Skip to main content
SpringerLink
Log in

Molecular and Phenotypic Characterization of Heterorhabditis indica (Nematoda: Rhabditida) Nematodes Isolated During a Survey of Agricultural Soils in Western Uttar Pradesh, India

  • Original Paper
  • Published:
Acta Parasitologica Aims and scope Submit manuscript

Abstract

Introduction

Entomopathogenic nematodes (EPNs) are important biocontrol agents of insect pests. To increase the availability of locally adapted entomopathogenic nematode isolates for biocontrol programs, a survey of several agricultural soils in Western Uttar Pradesh, India was conducted.

Materials and methods

Eight hundred and sixty soil samples from the districts Meerut, Bulandshahr, Baghpat, and Bijnor were collected and examined for the presence of entomopathogenic nematodos using the “Galleria baiting method”. Steinernema and Heterorhabditis nematodes were recovered. The isolated Heterorhabditis nematodes were molecularly, and morphologically characterized, and their biocontrol potential was evaluated against Spodoptera litura. Finally, the geographical distribution of entomopathogenic nematodes was studied based on the analysis of ITS GenBank records.

Results

A small proportion of the collected soil samples were positive for Heterorhabditis and Steinernema nematodes. Twelve soil samples were positive for the presence of Heterorhabditis nematodes, and 29 samples were positive for Steinernema. The Heterorhabditis nematodes were identified as Heterorhabditis indica based on morphological, morphometrical and molecular analyses. No other species of Heterorhabditis were isolated from the soil samples analyzed, suggesting that this species is dominant in the western part of Uttar Pradesh, India. The morphology of the nematode isolates was somewhat similar to the morphology of the H. indica isolate used for the original description of this species, with a notable exception mucrons were present in the hermaphrodite and female specimens we collected, but this structure was not observed in the specimens used for the original description of the species. Principal component analyses (PCA) show small inter- and intraspecific morphological variability between the nematodes species of the “Indica” clade. The insecticide properties of one isolate, CH7, were evaluated against Spodoptera litura, and the results show that this isolate effectively killed this pest under laboratory conditions, demonstrating its potential as a biocontrol agent.

Conclusion

This study sets the basis for establishing new biocontrol agents to be used in future pest management programs in India.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Achinelly MF, Eliceche DP, Belaich MN, Ghiringhelli PD (2017) Variability study of entomopathogenic nematode populations (Heterorhabditidae) from Argentina. Braz J Biol 77:569–579

    CAS  PubMed  Google Scholar 

  2. Adams BJ, Burnell AM, Powers TO (1998) A phylogenetic analysis of Heterorhabditis (Nemata: Rhabditidae) based on internal transcribed spacer 1 DNA sequence data. J Nematol 30:22–39

    CAS  PubMed  PubMed Central  Google Scholar 

  3. Adams BJ, Fodor A, Koppenhöfer HS, Stackenbrandt E, Stock SP, Klein MG (2006) Biodiversity and systematic of nematode–bacterium entomopathogens. Biol Control 38:4–21

    Google Scholar 

  4. Addinsoft (2007) XLSTAT. Analyse de données et statistique avec MS Excel, Addinsoft

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

    CAS  Google Scholar 

  6. Akhurst RJ (1980) Morphological and functional dimorphism in Xenorhabdus spp., bacteria symbiotically associated with the insect pathogenic nematodes. Neoaplectana and Heterorhabditis. J Gen Microbiol 121:303–309

    Google Scholar 

  7. Andaló V, Nguyen KB, Moino A (2007) Heterorhabditis amazonensis n. sp. (Rhabditida: Heterorhabditidae) from Amazonas. Brazil Nematol 8:853–867

    Google Scholar 

  8. Bedding RA, Akhurst RJ (1975) A simple technique for the detection of insect parasitic rhabditid nematodes in soil. Nematologica 21:109–110

    Google Scholar 

  9. Bhat AH, Chaubey AK & Askary TA (2020) Global distribution of entomopathogenic nematode, Steinernema and Heterorhabditis. Egypt J Biol Pest Control 30 (in press) https://doi.org/10.1186/s41938-020-0212-y.

  10. Bharti L, Bhat AH, Chaubey AK, Abolafia J (2020) Morphological and molecular characterization of Merlinius brevidens (Allen, 1955) Siddiqi, 1970 (Nematoda, Rhabditida, Merlinidae) from India. J Nat Hist 54 (in press). https://doi.org/10.1080/00222933.2020.1810352.

