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Entomopathogenic Nematodes and Their Bacterial Symbionts as Lethal Bioagents of Lepidopteran Pests

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Biocontrol of Lepidopteran Pests

Part of the book series: Soil Biology ((SOILBIOL,volume 43))

Abstract

The entomopathogenic nematodes, Steinernema and Heterorhabditis, are soil-dwelling parasites attacking a wide range of insect species including lepidopterans. Lepidopteran pests are destructive to agricultural crops as well as forest, ornamental and landscape vegetation. The pupal stages of these insects overwinter in the soils. The entomopathogenic nematodes have been proven to be the most successful biocontrol agents, also in comparison to chemical pesticides, to attack the insects in the cryptic habitats. Their foraging strategy and efficacy against lepidopteran pests in the field conditions on different crops have been detailed in this chapter. The incorporation of entomopathogenic nematodes in Bt refuge has also been discussed. In addition, the role of symbiotic entomopathogenic bacteria associated with these nematodes and their use as bioinsecticides have also been elaborated in this chapter.

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References

  • Akhurst RJ (1982) Antibiotic activity of Xenorhabdus spp., bacteria symbiotically associated with insect pathogenic nematodes of the families Heterorhabditidae and Steinernematidae. J Gen Microbiol 128:3061–3065

    CAS  PubMed  Google Scholar 

  • Barp MA, Kaya HK (1984) Evaluation of the entomogenous nematode Neoaplectana carpocapsae (=S. feltiae) Weiser (Rhabditida: S.tidae) and the bacterium Bacillus thuringiensis Berliner var. kurstaki for suppression of the Artichoke Plume Moth (Lepidoptera: Pterophoridae). J Econ Entomol 77:225–229

    Article  Google Scholar 

  • Baur ME, Kaya HK, Gaugler R, Tabashnik B (1997) Effects of adjuvants on entomopathogenic nematode persistence and efficacy against Plutella xylostella. Biocontrol Sci Technol 7:513–525

    Article  Google Scholar 

  • Baur ME, Kaya HK, Tabashnik BE, Chilcutt CF (1998) Suppression of diamondback moth (Lepidoptera: Plutellidae) with an entomopathogenic nematode (Rhabditida: Steinernematidae) and Bacillus thuringiensis Berliner. J Econ Entomol 91:1089–1095

    Article  CAS  PubMed  Google Scholar 

  • Bedding RA (1990) Logistic and strategies for introducing entomopathogenic nematode technology into developing countries. In: Gaugler R, Kaya HK (eds) Entomopathogenic nematodes in biological control. CRC Press, Boca Raton, pp 233–246

    Google Scholar 

  • Bélair G, Fournier Y, Dauphinais N (2003) Efficacy of steinernematid nematodes against three insect pests of crucifers in Quebec1. J Nematol 35:259–265

    PubMed Central  PubMed  Google Scholar 

  • Bentley W, Siegel JP, Holtz BA, Daane KM (2008) Navel orangeworm (Amyelois transitella) (Walker) and obliquebanded leafroller (Choristoneura rosaceana) (Harris) as pests of pistachio. In: Ferguson LF, Beede RH, Haviland DH, Holtz BA, Kallsen CE, Sanden BL (eds) Pistachio production manual. University of California, Davis, pp 179–191

    Google Scholar 

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

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Bowen DJ, Ensign JC (1998) Purification and characterization of a high-molecular-weight insecticidal protein complex produced by the entomopathogenic bacterium Photorhabdus luminescens. Appl Environ Microbiol 64:3029–3035

    PubMed Central  CAS  PubMed  Google Scholar 

  • Bowen DJ, Blackburn RM, Andreev O, Golubeva E, Bhartia R, ffrench-Constant RH (1998) Insecticidal toxins from bacterium Photorhabdus luminescens. Science 280:2129–2132

