievert, J., Barrett, R., Lackovic, M., Mabee, L., Schwartz, A., Mitchell, Y. & Moraga-McHaley, S. (2008) Acute pesticide poisoining among agricultural workers in the United States, 1998-2005. American Journal of Industrial Medicine, 51, 883–898.

    https://doi.org/10.1002/ajim.20623

    Campos-Herrera, R., Escuer, M., Labrador, S., Robertson, L., Barrios, L. & Gutiérrez, C. (2006) Distribution of the entomopathogenic nematodes from La Rioja (Northern Spain). Journal of Invertebrate Pathology, 95, 125–139.

    https://doi.org/10.1016/j.jip.2007.02.003

    Chandel, R.S., Chandla, V.K. & Dhiman, K.R. (2005) Vulnerability of potato white grubs to entomopathogenic fungi and nematodes. Potato Journal, 32, 192–194.

    Chattopadhyay, N., Balasubramaniam, R., Attri, S.D. Ray, K., Gracy, J., Khedikar, S. & Karmakar, C. (2019) Forewarning of incidence of Spodoptera litura (Tobacco caterpillar) in soybean and cotton using statistical and synoptic approach. Journal of Agrometeorology, 21, 68–75.

    Choudhary, A.K. & Srivastava, S.K. (2007) Efficacy and economics of some neem based products against tobacco caterpillar, Spodoptera litura F. on soybean in Madhya Pradesh, India. International Journal of Agricultural Science, 3, 15–17.

    Courtney, W.D., Polley, D. & Miller, V.L. (1955) TAF, an improved fixative in nematode technique. Plant Disease Reports, 39, 570–571.

    DolinskiI, C., Kamitani, F.L., Machado, I.R. & Winter, C.E. (2008) Molecular and morphological characterization of heterorhabditid entomopathogenic nematodes from the tropical rainforest in Brazil. Memórias do Instituto Oswaldo Cruz, Rio de Janeiro, 103, 150–159.

    https://doi.org/10.1590/S0074-02762008000200005

    Flanders, K.L., Miller, J.M. & 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. Journal of Economic Entomology, 89, 373–380.

    https://doi.org/10.1093/jee/89.2.373

    Forschler, B.T. & Nordin, G.L. (1988) Comparative pathogenicity of selected entomogenous nematodes to the hardwood borers, Prionoxystus roblniae (Lepidoptera: Cossidae) and Megacylletze vobiniae (Coleoptera: Cerambycidae). Journal of Invertebrate Pathology, 52, 343–347.

    https://doi.org/10.1016/0022-2011(88)90144-9

    Gedia, M.V., Vyas, H.J., Acharya, M.F. & Patel, P.V. (2008) Life table, rate of increase and stable age distribution of Spodoptera litura (Fabricius) on Cotton. Annals of Plant Protection Sciences, 16, 62–65.

    Glazer, I., Eliyau, M., Salame, L., Nakash, Y. & Blumberg, D. (2007) Evaluation of the efficacy of the entomopathogenic nematodes, Heterorhabditis sp. against sap beetles (Coleopteran: Nitidulidae). BioControl, 52, 259–270.

    https://doi.org/10.1007/s10526-006-9027-3

    Hall, T.A. (1999) BioEdit: a user–friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.

    Harris, N.C., Coonan, T.J., King, J.L. & Dunn, R.R. (2013) Endemism in host–parasite interactions among island populations of an endangered species. Diversity and Distributions, 19, 377–385.

    https://doi.org/10.1111/ddi.12016

    Hasegawa, M., Kishino, H. & Yano, T. (1985) Dating of the humanape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution, 22, 160–174.

    https://doi.org/10.1007/BF02101694

    Hill, V., Kuhnert, P., Erb, M. & Machado, R.A.R. (2020) Identification of Photorhabdus symbionts by MALDI-TOF mass spectrometry. Microbiology, mic000905.

    https://doi.org/10.1101/2020.01.10.901900

    Hussain, M.A. & Ahmad, W. (2015) The management of Helicoverpa species by entomopathogenic nematodes. In: Sree, K.S. & Varma, A. (Eds.), Biocontrol of Lepidopteran Pests. Soil Biology, 43, pp. 289–314.

    https://doi.org/10.1007/978-3-319-14499-3_14

    Imran, M., Hanif, K., Ahmad, M., Nasir, M. & Aslam-Sheikh, U.A. (2017) Comparative toxicity of insecticides against two important insect pests of cauliflower crop. Asian Journal of Agriculture and Biology, 5, 88–98.

