Current and potential use of pathogens in the management of turfgrass insects as affected by new pesticide regulations in North America

International Journal of Pest Management

Volumn 56, Issue 1, 2010, Pages 51-60

  Bélair, Guy ^a   Koppenhöfer, Albrecht M ^b   Dionne, Julie ^c   Simard, Louis ^a  

^a AGRICULTURE AND AGRI FOOD CANADA   (Canada)

^b RUTGERS UNIVERSITY   (United States)

^c Royal Canadian Golf Association   (Canada)

Author keywords

Anomala orientalis; Cyclocephala borealis; Entomopathogenic nematodes; Golf courses; Mole crickets; Pesticide regulations; Popillia japonica; Turfgrass; White grubs

Indexed keywords

ENTOMOLOGY; GOLF COURSE; GRASS; HEALTH RISK; INSECT; PATHOGEN; PATHOGENICITY; PEST CONTROL; PESTICIDE APPLICATION; REGULATORY FRAMEWORK; VIRULENCE;

CANADA; NORTH AMERICA;

ANOMALA ORIENTALIS; CYCLOCEPHALA BOREALIS; GRYLLOTALPIDAE; HEXAPODA; INSECTIVORA; NEMATODA; POACEAE; POPILLIA JAPONICA;

EID: 70949100513     PISSN: 09670874     EISSN: 13665863     Source Type: Journal    
DOI: 10.1080/09670870903076012     Document Type: Article

References (85)

