Skip to main content
SpringerLink
Log in

Entomopathogenic nematodes (Steinernema spp. and Heterorhabditis bacteriophora) and a fungus Beauveria brongniartii for biological control of the white grubs, Ectinohoplia rufipes and Exomala orientalis, in Korean golf courses

  • Published:
BioControl Aims and scope Submit manuscript

Abstract

Three species of entomopathogenicnematodes, a combination of two nematodespecies, an entomopathogenic fungal species,and a combination of a nematode and fungalspecies were evaluated against the white grubsEctinohoplia rufipes and Exomalaorientalis (Coleoptera: Scarabaeidae) in the field. The nematodes were acommercial formulation of Steinernemacarpocapsae (BioSafe) and S. glaseri from Dongrae and from Hanrim, and Heterorhabditis bacteriophora from Hamyang,Republic of Korea. The entomopathogenic funguswas Beauveria brongniartii, produced onSabouraud maltose agar plus 1% yeast (SMAY),rice bran, or compost. The combinationtreatment was S. carpocapsae with H.bacteriophora or B. brongniartii. Fieldapplications were made in August or Septemberagainst third instars at a golf course infestedwith E. rufipes in Gyeongnam Province in1991, and one in Pusan with E. orientalisin 1992 and 1993. In 1991, a significantreduction of 70.2 to 79.4% of E. rufipeslarvae was observed in the nematode, fungal andchemical (fenitrothion) treatments comparedwith a 15.7% reduction in the control. In1992, the E. orientalis larval populationwas reduced between 62.7 and 82.8% in thetreatments compared to 10.7% in the control.In 1993, larval reductions in plots treatedwith nematodes (78.3 to 97%) and B.brongniartii propagated on rice bran (84.5%)were significantly better than in plots treatedwith B. brongniartii propagated on SMAY(63.6%) or compost (59.6%). Combining twonematode species did not enhance the efficacycompared to treatments with one nematodespecies alone, but combining S.carpocapsae with B. brongniartiiproduced on SMAY resulted in a significantincrease in grub mortality over the applicationof the fungus alone produced on SMAY orcompost. The high efficacy of the nematode andmost fungal treatments was attributed to theclose proximity of the white grubs to the soilsurface which allowed for excellentpathogen-host contact and to favorable soiltemperatures, sandy soil, post irrigationapplication and/or rain and a minimal thatchlayer in the turfgrass.

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

Similar content being viewed by others

References

  • Akhurst, R.J., R.A. Bedding, R.M. Bull and D.J. Smith, 1992. An epizootic of Heterorhabditis spp. (Heterorhabditidae: Nematoda) in sugar cane scarabaeids (Coleoptera). Fundam. Appl. Nematol. 15: 71–73.

    Google Scholar 

  • Alm, S.R., T. Yeh, J.L. Hanula and R. Georgis, 1992. Biological control of Japanese, Oriental, and Black Turfgrass Ataenius beetle (Coleoptera: Scarabaeidae) larvae with entomopathogenic nematodes (Nematoda: Steinernematidae, Heterorhabditidae). J. Econ. Entomol. 85: 1660–1665.

    Google Scholar 

  • Barbercheck, M.E. and H.K. Kaya, 1991. Effect of host condition and soil texture on host finding by the entomogenous nematodes Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae) and Steinernema carpocapsae (Rhabditida: Steinernematidae). Environ. Entomol. 20: 582–589.

    Google Scholar 

  • Bedding, R.A. and R.J. Akhurst, 1975. A simple technique for the detection of insect pathogenic nematodes in soil. Nematologica 21: 109–110.

    Google Scholar 

  • Choo, H.Y., A.M. Koppenhöfer and H.K. Kaya, 1996. Combination of two entomopathogenic nematode species for suppression of an insect pest. J. Econ. Entomol. 89: 97–103.

    Google Scholar 

  • Choo, H.Y., H.K. Kaya and S.P. Stock, 1995. Isolation of entomopathogenic nematodes (Steinernematidae and Heterorhabditidae) from Korea. Jpn. J. Nematol. 25: 44–51.

    Google Scholar 

  • Choo, H.Y., D.W. Lee, S.M. Lee, T.W. Kweon, Y.T. Sung and P.Y. Cho, 1998. White grubs in turfgrass of golfcourses and their seasonal density. Kor. Turfgrass Sci. 12: 225–236 (in Korean with English summary).

    Google Scholar 

  • Choo, H.Y., D.W. Lee, J.W. Park and J.W. Lee, 1999. Comparison of four major scarab beetles, Ectinohoplia rufipes, Adoretus tenuimaculatus, Exomala orientalis and Popillia quadriguttata in golfcourses. Kor. Turfgrass Sci. 13: 101–112 (in Korean with English summary).

    Google Scholar 

  • Downing, A.S., 1994. Effect of irrigation and spray volume on efficacy of entomopathogenic nematodes (Rhabditida: Heterorhabditidae) against white grubs (Coleoptera: Scarabaeidae). J. Econ. Entomol. 87: 643–646.