    Kajol, Bhat, A.H., Aasha & Chaubey, A.K. (2020) Biochemical and molecular characterization of associated Photorhabdus symbiont of Indian strain of Heterorhabditis indica and its efficacy. Pakistan Journal of Nematology, 38, 15–24.

    https://doi.org/10.18681/pjn.v38.i01.p15-24

    Kalia, V., Sharma, G., Shapiro-Ilan, D.I. & Ganguly, S. (2014) Biocontrol potential of Steinernema thermophilum and its symbiont Xenorhabdus indica against lepidopteran pests: virulence to egg and larval stages. Journal Nematology, 46, 18–26.

    Kaya, H.K. & Gaugler, R. (1993) Entomopathogenic nematodes. Annual Review of Entomology, 38, 181–206.

    https://doi.org/10.1146/annurev.en.38.010193.001145

    Kranthi, K.R., Jadhav, D.R., Wanjari, R.R., Ali, S.S. & Russell, D.A. (2001) Carbamate and organophosphate resistance in cotton pests in India. Bulletin of Entomological Research, 91, 37–46.

    Kumar, P.V., Sreedevi, K. & Singh, S. (2017) Diagnostics of major white grub species associated with potato crop ecosystem in Himachal Pradesh, India. International Journal Current Microbiology Applied Science, 6, 2545–2555,

    https://doi.org/10.20546/ijcmas.2017.609.313

    Kumar, S., Stecher, G. & Tamura, K. (2016) MEGA7: Molecular Evolutionary Genetics Analysis Version 7.0 for bigger datasets. Molecular Biology and Evolution, 33, 1870–1874.

    https://doi.org/10.1093/molbev/msw054

    Lewis, E.E., Gaugler, R. & Harrison, R. (1992) Entomopathogenic nematode host finding: response to host contact cues by cruise and ambush foragers. Parasitology, 105, 309–319.

    https://doi.org/10.1017/S0031182000074230

    Machado, R.A.R., Bruno, P., Arce, C.C.M., Liechti, N., Köhler, A., Bernal, J. & Turlings, T.C. (2019) Photorhabdus khanii subsp. guanajuatensis subsp. nov., isolated from Heterorhabditis atacamensis, and Photorhabdus luminescens subsp. mexicana subsp. nov., isolated from Heterorhabditis mexicana entomopathogenic nematodes. International Journal of Systematic and Evolutionary Microbiology, 69, 652–661.

    https://doi.org/10.1099/ijsem.0.003154

    Machado, R.A.R., Wüthrich, D., Kuhnert, P., Arce, C.C.M., Thönen, L., Ruiz, C., Zhang, X., Robert, C.A.M., Karimi, J., Kamali, S., Ma, J., Bruggmann, R. & Erb, M. (2018) Whole-genome-based revisit of Photorhabdus phylogeny: proposal for the elevation of most Photorhabdus subspecies to the species level and description of one novel species Photorhabdus bodei sp. nov., and one novel subspecies Photorhabdus laumondii subsp. clarkei subsp. nov. International Journal of Systematic and Evolutionary Microbiology, 68, 2664–2681.

    https://doi.org/10.1099/ijsem.0.002820

    Mashela, P.W., Shokoohi, E. & Pofu, K.M. (2020) Morphological adjustments to hydrostatic pressure in pseudocoelomic cavity of Steinernema feltiae in response to Nemafric-BL phytonematicide. PLoS ONE, 15 (1), e0227448,

    https://doi.org/10.1371/journal.pone.0227448.