  11. Bhat AH, Askary TA, Ahmad MJ, Bhargava, Rana, Chaubey AK (2020) Description of Heterorhabditis bacteriophora (Nematoda: Heterorhabditidae) isolated from hilly areas of Kashmir valley. Egypt J Biol Pest Control 30 (in press) https://doi.org/10.1186/s41938-019-0197-6.

  12. Bhat AH, Sharma L, Chaubey AK (2020) Characterisation of Xenrorhabdus stockiae associated symbiont of Steinernema surkhetense with a note on its geographical distribution and virulence. Egypt Acad J Biol Sci A. Entomol 13:105–122. https://doi.org/10.21608/eajbsa.2020.75906

    Article  Google Scholar 

  13. Bhat AH, Chaubey AK, 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. J Helminthol 92:1–10

    Google Scholar 

  14. Bhat AH, Chaubey AK, Shokoohi E, Mashela PW (2019) Study of Steinernema hermaphroditum (Nematoda, Rhabditida), from the West Uttar Pradesh, India. Acta Parasitol 64:720–737. https://doi.org/10.2478/s11686-019-00061-9

    Article  CAS  PubMed  Google Scholar 

  15. Bhat AH, Istkhar CAK, Půža V, San-Blas, (2017) First report and comparative study of Steinernema surkhetense (Rhabditida: Steinernematidae) and its symbiont bacteria from subcontinental India. J Nematol 49:92–102

    CAS  PubMed  PubMed Central  Google Scholar 

  16. Bhat AH, Chaubey AK, Upadhyay SK (2016) Morphotaxometric and molecular validation of entomopathogenic nematode, Steinernema abbasi (Rhabditida: Steinernematidae) with mucronate processes in adults of second generations off subhumid region, Uttar Pradesh. World J Pharma Pharm Sci 5:1558–1579

    CAS  Google Scholar 

  17. Bird AF, Akhurst RJ (1983) The nature of the intestinal vesicle in nematodes of the family Steinernematidae. Int J Parasitol 13:599–606

    Google Scholar 

  18. Boemare NE, Akhurst RJ, Mourant RG (1993) DNA relatedness between Xenorhabdus spp. (Enterobacteriaceae), symbiotic bacteria of entomopathogenic nematodes and a proposal to transfer Xenorhabdus luminescens to a new genus, Photorhabdus gen. nov. Int J Syst Bacteriol 43:249–255

    CAS  Google Scholar 

  19. Boff MIC, Wiegers GL, Smits PH (2000) The influence of storage temperature and time on infectivity and reproduction of Heterorhabditis megidis (strain NLH-E87.3). IOBC WPRS Bulletin 23:53–60

    Google Scholar 

  20. Campos-Herrera R, Escuer M, Robertson L, Gutiérrez C (2006) Morphological and ecological characterization of Steinernema feltiae (Rhabditida: Steinernematidae) Rioja strain isolated from Bibio hortulanus (Diptera: Bibionidae) in Spain. J Nematol 38:68–75

    CAS  PubMed  PubMed Central  Google Scholar 

  21. Campos-Herrera R, Barbercheck M, Hoy CW, Stock SP (2012) Entomopathogenic nematodes as a model system for advancing the frontiers of ecology. J Nematol 44:162–176

    PubMed  PubMed Central  Google Scholar 

  22. Chattopadhyay N, Balasubramaniam R, Attri SD, 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. J Agrometeorol 21:68–75

    Google Scholar 

  23. Choudhary AK, Srivastava SK (2007) Efficacy and economics of some neem based products against tobacco caterpillar, Spodoptera litura F. on soybean in Madhya Pradesh. India Int J Agric Sci 3:15–17

    Google Scholar 

  24. Constant P, Marchay Fischer–Le Saux LM, Briand-Panoma S, Mauleon H (1998) Natural occurrence of entomopathogenic nematodes (Rhabditida: Steinernematidae and Heterorhabditidae) in Guadalupe islands. Fundam Appl Nematol 21:667–672

  25. Courtney WD, Polley D, Miller VL (1955) TAF, an improved fixative in nematode technique. Plant Dis Rep 39:570–571

    CAS  Google Scholar 

  26. Dhaliwal GS, Koul O (2010) Quest for Pest Management: FromGreen Revolution to Gene Revolution. Kalyani Publishers, NewDelhi