    Article  CAS  PubMed  Google Scholar 

  • Bruck DJ, Edwards DL, Donahue KM (2008) Susceptibility of the strawberry crown moth (Lepidoptera: Sesiidae) to entomopathogenic nematodes. J Econ Entomol 101:251–255

    Article  PubMed  Google Scholar 

  • Buhler WG, Gibb TJ (1994) Persistence of S. carpocapsae and S. glaseri as measured by their control of black cutworm larvae in bentgrass. J Econ Entomol 87:638–642

    Article  Google Scholar 

  • Cabanillas HE, Raulston JR (1995) Impact of S. riobravis (Rhabditida: Steinernematidae) on the control of Helicoverpa zea (Lepidoptera: Noctuidae) in corn. J Econ Entomol 88:58–64

    Article  Google Scholar 

  • Cabanillas HE, Raulston JR (1996) Evaluation of S. riobravis, S. carpocapsae, and irrigation timing for the control of corn earworm, Helicoverpa zea. J Nematol 28:75–82

    PubMed Central  CAS  PubMed  Google Scholar 

  • Campbell JF, Gaugler R (1993) Nictation behaviour and its ecological implications in the host search strategies of entomopathogenic nematodes. Behaviour 126:155–169

    Article  Google Scholar 

  • Campbell JF, Gaugler R (1997) Inter-specific variation in entomopathogenic nematode foraging strategy: dichotomy or variation along a continuum? Fund Appl Nematol 20:393–398

    Google Scholar 

  • Campbell J, Lewis E, Yoder F, Gaugler R (1996) Entomopathogenic nematode spatial distribution in turfgrass. Parasitology 113:473–482

    Article  PubMed  Google Scholar 

  • Chambers U, Bruck DJ, Olsen J, Walton VM (2010) Control of overwintering filbertworm (Lepidoptera: Tortricidae) larvae with S. carpocapsae. J Econ Entomol 103:416–422

    Article  PubMed  Google Scholar 

  • Chang YT, Hsieh C, Wu LC, Chang HC, Kao SS, Meng M, Hsieh FC (2013) Purification and properties of an insecticidal metalloprotease produced by Photorhabdus luminescens strain 0805-P5G, the entomopathogenic nematode symbiont. Int J Mol Sci 14:308–321

    Article  PubMed Central  CAS  Google Scholar 

  • Ciche TA, Ensign JC (2003) For the insect pathogen Photorhabdus luminescens, which end of a nematode is out? Appl Environ Microbiol 69:1890–1897

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Clarke DJ (2008) Photorhabdus: a model for the analysis of pathogenicity and mutualism. Cell Microbiol 10:2159–2167

    Article  CAS  PubMed  Google Scholar 

  • Cottrell TE, Shapiro-Ilan DI, Horton DL, Mizell RF (2011) Laboratory virulence and orchard efficacy of entomopathogenic nematodes against the lesser peachtree borer (Lepidoptera: Sesiidae). J Econ Entomol 104:47–53

    Article  CAS  PubMed  Google Scholar 

  • Cowles KN, Goodrich-Blair H (2005) Expression and activity of a Xenorhabdus nematophila haemolysin required for full virulence towards Manduca sexta insects. Cell Microbiol 7:209–219

    Article  CAS  PubMed  Google Scholar 

  • Dudney RA (1997) Use of Xenorhabdus nematophilus Im/1 and 19061/1 for fire ant control. US Patent US 5,616,318 970, 401. Application Information US 95-488,820 950,609

    Google Scholar 

  • Ebssa L, Koppenhöfer AM (2011) Efficacy and persistence of entomopathogenic nematodes for black cutworm control in turfgrass. Biocontrol Sci Technol 21:779–796

    Article  Google Scholar 

  • Feaster MA, Steinkraus DC (1996) Inundative biological control of Helicoverpa zea (Lepidoptera: Noctuidae) with the entomopathogenic nematode S. riobravis (Rhabditida: Steinernematidae). Biol Control 7:38–43