    Nadler, S.A., De Ley, P., Mundo-Ocampo, M., Smythe, A.B., Stock, S.P., Bumbarger, D., Adams, B.J., De Ley, T., Holovachov, I.O. & Baldwin, J.G. (2006) Phylogeny of Cephalobina (Nematoda): molecular evidence for recurrent evolution of probolae and incongruence with traditional classifications. Molecular Phylogenetics and Evolution, 40, 696–711.

    https://doi.org/10.1016/j.ympev.2006.04.005

    Nazrussalam, A.A., Ahmad, T. & Ali, H. (2007) Relative performance of insecticides and multineem schedules for management of pod borer, Helicoverpa armigera (Hübner) in pigenpea. Journal of Biological Sciences, 7, 1545–1547.

    https://doi.org/10.3923/jbs.2007.1545.1547

    Nei, M. & Kumar, S. (2000) Molecular evolution and phylogenetics. Vol. 86. Oxford University Press, New York, 333 pp. [https://sci-hub.tw/]

    https://doi.org/10.1046/j.1365-2540.2001.0923

    Nguyan, K.B., Shapiro-Ilan, D.I. & Mbata, G.N. (2008) Heterorhabditis georgiana n. sp. from Georgia, USA. Nematology, 10, 433–448.

    https://doi.org/10.1163/156854108783900276

    Patel, H.K., Patel, N.G. & Patel, V. (1971) Quantitative estimation of damage to tobacco caused by the leaf-eating caterpillar, Prodenia litura. Pest Articles & News Summaries, 17, 202–205.

    https://doi.org/10.1080/09670877109413349

    Patil, R.A., Mehta, D.M. & Jat, B.L. (2014) Studies on life fecundity tables of Spodoptera litura Fabricius on tobacco Nicotiana tabacum Linnaeus. African Journal of Agricultural Research, 3, 1–5.

    https://doi.org/10.4172/2161-0983.1000118

    Punithavalli, M., Muthukrishnan, N. & Rajkumar, M.B. (2014) Impact of Rice genotypes on the developmental characteristics of Rice leaf folder, Cnaphalocrocis medinalis. Indian Journal of Plant Protection, 42, 38–43.

    Pillay, U., Martin, L.A., Rutherford, R.S. & Berry, S.D. (2009) Entomopathogenic nematodes in Sugarcane in South Africa. Proceedings of South Africa Sugarcane Technology Assessment, 82, 538–541.

    Poinar, G.O. Jr. (1991) Genetic engineering of nematodes for pest control. In: Maramorosch, K. (Eds.), Biotechnology for Biological Control of Pests and Vectors. CRC Press, Boca Raton, Florida, pp.77–93.

    https://doi.org/10.1201/9781351070300-8

    Poinar, G.O. Jr., Karunakar, G.K. & David, H. (1992) Heterorhabditis indicus n. sp. (Rhabditida, Nematoda) from India: separation of Heterorhabditis spp. by infective juveniles. Fundamental and Applied Nematology, 15, 467–472.

    Poinar, G.O. Jr. (1971) Use of nematodes for microbial control of insects pests. In: Burges, H.D. & Hussey, N.W. (Eds.), Microbial control of Insects and Mites. Academic Press, New York, London, pp. 181–203.

    Poinar, G.O. Jr. (1976) Description and biology of a new insect parasitic rhabitoid, Heterorhabditis bacteriophora n. gen. n. sp. (Rhabditida; Heterorhabditidae n. family). Nematologica, 21, 463–470.

    https://doi.org/10.1163/187529275X00239

    Půža, V., Chundelová, D., Nermuť, J., Žurovcová, M. & Mráček, Z. (2015) Intra-individual variability of ITS region in entomopathogenic nematodes (Steinernematidae: Nematoda): implications for their taxonomy. BioControl, 60, 547–554.

    https://doi.org/10.1007/s10526-015-9664-5

    Rai, B.K., Joshi, H.C., Rathore, Y.K., Dutta, S.M. & Shinde, V.K.R. (1969) Studies on the bionomics and control of white grub, Holotrichia consanguinea Blanch in Lalsot district Jaipur, Rajasthan. Indian Journal of Entomology, 31, 132–142.