    Google Scholar 

  27. Dhir BC, Mohapatra HK, Senapati B (1992) Assessment of crop loss in groundnut due to tobacco caterpillar, Spodoptera litura (F.). Indian J Plant Prot 20:215–217

    Google Scholar 

  28. Divya K, Sankar M, Marulasiddesha KN (2010) Efficacy of Entomopathogenic nematode, Heterorhabditis indica against three lepidopteran insect pests. Asian J Exp Biol Sci 1:183–188

    Google Scholar 

  29. Dolinski C, Kamitani F, Machado I, Winter C (2008) Molecular and morphological characterization of heterorhabditid entomopathogenic nematodes from the tropical rainforest in Brazil. Mem Inst Oswaldo Cruz 103:150–159

    CAS  PubMed  Google Scholar 

  30. Ffrench-Constant R, Waterfield N, Daborn P, Joyce S, Bennett H, Au C, Dowling A, Boundy S, Reynolds S, Clarke D (2003) Photorhabdus: towards a functional genomic analysis of a symbiont and pathogen. FEMS Microbiol Rev 26:433–456

    CAS  PubMed  Google Scholar 

  31. Forschler BT, Nordin GL (1988) Comparative pathogenicity of selected entomogenous nematodes to the hardwood borers, Prionoxystus roblniae (Lepidoptera: Cossidae) and Megacylletze vobiniae (Coleoptera: Cerambycidae). J Invert Pathol 52:343–347. https://doi.org/10.1016/0022-2011(88)90144-9

    Article  Google Scholar 

  32. Gaugler R, Kaya HK (1990) Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, Florida, pp 233–246

    Google Scholar 

  33. Grewal PS, Ehlers RU, Shapiro-Ilan DI (2005) Nematodes as biological control agents. CABI Publishing, Wallingford

    Google Scholar 

  34. Hara AH, Kaya HK (1982) Effects of selected insecticides and nematicides on the in vitro development of the entomogenous nematode Neoaplectana carpocapsae. J Nematol 14:486–491

    CAS  PubMed  PubMed Central  Google Scholar 

  35. Harris NC, Coonan TJ, King JL, Dunn RR (2013) Endemism in host–parasite interactions among island populations of an endangered species. Divers Distrib 19:377–438

    Google Scholar 

  36. Hasegawa M, Kishino H, Yano T (1985) Dating of the human ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174

    CAS  Google Scholar 

  37. Hill DS (1983) Agricultural Insect Pests of the Tropics and their Control, 2nd edn. Cambridge University Press, London, p 746

    Google Scholar 

  38. Hunt DJ, Subbotin SA (2016) Taxonomy and systematics. In: Advances in entomopathogenic nematode taxonomy and phylogeny (Nguyen HB and Hunt DJ eds.). Leiden, the Netherlands, Brill Publishing, pp. 13–58

  39. Imran M, Hanif K, Ahmad M, Nasir M, Aslam Sheikh UA (2017) Comparative toxicity of insecticides against two important insect pests of cauliflower crop. Asian J Agric Biol 5:88–98

    Google Scholar 

  40. Kajol BAH, Aasha CAK (2020) Biochemical and molecular characterization of associated Photorhabdus symbiont of Indian strain of Heterorhabditis indica and its efficacy. Pak J Nematol 38:15–24. https://doi.org/10.18681/pjn.v38.i01.p15-24

    Article  Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  42. Kaya HK, Gaugler R (1993) Entomopathogenic nematodes. Annu Rev Entomol 38:181–206

    Google Scholar 

  43. Kranthi KR, Jadhav DR, Wanjari RR, Ali SS, Russell DA (2001) Carbamate and organophosphate resistance in cotton pests in India. Bull Entomol Res 91:37–46

    CAS  PubMed  Google Scholar 

  44. Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054

    Article  CAS  Google Scholar 

  45. Kung SP, Gaugler R, Kaya HK (1990) Influence of soil, pH and oxygen on persistence of Steinernema spp. J Nematol 22:440–445

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Kung SP, Gaugler R, Kaya HK (1991) Effect of temperature, moisture and relative humidity on entomopathogenic nematode persistence. J Invert Pathol 57:242–249

    Google Scholar 

  47. Lortkipanidze M, Hwseynov K, Kokhia M, Gorgadze O, Kuchava M (2018) Effect of Temperature on the Virulence of Entomopathogenic Nematodes. Adv Ecol Environ Res 3:32–38