    Article  Google Scholar 

  • Forst S, Dowds B, Boemare N, Stackebrandt E (1997) Xenorhabdus and Photorhabdus spp.: bugs that kill bugs. Annu Rev Microbiol 51:47–72

    Article  CAS  PubMed  Google Scholar 

  • Furgani G, Boszormenyi E, Fodor A, Mathe-Fodor A, Forst S (2008) Xenorhabdus antibiotics: a comparative analysis and potential utility for controlling mastitis caused by bacteria. J Appl Microbiol 104:745–758

    Article  CAS  PubMed  Google Scholar 

  • Gassmann AJ, Stock SP, Carrière Y, Tabashnik BE (2006) Effect of entomopathogenic nematodes on the fitness cost of resistance to Bt toxin Cry1Ac in pink bollworm (Lepidoptera: Gelechiidae). J Econ Entomol 99:920–926

    Article  CAS  PubMed  Google Scholar 

  • Gassmann AJ, Stock SP, Sisterson MS, Carrière Y, Tabashnik BE (2008) Synergism between entomopathogenic nematodes and Bacillus thuringiensis crops: integrating biological control and resistance management. J Appl Ecol 45:957–966

    Article  Google Scholar 

  • Gaugler R, Campbell J, McGuire T (1989) Selection for host finding in S. feltiae. J Invertebr Pathol 54:363–372

    Article  Google Scholar 

  • Georgis R, Poinar GO Jr (1994) Nematodes as bioinsecticides in turf and ornamentals. In: Leslie AR (ed) Integrated pest management of turfgrass and ornamentals. Lewis Publishers, Boca Raton, pp 477–489

    Google Scholar 

  • Glaser RW (1932) Studies on Neoaplectana glaseri, nematode parasite of the Japanese beetle (Popillia japonica). N J Dept Agric 211:34

    Google Scholar 

  • Gouge DH, Reaves LL, Stoltman MM, Van Berkum JR, Burke RA, Forlow Jech LJ, Henneberry TJ (1996) Control of Pink boll-worm Pectiniphora gossipiella (Saunders) larvae in Arizona and Texas cotton fields using entomopathogenic nematodes S. riobravis. In: Ritcher DA, Armour J (eds) Proceedings of the Beltwide cotton production research conference. National Cotton Council of America, Memphis, pp 1078–1082

    Google Scholar 

  • Gouge DH, Smith KA, Payne C, Lee LL, Van Berkum JR, Ortega D, Henneberry, TJ (1997) Control of Pink boll-worm Pectiniphora gossipiella (Saunders) with biocontrol and biorational agents. In: Dugger P, Ritcher DA (eds) Proceedings of the Beltwide cotton production research conference. National Cotton Council of America, Memphis, pp 1066–1072

    Google Scholar 

  • Gray PA, Johnson DT (1983) Survival of the nematode Neoaplectana carpocapsae in relation to soil temperature, moisture, and time. J Georgia Entomol Soc 18:454–460

    Google Scholar 

  • Hannon ER, Sisterson MS, Stock SP, Carrière Y, Tabashnik BE, Gassmann AJ (2010) Effects of four nematode species on fitness costs of pink bollworm resistance to Bacillus thuringiensis toxin Cry1Ac. J Econ Entomol 103:1821–1831

    Article  PubMed  Google Scholar 

  • Kaya HK, Brown LR (1986) Field application of entomogenous nematodes for biological control of clear-wing moth borers in alders and sycamore trees. J Arboric 12:150–154

    Google Scholar 

  • Kienzle J, Zimmer J, Volk F, Zebitz CPW (2008) Experiences with entomopathogenic nematodes for the control of overwintering codling moth larvae in Germany. Archived at http://orgprints.org/13712

  • Koppenhöfer AM (2007) Nematodes. In: Lacey LA, Kaya HK (eds) Field manual of techniques in invertebrate pathology: application and evaluation of pathogens for control of insects and other invertebrate pests, 2nd edn. Springer, Dordrecht, pp 249–264