    Google Scholar 

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

    Google Scholar 

  • Ferron, P., 1981. Pest control by the fungi Beauveria and Metarhizium. In: H.D. Burges (eds), Microbial Control of Pests and Plant Disease 1970–1980. Academic Press, London. pp. 465–482.

    Google Scholar 

  • Forschler, B.T. and W.A. Gardner, 1991. Field efficacy and persistence of entomogenous nematodes in the management of white grubs (Coleoptera: Scarabaeidae). J. Econ. Entomol. 84: 1454–1459.

    Google Scholar 

  • Glare, T.R., 1994. Stage-dependent synergism using Metarhizium anisopliae and Serratia entomophila against Costelytra zealandica. Biocontr. Sci. Technol. 4: 321–329.

    Google Scholar 

  • Georgis, R. and R. Gaugler, 1991. Predictability in biological control using entomopathogenic nematodes. J. Econ. Entomol. 84: 713–720.

    Google Scholar 

  • Hiromori, H. and J. Nishigaki, 1998. Joint action of an entomopathogenic fungus Metarhizium anisopliae with synthetic insecticides against the scarab beetle, Anomala cuprea (Coleoptera: Scarabaeidae) larvae. Appl. Entomol. Zool. 33: 77–84.

    Google Scholar 

  • Jaques, R. and O.N. Morris, 1981. Compatibility of pathogens with other methods of pest control and with different crops. In: H.D. Burges (eds), Microbial Control of Pests and Plant Disease 1970–1980. Academic Press, New York. pp. 283–302.

    Google Scholar 

  • Kaya, H.K. and R. Gaugler, 1993. Entomopathogenic nematodes. Annu. Rev. Entomol. 38: 181–206.

    Google Scholar 

  • Kaya, H.K. and S.P. Stock, 1997. Techniques in insect pathology. In: L.A. Lacey (eds), Manual of Techniques in Insect Pathology. Academic Press, San Diego. pp. 281–324.

    Google Scholar 

  • Kaya, H.K., M.G. Klein and T.M. Burlando, 1993. Impact of Bacillus popilliae, Rickettsiella popilliae and entomopathogenic nematodes on a population of the scarabaeid, Cyclocephala hirta. Biocontr. Sci.Technol. 3: 443–453.

    Google Scholar 

  • Keller, S., 1992. The Beauveria-Melolontha project: experiences with regard to locust and grasshopper control. In: C.J. Lomer and C. Prior (eds), Biological Control of Locusts and Grasshoppers. CAB International, Wallingford. pp. 279–286.

    Google Scholar 

  • Klein, M.G., 1990. Efficacy against soil-inhabiting insect pests. In: R. Gaugler and H.K. Kaya (eds), Entomopathogenic Nematodes in Biological Control. CRC Press, Boca Raton. pp. 195–214.

    Google Scholar 

  • Klein, M.G., 1993. Biological control of scarabs with entomopathogenic nematodes. In: R. Bedding, R. Akhurst and H. Kaya (eds), Nematodes and The Biological Control of Insect Pests. CSIRO Publications, East Melbourne. pp. 49–57.

    Google Scholar 

  • Klein, M.G. and R. Georgis, 1992. Persistence of control of Japanese beetle (Coleoptera: Scarabaeidae) larvae with steinernematid and heterorhabditid nematodes. J. Econ. Entomol. 85: 727–730.

    Google Scholar 

  • Klein, M.G. and T.A. Jackson, 1992. Bacterial diseases of scarabs. In: T.A. Jackson and T.R. Glare (eds), Use of Pathogens in Scarab Pest Management. Intercept, Andover. pp. 43–61.

    Google Scholar 

  • Koppenhöfer, A.M., H.Y. Choo, H.K. Kaya, D.W. Lee and W.D. Gelernter, 1999. Increased field and greenhouse efficacy against scarab grubs with a combination of an entomopathogenic nematode and Bacillus thuringiensis. Biol. Contr. 14: 37–44.

    Google Scholar 

  • Koppenhöfer, A.M. and H.K. Kaya, 1997. Additive and synergistic interaction between entomopathogenic nematodes and Bacillus thuringiensis for scarab grub control. Biol. Contr. 8: 131–137.

    Google Scholar 

  • Koppenhöfer, A.M., P. Grewal and H.K. Kaya, 2000. Synergism of imidacloprid and entomopathogenic nematodes against white grubs: the mechanism. Entomol. Exp. Appl. 94: 283–293.

    Google Scholar 

  • Lewis, E.E., R. Gaugler and R. Harrison, 1993. Responses of cruiser and ambusher entomopathogenic nematodes (Steinernematidae) to host volatile cues. Can. J. Zool. 71: 765–769.

    Google Scholar 

  • McCoy, C.W., 1990. Entomogenous fungi as microbial pesticides. In: R.R. Baker and P.E. Dunn (eds), New Directions in Biological Control: Alternatives for Suppressing Agricultural Pests and Diseases. Alan Liss, New York. pp. 115–138.