    Google Scholar 

  48. Loya LJ, Hower JAA (2003) Infectivity and reproduction potential of the Oswego strain of Heterorhabditis bacteriophora associated with life stages of the clover root curculio, Sitona hispidulus. J Invert Pathol 72:63–72

    Google Scholar 

  49. Machado RAR, Bruno P, Arce CCM, Liechti N, Köhler A, Bernal J, Bruggmann R, Turlings TCJ (2019) Photorhabdus khanii subsp. guanajuatensis subsp. nov., isolated from Heterorhabditis atacamensis, and Photorhabdus luminescens subsp. mexicana subsp. nov., isolated from Heterorhabditis mexicana entomopathogenic nematodes. Int J Syst Evol Microbiol 69:652–661

    CAS  PubMed  Google Scholar 

  50. Machado RAR, Wüthrich D, Kuhnert P, Arce CCM, Thönen L, Ruiz C, Zhang X, Robert CAM, Karimi J, Kamali S, Ma J, Bruggmann R, Met E (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. Int J Syst Evol Microbiol 68:2664–2681

    CAS  PubMed  Google Scholar 

  51. Malan A, Knoetze R, Tiedt LR (2014) Heterorhabditis noenieputensis n. sp. Rhabditida: Heterorhabditidae), a new entomopathogenic nematode from South Africa. J Helminthol 88:139–151

    CAS  PubMed  Google Scholar 

  52. Martens EC, Heungens K, Goodrich-Blair H (2003) Early colonization events in the mutualistic association between Steinernema carpocapsae nematodes and Xenorhabdus nematophila bacteria. J Bacteriol 185:3147–3154

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Mashela PW, Shokoohi E, Pofu KM (2020) Morphological adjustments to hydrostatic pressure in pseudocoelomic cavity of Steinernema feltiae in response to Nemafric-BL phytonematicide. PLoS ONE. https://doi.org/10.1371/journal.pone.0227448

    Article  PubMed  PubMed Central  Google Scholar 

  54. Nadler SA, Bolotin E, Stock SP (2006) Phylogenetic relationships of Steinernema Travassos, 1927 (Nematoda: Cephalobina: Steinernematidae) based on nuclear, mitochondrial and morphological data. Syst Parasitol 63:161–181

    PubMed  Google Scholar 

  55. Nakasuji F, Matsuzaki T (1977) The control threshold density of the tobacco cutworm Spodoptera litura on egg plants and sweet peppers in vinyl-house. Appl Entomol Zool 12:184–189

    Google Scholar 

  56. Nei M, Kumar S (2000) Molecular evolution and phylogenetics. New York Oxford University Press 86:333. https://doi.org/10.1046/j.1365-2540.2001.0923

    Article  Google Scholar 

  57. Nguyen KB, Gozel N, Koppenhöfer HS, Adams BJ (2006) Heterorhabditis floridensis n.sp, (Rhabditida: Heterorhabditidae) from Florida. Zootaxa 1177:1–19

    Google Scholar 

  58. Nguyen KB, Shapiro-Ilan DI, Stuart RJ, Mccoy CW, James RR, Adams BJ (2004) Heterorhabditis mexicana n. sp. (Rhabditida: Heterorhabditidae) from Tamaulipas, Mexico, and morphological studies of the bursa of Heterorhabditis spp. Nematology 6:231–244

    Google Scholar 

  59. Patel HK, Patel NG, Patel VC (1971) Quantitative estimation of damage to tobacco caused by the leaf-eating caterpillar, Prodenia litura. Proc Natl Acad Sci USA 17:202–205

    Google Scholar 

  60. Patil RH (2002) Evaluation of insect pest management components in soybean ecosystem. Ph.D. Thesis, University of Agricultural Sciences, Dharwad (Karnataka, India), pp. 166

  61. Phan KL, Subbotin SA, Nguyen NC, Moens M (2003) Heterorhabditis baujardi sp. n. (Rhabditida: Heterorhabditidae) from Vietnam and morphometric data for H. indica populations. Nematology 5:367–382

    Google Scholar 

  62. Poinar GO Jr (1990) Entomopathogenic nematodes in biological control. In: Gaugler, r. and kaya H.K. (ed) Taxonomy and Biology of Steinernematidae and heterorhabdtidae. USA, CRC Press, Boca FL, pp 23–74