    Chapter  Google Scholar 

  • Lacey LA, Chauvin RL (1999) Entomopathogenic nematodes for control of codling moth in fruit bins. J Econ Entomol 92:104–109

    Article  CAS  PubMed  Google Scholar 

  • Lacey LA, Unruh TR (1998) Entomopathogenic nematodes for control of codling moth, Cydia pomonella (Lepidoptera: Tortricidae): effect of nematode species, concentration, temperature, and humidity. Biol Control 13:190–197

    Article  Google Scholar 

  • Lacey LA, Neven LG, Headrick HL, Fritts R Jr (2005) Factors affecting entomopathogenic nematodes (Steinernematidae) for control of overwintering codling moth (Lepidoptera: Tortricidae) in fruit bins. J Econ Entomol 98:1863–1869

    Article  PubMed  Google Scholar 

  • Lindegren JE, Agudelo-Silva F, Valero KA, Curtis CE (1987) Comparative small scale field application of S. feltiae for navel orangeworm control. J Nematol 19:503–504

    PubMed Central  CAS  PubMed  Google Scholar 

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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Mohan S, Sabir N (2005) Biosafety concerns on the use of Photorhabdus luminescens as biopesticide: experimental evidence of mortality in egg parasitoid Trichogramma spp. Curr Sci 89:1268–1272

    Google Scholar 

  • Mohan S, Raman R, Gaur HS (2003) Foliar application of Photorhabdus luminescens, symbiotic bacteria from entomopathogenic nematode H. indica, to kill cabbage butterfly Pieris brassicae. Curr Sci 84:1397

    Google Scholar 

  • Pena JE, Schroeder WJ, Osborne LS (1990) Use of entomogenous nematodes of the families Heterorhabditidae and Steinernematidae to control banana moth (Opogona sachari). Nematropica 20:51–55

    Google Scholar 

  • Poinar GO Jr (1993) Taxonomy and biology of Steinernematidae and Heterorhabditidae. In: Gaugler R, Kaya HK (eds) Entomopathogenic nematodes in biological control. Marcel Dekker, New York, pp 23–61

    Google Scholar 

  • Poinar GO Jr, Georgis R (1990) Characterization and field application of H. bacteriophora strain HP88. Revue-de-Nematologie 13:387–393

    Google Scholar 

  • Pollock C (2002) Nematodes effective against grape pests. http://fusion.ag.ohio state.edu/news/story.asp. Accessed 18 Feb 2003

  • Rajagopal R, Mohan S, Bhatnagar RK (2006) Direct infection of Spodoptera litura by Photorhabdus luminescens encapsulated in alginate beads. J Invertebr Pathol 93:50–53

    Article  CAS  PubMed  Google Scholar 

  • Razek AAS (2003) Pathogenic effects of Xenorhabdus nematophilus and Photorhabdus luminescens against pupae of the Diamondback moth, Plutella xylostella. J Pest Sci 76:108–111

    Google Scholar 

  • Riga E, Lacey LA, Guerra N, Headrick HL (2006) Control of the oriental fruit moth, Grapholita molesta, using entomopathogenic nematodes in laboratory and fruit bin assays. J Nematol 38:168–171

    PubMed Central  CAS  PubMed  Google Scholar 

  • Saunders MC, All JN (1985) Association of entomophilic rhabditoid nematode populations with natural control of first-instar larvae of the grape root borer, Vitacea polistiformis, in Concord grape vineyards. J Invertebr Pathol 45:147–151

    Article  Google Scholar 

  • Schroer S, Ehlers RU (2005) Foliar application of the entomopathogenic nematode S. carpocapsae for biological control of diamondback moth larvae (Plutella xylostella). Biol Control 33:81–86

    Article  Google Scholar 

  • Schroer S, Sulistydanto D, Ehlers RU (2005) Control of Plutella xylostella using polymer-formulated S. carpocapsae and Bacillus thuringiensis in cabbage fields. J Appl Entomol 129:128–204