    Rana, A., Bhat, A.H., Bhargava, S., Chaubey, A.K. & Abolafia, J. (2020) Morphological and molecular characterization of Acrobeloides saeedi Siddiqi, De Ley and Khan, 1992 (Rhabditida, Cephalobidae) from India and comments on its status. Journal of Nematology, 52. [in press]

    https://doi.org/10.21307/jofnem-2020-027

    Ranganathaiah, K.G., Veeresh, G.K. & Govindu, H.C. (1973) A new entomogenous fungus on the root grub (Holotrichia serrata F.) from Mysore. Current Science, 42, 432–433.

    Rao, G.N. & Vijaylakshmi, U. (1959) A note on the occurrence of certain parasitic fungi on insect pests of sugarcane. Current Science, 28, 1–295.

    Rzhetsky, A. & Nei, M. (1992) A simple method for estimating and testing minimum evolution trees. Molecular Biology Evolution, 9, 945–967.

    Sagun, J.H., Davies, K.A., Fontanilla, I.K., Chan, M.A. & Laurente, D.A. (2015) Characterization of an isolate of Heterorhabditis bacteriophora (Nematoda: Heterorhabditidae) from the Northern Territory, Australia, using morphology and molecular data. Zootaxa, 4040 (1), 1–17.

    https://doi.org/10.11646/zootaxa.4040.1.2

    Sahayaraj, K. & Paulraj, M.G. (1998) Screening the relative toxicity of some plant extracts to Spodoptera litura Fab. (Insecta: Lepidoptera: Noctuidae) of ground nut. Fresenius Environmental Bulletin, 7, 557–560.

    Seinhorst, J.W. (1959) A rapid method for the transfer of nematodes from fixative to anhydrous glycerin G. Nematologica, 4, 67–69.

    https://doi.org/10.1163/187529259X00381

    Shapiro-Ilan, D.I., Lewis, E.E., Tedders, W.L. & Son, Y. (2003) Superior efficacy observed in entomopathogenic nematodes applied in infected-host cadavers compared with application in aqueous suspension. Journal of Invertebrate Pathology, 83, 270–272.

    https://doi.org/10.1016/S0022-2011(03)00101-0

    Shelter, D.J., Suleman, P.E. & Goergis, R. (1988) Irrigation and use of EPNs Neoplectana sp. and Heterorhabditis heliothiodis (Rhabditida: Heterorhabditidae and Steinernematidae) for the control of Japanese beetle (Coleoptera: Scarabaeidae) grubs in turf grass. Journal of Economic Entomology, 81, 1318–1988.

    https://doi.org/10.1093/jee/81.5.1318

    Shrilakshmi, R.G. & Patil, R.R. (2017) Assessment of economic injury level (EIL) due to Holotrichia fissa Brenske on groundnut under greenhouse and field conditions. International Journal of Current Microbiology & Applied Science, 6, 952–956. https://doi.org/10.20546/ijcmas.2017.607.116

    Shokoohi, E., Marais, M., Mashela, P.W. & Divsalar, N. (2020) Morphological and molecular variations within Helicotylenchus vulgaris. Biologia, 75. [in press]

    https://doi.org/10.2478/s11756-020-00551-6

    Singh, O.P. (2005) Consumption pattern of insecticide in Helicoverpa armigera management in India. In: Recent Advances in Helicoverpa armigera Management. Indian Society of Pulses Research and Development, Kanpur, pp. 17–24.

    Sivakumar, C.V., Jayaraj, S. & Subramanian, S. (1989) Observations on an Indian population of the entomopathogenic nematode, Heterorhabditis bacteriophora Poinar, 1976. Journal of Biological Control, 2, 112–113.

    Suman, Bhat, A.H, Aasha, Chaubey, A.K. & Abolofia, J. (2020) Morphological and molecular characterization of Distolabrellus veechi (Rhabditida: Mesorhabditidae) from India. Nematology, 22, 439–452.

    https://doi.org/10.1163/15685411-00003315

    Supekar, S. & Mohite, P. (2005) Utilization of entomopathogenic nematodes against White grub Holotrichia seerata Fab infesting Sugarcane. Journal of Global Biosciences, 4, 3178–3181.