    Google Scholar 

  63. Poinar GO Jr, Karunakar GK, David H (1992) Heterorhabditis indicus n. sp. (Rhabditida, Nematoda) from India: separation of Heterorhabditis spp. by infective juveniles. Fundam Appl Nematol 15:467–472

    Google Scholar 

  64. Punithavalli M, Sharma AN, Balaji RM (2014) Seasonality of the common cutworm Spodoptera litura in a soybean ecosystem. Phytoparasitica 42:213–222

    Google Scholar 

  65. Rana A, Bhat AH, Bhargava S, Chaubey AK, Abolofia J (2020) Morphological and molecular characterization of Acrobeloides saeedi Siddiqi et al. (Rhabditida, Cephalobidae) from India and comments on its status. J Nematol https://doi.org/10.21307/jofnem-2020-027

  66. Razia M, Padmanaban R, Raja RK, Chellapandi P, Sivaramakrishnan, (2011) Monitoring entomopathogenic nematodes as ecological indicators in the cultivated lands of Karur district, Tamil Nadu: a survey report. Electron J Biol 7:16–19

    Google Scholar 

  67. Rzhetsky A, Nei M (1992) A simple method for estimating and testing minimum evolution trees. Mol Biol Evol 9:945–967

    CAS  Google Scholar 

  68. Sandstrom JP, Russel JA, White JP, Moran NA (2001) Independent origins and horizontal transfer of bacterial symbionts of aphids. Mol Ecol 10:217–228

    CAS  PubMed  Google Scholar 

  69. Sankara M, Sethuramanb V, Palaniyandib M, Prasada JS (2009) Entomopathogenic nematode-Heterorhabditis indica and its compatibility with other biopesticides on the Greater wax moth - Galleria mellonella (L.). Indian J Sci Technol 2:57–62

    Google Scholar 

  70. Seinhorst JW (1959) A rapid method for the transfer of nematodes from fixative to anhydrous glycerine. Nematologica 4:67–69

    Google Scholar 

  71. Selvan S, Campbell JFC, Gaugler R (1993) Density-dependant effects on entomopathogenic nematodes (Heterohabditidae : Steinernematidae) within an insect host. J Invert Pathol 62:278–284

    Google Scholar 

  72. Shahina F, Manzar H, Tabassum KA (2004) Symbiotic bacteria Xenorhabdus and Photorhabdus associated with entomopathogenic nematodes in Pakistan. Pak J Nematol 22:117–128

    Google Scholar 

  73. Shahina F, Tabassum KA, Salma J, Mehreen G, Knoetze R (2016) Heterorhabditis pakistanense n. sp. (Nematoda: Heterorhab-ditidae) a new entomopathogenic nematode from Pakistan. J Helminthol 91:222–235. https://doi.org/10.1017/S0022149X16000158

    Article  PubMed  Google Scholar 

  74. Shamseldean MM, Abou El-Sooud AB, Abd-Elgawad MM, Saleh MM (1996) Identification of a new heterorhabditid species from Egypt, Heterorhabditis taysearae n. sp. (Rhabditida: Heterorhabditidae). Egypt J Biol Pest Control 6:129–138

    Google Scholar 

  75. Shapiro-Ilan DI, Lewis EE, Behle RW, McGuire MR (2001) Formulation of Entomopathogenic Nematode-Infected Cadavers. J Invertn Pathol 78:17–23. https://doi.org/10.1006/jipa.2001.5030

    Article  CAS  Google Scholar 

  76. Shapiro-Ilan DI, Lewis EE, Tedders WL, Son Y (2003) Superior efficacy observed in entomopathogenic nematodes applied in infected-host cadavers compared with application in aqueous suspension. J Invert Pathol 83:270–272

    Google Scholar 

  77. Sivakumar CY, Jayaraj S, Subramanian S (1989) Observations on an Indian population of the entomopathogenic nematode, Heterorhabditis bacteriophora Poinar, 1976. J Biol Control 2:112–113

    Google Scholar 

  78. Smith IM, McNamara DG, Scott PR, Holderness M (1997) Spodoptera littoralis and Spodoptera litura. Quarantine Pests for Europe, 2nd edn. CAB International, Wallingford, Oxon, UK, pp 518–525

    Google Scholar 

  79. Somvanshi VS, Gahoi S, Banakar P, Thakur PK, Kumar M, Sajnani M, Pandey P, Rao U (2016) A transcriptomic insight into the infective juvenile stage of the insect parasitic nematode Heterorhabditis indica. BMC Genom 17:166. https://doi.org/10.1186/s12864-016-2510-z

    Article  CAS  Google Scholar 

  80. Spiridonov SE, Subbotin SA (2016) Phylogeny and phylogeography of Heterorhabditis and Steinernema. In: Advances in entomopathogenic nematode taxonomy and phylogeny (Nguyen HB and Hunt DJ eds.). Leiden, the Netherlands, Brill Publishing, pp. 413–427.