    Article  Google Scholar 

  • Shapiro-Ilan DI, Gaugler R (2010) Nematodes: Rhabditida: Steinernematidae & Heterorhabditidae. In: Shelton A (ed) Biological control: a guide to natural enemies in North America. Cornell University. http://www.biocontrol.entomology.cornell.edu/pathogens/nematodes.htm

  • Shapiro-Ilan DI, Gouge DH, Koppenho¨fer AM (2002) Factors affecting commercial success: case studies in cotton, turf and citrus. In: Gaugler R (ed) Entomopathogenic nematology. CABI Publishing, Wallingford, pp 333–355

    Chapter  Google Scholar 

  • Siegel J, Lacey LA, Fritts R, Higbee BS, Noble P (2004) Use of Steinernematid nematodes for post harvest control of navel orangeworm (Lepidoptera: Pyralidae, Amyelois transitella) in fallen pistachios. Biol Cont 30:410–417

    Article  Google Scholar 

  • Snyder H, Stock SP, Kim SK, Flores-Lara Y, Forst S (2007) New insights into the colonization and release processes of Xenorhabdus nematophila and the morphology and ultrastructure of the bacterial receptacle of its nematode host, S. carpocapsae. Appl Environ Microbiol 73:5338–5346

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Somvanshi VS, Ganguly S, Paul AVN (2006) Field efficacy of the entomopathogenic nematode S. thermophilum Ganguly and Singh (Rhabditida: Steinernematidae) against diamondback moth (Plutella xylostella L.) infesting cabbage. Biol Control 37:9–15

    Article  Google Scholar 

  • Thomas GM, Poinar GO Jr (1979) Amended description of the genus Xenorhabdus Thomas and Poinar. Int J Syst Bacteriol 33:878–879

    Article  Google Scholar 

  • Unruh TR, Lacey LA (2001) Control of codling moth, Cydia pomonella (Lepidoptera: Tortricidae) with S. carpocapsae: effects of supplemental wetting and pupation site on infection rate. Biol Control 20:48–56

    Article  Google Scholar 

  • Wang J (1993) Control of the peach fruit moth, Carposina niponensis, using entomopathogenic nematodes. In: Bedding R, Akhurst R, Kaya H (eds) Nematodes and the biological control of insect pests. CSIRO Publications, East Melbourne, pp 59–65

    Google Scholar 

  • Waterfield N, Bowen DJ, Fetherston JD, Perry RD, ffrench-Constant RH (2001) The toxin complex genes of Photorhabdus: a growing gene family. Trends Microbiol 9:185–191

    Article  CAS  PubMed  Google Scholar 

  • Xu JL, Yang P (1992) The application of the codling moth nematode against the litchi stemborer. Acta Phytophylacica Sinica 19:217–222

    Google Scholar 

  • Zalom FG, Barnett WW, Weakley CV (1984) Efficacy of winter sanitation for managing the navel orangeworm, Paramyelois transitella (Walker), in California almond orchards. Prot Ecol 7:37–41

    Google Scholar 

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Authors and Affiliations

  1. Division of Nematology, Indian Agricultural Research Institute, New Delhi, 110012, India

    Sharad Mohan

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  1. Sharad Mohan
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Correspondence to Sharad Mohan .

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  1. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida, Uttar Pradesh, India

    K. Sowjanya Sree

  2. Amity Institute of Microbial Technology, Amity University Uttar Pradesh, Noida, Uttar Pradesh, India

    Ajit Varma

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Mohan, S. (2015). Entomopathogenic Nematodes and Their Bacterial Symbionts as Lethal Bioagents of Lepidopteran Pests. In: Sree, K., Varma, A. (eds) Biocontrol of Lepidopteran Pests. Soil Biology, vol 43. Springer, Cham. https://doi.org/10.1007/978-3-319-14499-3_13

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