    Tailliez, P., Laroui, C., Ginibre, N., Paule, A., Pagès, S. & Boemare, N. (2010) Phylogeny of Photorhabdus and Xenorhabdus based on universally conserved protein-coding sequences and implications for the taxonomy of these two genera. Proposal of new taxa: X. vietnamensis sp. nov., P. luminescens subsp. caribbeanensis subsp. nov., P. luminescens subsp. hainanensis subsp. nov., P. temperata subsp. khanii subsp. nov., P. temperata subsp. tasmaniensis subsp. nov., and the reclassification of P. luminescens subsp. thracensis as P. temperata subsp. thracensis comb. nov. International Journal of Systematic and Evolutionary Microbiology, 60, 1921–1937.

    https://doi.org/10.1099/ijs.0.014308-0

    Talekar, N.S., Opena, R.T. & Hanson, P. (2006) Helicoverpa armigera management: A review of AVRDC’s research on host plant resistance in tomato. Crop Protection, 25, 461–467.

    https://doi.org/10.1016/j.cropro.2005.07.011

    Tong, H., Su, Q., Zhou, X. & Bai, L. (2013) Field resistance of Spodoptera litura (Lepidoptera: Noctuidae) to organophosphates, pyrethroids, carbamates and four newer chemistry insecticides in Hunan, China. Journal of Pest Science, 86, 599–609.

    https://doi.org/10.1007/s10340-013-0505-y

    van Lenteren, J.C. & Godfray, H.C.J. (2005) European science in the Enlightenment and the discovery of the insect parasitoid life cycle in The Netherlands and Great Britain. Biological Control, 32, 12–24.

    https://doi.org/10.1016/j.biocontrol.2004.08.009

    van Lenteren, J.C., Bale, J.S., Bigler, F., Hokkanen, H.M.T. & Loomans, A.J.M. (2006) Assessing risks of releasing exotic biological control agents of arthropod pests. Annual Review of Entomology, 51, 609–634.

    https://doi.org/10.1146/annurev.ento.51.110104.151129

    Vanlalhlimpuia, Lalramliana, Lalramnghaki, H.C. & Vanramliana, (2018) Morphological and molecular characterization of entomopathogenic nematode, Heterorhabditis baujardi (Rhabditida, Heterorhabditidae) from Mizoram, Northeastern India. Journal of Parasitological Disease, 42, 341–349. [https://sci-hub.tw/]

    https://doi.org/10.1007/s12639-018-1004-0

    Venette, R.C., Davis, E.E., Zaspel, J., Heisler, H. & Larsen, M. (2003) Mini risk assessment. Rice cutworm, Spodoptera litura Fabricius (Lepidoptera: Noctuidae). Available from: http://www.aphis.usda.gov/ppq/ep/pestdetection/pra/sliturapra (accessed 29 September 2020)

    Vrain, T.C., Wakarchuk, D.A., Lévesque, A. & Hamilton, R.I. (1992) Intraspecific rDNA restriction fragment length polymorphism in the Xiphinema americanum group. Fundamentals and Applied Nematology, 15, 563–73.

    Wan, P., Wu, K.M., Huang, M.S., Yu, D.Z. & Wu, J.P. (2008) Population dynamics of Spodoptera litura (Lepidoptera: Noctuidae) on Bt cotton in the Yangtze River Valley of China. Environmental Entomology, 37, 1043–1048.

    https://doi.org/10.1093/ee/37.4.1043

    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-a

    Xing-Yue, L., Qi-Zhi, L., Nermuť, J., Půža, V. & Mráček, Z. (2012) Heterorhabditis beicherriana n. sp. (Nematoda: Heterorhabditidae), a new entomopathogenic nematode from the Shunyi district of Beijing, China. Zootaxa, 3569 (1), 25–40,

    https://doi.org/10.11646/zootaxa.3569.1.2

    Zhang, X., van Doan, C., Arce, C.C.M. Hu, L., Gruenig, S., Parisod, C., Hibbard, B.E., Hervé, M.R., Nielson, C., Robert, C.A.M., Machado, R.A.R. & Erb, M. (2019) Plant defense resistance in natural enemies of a specialist insect herbivore. Proceedings of the National Academy of Sciences, 116, 23174–23181.

    https://doi.org/10.1073/pnas.1912599116