  81. Stuart RJ, Barbercheck ME, Grewal PS, Taylor RAJ, Hoy CW (2006) Population biology of entomopathogenic nematodes: Concepts, issues, and models. Biol Control 38:80–102

    Google Scholar 

  82. Suman BAH, Aasha CAK, Abolofia J (2020) Morphological and molecular characterisation of Distolabrellus veechi (Rhabditida: Mesorhabditidae) from India. Nematology 22:439–452. https://doi.org/10.1163/15685411-00003315

    Article  CAS  Google Scholar 

  83. Susurluk IA, Kumral NA, Peters A, Bilgili U, Aclkgoz E (2009) Pathogenicity, reproduction and foraging behaviours of some entomopathogenic nematodes on a new pest, Dorcadion pseudopreissi (Coleoptera; Cerambycidae). Biocontrol Sci Technol 19:585–594

    Google Scholar 

  84. Vanlalhlimpuia L, Lalramnghaki HC, Vanramliana, (2018) Morphological and molecular characterization of entomopathogenic nematode, Heterorhabditis baujardi (Rhabditida, Heterorhabditidae) from Mizoram, northeastern India. J Parasit Dis 42:341–349. https://doi.org/10.1007/s12639-018-1004-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Vashisth S, Chandel YS, Kumar S (2012) Biology and damage potential of Spodoptera litura Fabricius on some important greenhouse crops. J Insect Sci 25:150–154

    Google Scholar 

  86. Vrain TC, Wakarchuk DA, Levesque AC, Hamilton RI (1992) Intraspecific rDNA restriction fragment length polymorphisms in the Xiphinema americanum group. Fundam Appl Nematol 15:563–574

    Google Scholar 

  87. Wan P, Wu KM, Huang MS, Yu DZ, Wu JP (2008) Population dynamics of Spodoptera litura (Lepidoptera: Noctuidae) on Bt cotton in the Yangtze River Valley of China. Environ Entomol 37:1043–1048

    PubMed  Google Scholar 

  88. White GF (1927) A method for obtaining infective nematode larvae from cultures. Science 66:302–303

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the Head of the Department of Zoology for providing necessary laboratory facilities. Thanks also goes to Suman Bhargava for assisting in reference setting according to journal format.

Funding

AHB is thankful to the Department of Science and Technology for providing DST Inspire Fellowship/2014/76. The work of RARM is supported by the Swiss National Science Fundation (PZ00P3_186094).

Author information

Authors and Affiliations

  1. Nematology Laboratory, Department of Zoology, Chaudhary Charan Singh University, Meerut, 250004, India

    Aashaq Hussain Bhat & Ashok Kumar Chaubey

  2. Green Biotechnologies Research Centre of Excellence, University of Limpopo, Private Bag X1106, Sovenga, 0727, Republic of South Africa

    Ebrahim Shokoohi

  3. Experimental Biology Research Group, Institute of Biology, University of Neuchatel, 2000, Neuchatel, Switzerland

    Ricardo A. R. Machado

  4. Department of Zoology, Government Degree College Billawar-184204, University of Jammu, Billawar, Jammu, Jammu and Kashmir, India

    Aashaq Hussain Bhat

Authors
  1. Aashaq Hussain Bhat
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ashok Kumar Chaubey
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ebrahim Shokoohi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ricardo A. R. Machado
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Aashaq Hussain Bhat.

Ethics declarations

Conflict of interest

There is no conflict of interest.

Ethics approval

This article does not contain any studies with human participants or animals.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (TIF 1715 kb)

Supplementary file2 (DOCX 28 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bhat, A.H., Chaubey, A.K., Shokoohi, E. et al. Molecular and Phenotypic Characterization of Heterorhabditis indica (Nematoda: Rhabditida) Nematodes Isolated During a Survey of Agricultural Soils in Western Uttar Pradesh, India. Acta Parasit. 66, 236–252 (2021). https://doi.org/10.1007/s11686-020-00279-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

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

Keywords

Search

Navigation