    Google Scholar 

  • Rath, A.C., 1992. Metarhizium anisopliae for control of the Tasmanian pasture scarab Adoryphorus couloni. In: T.A. Jackson and T.R. Glare (eds), Use of Pathogens in Scarab Pest Management. Intercept, Andover. pp. 217–227.

    Google Scholar 

  • Rath, A.C., D. Worledge, T.B. Koen and B.A. Rowe, 1995. Long-term field efficacy of the entomogenous fungus Metarhizium anisopliae against subterranean scarab, Adoryphorus couloni. Biocontr. Sci. Technol. 5: 439–451.

    Google Scholar 

  • Samuels, K.D.Z., D.E. Pinnock and R.M. Bull, 1990. Scarabaeid larvae control in sugarcane using Metarhizium anisopliae. J. Invertebr. Pathol. 55: 135–137.

    Google Scholar 

  • SAS Institute, 1988. SAS/STAT user's guide, vols. 1 and 2. Cary, NC.

  • Selvan, M.S., P.S. Grewal, R. Gaugler and M. Tomalak, 1994. Evaluation of steinernematid nematodes against Popillia japonica (Coleoptera: Scarabaeidae) larvae: species, strains, and rinse after application. J. Econ. Entomol. 87: 605–609.

    Google Scholar 

  • Smits, P.H., 1992. Control of white grubs, Phyllopertha horticola and Amphimallon solstitialis in grass with heterorhabditid nematodes. In: T.A. Jackson and T.R. Glare (eds), Use of Pathogens in Scarab Pest Management. Intercept, Andover. pp. 229–235.

    Google Scholar 

  • Smits, P.H., 1996. Post-application persistence of entomopathogenic nematodes. Biocontr. Sci. Technol. 6: 379–387.

    Google Scholar 

  • Smits, P.H., G.L. Wiegers and H.J. Vlug, 1994. Selection of insect parasitic nematodes for biological control of the garden chafer, Phyllopertha horticola. Entomol. Exp. Appl. 70: 77–82.

    Google Scholar 

  • Stock, S.P., H.Y. Choo and H.K. Kaya, 1997. First record of Steinernema glaseri Steiner, 1929 (Nematoda: Steinernematidae) in Asia, with notes on intraspecific. Nematologica43: 377–381.

    Google Scholar 

  • Storey, G.K. and W.A. Gardner, 1988. Movement of an aqueous spray of Beauveria bassiana into the profile of four Georgia soils. Environ. Entomol. 17: 135–139.

    Google Scholar 

  • Thurston, G.S., H.K. Kaya, T.M. Burlando and R.E. Harrison, 1993. Milky disease bacterium as a stressor to increase susceptibility of scarabaeid larvae to an entomopathogenic nematode. J. Invertebr. Pathol. 61: 167–172.

    Google Scholar 

  • Thurston, G.S., H.K. Kaya and R. Gaugler, 1994. Characterizing the enhanced susceptibility of milky disease-infected scarabaeid grubs to entomopathogenic nematodes. Biol. Contr. 4: 67–73.

    Google Scholar 

  • Yokoyama, T.M. Hasegawa, A. Fujiie, M. Sawada and K. Noguchi, 1998. Microbial control of scarab beetle larvae by a formulation of Metarhizium anisopliae (Deuteromycotina: Hyphomycetes) in a sweet potato field. Appl. Entomol. Zool. 33: 215–218.

    Google Scholar 

  • Zimmerman, G., 1992. Use of the fungus, Beauveria brongniartii, for the control of European cockchafers, Melolontha spp., in Europe. In: T.A. Jackson and T.R. Glare (eds), Use of Pathogens in Scarab Pest Management. Intercept, Andover. pp. 199–208.

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Agricultural Biology, Gyeongsang National University, Chinju, Gyeongnam, 660-701, Republic of Korea; e-mail

    Ho Yul Choo, Jin Huh, Dong Woon Lee & Hyeong Hwan Kim

  2. Department of Nematology, University of California, Davis, CA, 95616, USA

    Harry K. Kaya

  3. Nambu Forestry Experiment Station, Chinju, Gyeongnam, 660-300, Republic of Korea

    Sang Myeong Lee

  4. Department of Applied Biological Science, College of Natural Resources and Life Science, Dong-A University, Pusan, 604-714, Republic of Korea

    Young Moo Choo

Authors
  1. Ho Yul Choo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Harry K. Kaya
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jin Huh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dong Woon Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hyeong Hwan Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Sang Myeong Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Young Moo Choo
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Choo, H.Y., Kaya, H.K., Huh, J. et al. Entomopathogenic nematodes (Steinernema spp. and Heterorhabditis bacteriophora) and a fungus Beauveria brongniartii for biological control of the white grubs, Ectinohoplia rufipes and Exomala orientalis, in Korean golf courses. BioControl 47, 177–192 (2002). https://doi.org/10.1023/A:1014559729607

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1014559729607

Search

Navigation