1. 114957 Canada Ltee (Spraytech. Societe d'arrosage) v. Hudson (Town), 2 S.C.R.241, 2001 SCC 40.
2. Alm SR, Villani MG, Yeh T, Shutter R. 1997. Bacillus thuringiensis japonensis strain buibui for control of Japanese and oriental beetle larvae (Coleoptera: Scarabaeidae). Appl Entomol Zool. 32:477-484.
3. An R, Grewal PS. 2007. Differences in the virulence of Heterorhabditis bacteriophora and Steinernema scarabaei to three white grub species: the relative contribution of the nematodes and their symbiotic bacteria. Biol Control. 43:310-316.
4. Ansari MA, Shah FA, Tirry L, Moens M. 2006. Field trials against Hoplia philanthus (Coleoptera: Scarabaeidae) with a combination of an entomopathogenic nematode and the fungus Metarhizium anisopliae CLO 53. Biol Control. 39:453-459.
5. Ansari MA, Tirry L, Moens M. 2004. Interaction between Metarhizium anisopliae CLO 53 and entomopathogenic nematodes for the control of Hoplia philanthus. Biol Control. 31:172-180.
6. Asano A, Yamashita C, Iizuka T, Takeuchi K, Yamanaka S, Cerf D, Yamamoto T. 2003. A strain of Bacillus thuringiensis subsp. galleriae containing a novel cry8 gene highly toxic to Anomala cuprea (Coleoptera: Scarabaeidae). Biol Control. 28:191-196.
7. Bixby A, Alm SR, Power K, Grewal P, Swier SR. 2007. Susceptibility of four species of turfgrass-infesting scarabs (Coleoptera: Scarabaeidae) to Bacillus thuringiensis serovar japonensis strain buibui. J Econ Entomol. 100:1604-1610.
8. Bosch D, Schipper D, Van der Kleij H, de Maagd RA, Stiekema WJ. 1994. Recombinant Bacillus thuringiensis crystal proteins with new properties: possibilities for resistance management. Biotechnology 12:915-918.
9. Boughton AJ, Harrison RL, Lewis LC, Bonning BC. 1999. Characterization of a nuclearpolyhecroviurs from black cutworm, Agrostis ipsilon (Lepidoptera: Noctuidae). J Invertebr Pathol. 74:289-294.
10. Cappaert DC, Koppenhöfer AM. 2003. Steinernema scarabaei, an entomopathogenic nematode for control of the European chafer. Biol Control. 28:379-386.
11. Choo HY, Koppenhöfer AM, Kaya HK. 1996. Combination of two entomopathogenic nematode species for suppression of an insect pest. J Econ Entomol. 89:97-103.
12. Christie M. 2008. Private Property Pesticide By-laws In Canada. 2008. Ottawa (Ontario); [cited 2009 Jan 4]. Available from: http://www.flora.org/healthyottawa/ BylawList.pdf.
13. City of Toronto. Pesticide By-Law. 2005. Toronto (Ontario); [cited 2009 Jan 4]. Available from: http://www.toronto.ca/legdocs/municode/1184_612.pdf.
14. de Maagd RA, Weemen-Henriks M, Molthoff JW, Naimov S. 2003. Activity of wild type and hybrid Bacillus thuringiensis d-endotoxins against Agrotis ipsilon. Arch Microbiol. 179:363-367.
15. Dutky SR. 1963. The milky diseases. In: Steinhaus EA, editor. Insect pathology: an advanced treatise, Vol. 2. New York: Academic Press. p. 75-115.
16. Ehlers R-U, Gerwien A. 1993. Selection of entomopathogenic nematodes (Steinernematidae and Heterorhabditidae, Nematoda) for the biological control of cranefly larvae Tipula paludosa (Tipulidae, Diptera). Zeitschrift für Pflanzenkrankheiten und Pflanzenschutz. 100:343-353.
17. Enkerli J, Widmer F, Keller S. 2004. Long-term field persistence of Beauveria brongniartii strains applied as biocontrol agents against European cockchafer larvae in Switzerland. Biol Control. 29:115-123.
18. Feitelson JS, Quick TC, Gaertner F. 1990. Alternative hosts for Bacillus thuringiensis delta-endotoxins genes. In: Baker RR, Dunn PE, editors. New directions in biological control: alternatives for suppressing agricultural pests and diseases. New York: Wiley-Liss. p. 561-571.
19. Fleming WE. 1968. Biological control of the Japanese beetle. USDA Technical Bulletin 1383. U.S. Printing Office, Washington, DC.
20. Fleming WE, Ladd TL. 1979. Milky disease for control of Japanese beetle. U.S. Department of Agriculture Leaflet 500. U.S. Department of Agriculture, Washington, DC.
21. Foreign Affairs and International Trade Canada 2009. Dispute Settlement NAFTA -Chapter 11 - Investment, Dow AgroSciences LLC v. Government of Canada. 2008. Ottawa (Ontario); [cited 2009 Jan 4]. Available from: http://www.international.gc.ca/trade-agreements-accords-commerciaux/disp-diff/agrosciences_archive.aspx?lang1/4eng.
22. Garczynski SF, Siegel JP. 2007. Bacteria. In: Lacey LA, Kaya HK, editors. Field manual of techniques in invertebrate pathology; 2nd ed. Dordrecht: Kluwer Academic Publisher. p. 175-197.
23. Georgis R, Koppenhöfer AM, Lacey LA, Bélair G, Duncan LW, Grewal PS, Samish M, Tan L, Torr P, van Tol RWHM. 2006. Successesand failures in the use ofparasitic nematodes for pest control. Biol Control. 37:103-123.
24. Georgis R, Poinar GO, Jr. 1994. Nematodes as bioinsecticides in turf and ornamentals. In: Leslie A, editor. Integrated pest management for turf and ornamentals. Boca Raton (FL): CRC Press. p. 477-489.
25. Gosselin ME, Bélair G, Simard L, Brodeur J. 2009. Toxicity of spinosad and Beauveria bassiana to the black cutworm, and the additivity of sub-letal doses. Biocontrol Sci Techn. 19:195-210.
26. Government of Ontario 2009. Ontario regulation 63/09. Toronto (Ontario); [cited 2009 Jan 4]. Available from: http://www.e-laws.gov.on.ca/html/source/regs/english/2009/elaws_src_regs_r09063_e.htm.
27. Grewal PS, Koppenhöfer AM, Choo HY. 2005. Lawn, turfgrass and pasture applications. In: Grewal PS, Ehlers R-U, Shapiro-Ilan DI, editors. Nematodes as biocontrol agents. Wallingford, UK: CABI Publishing. p. 115-146.
28. Grewal PS, Power KT, Grewal SK, Suggars A, Haupricht S. 2004. Enhanced consistency in biological control of white grubs (Coleoptera: Scarabaeidae) with new strains of entomopathogenic nematodes. Biol Control. 30:73-82.
29. Health Canada 2008. Reduced-Risk Update: Update on Reduced-Risk Pesticides in Canada. Ottawa (Ontario); [cited 2009 Jan 4]. Available from: http://www.hc-sc.gc.ca/cps-spc/pubs/pest/_decisions/rr2008-01/index-eng.php.
30. Jackson TA, Huger AM, Glare TR. 1993. Pathology of amber disease in the New Zealand grass grub Costelytra zealandica (Coleoptera: Scarabaeidae). J Invertebr Pathol. 61:123-130.
31. Jackson TA, Pearson JF, O'Callaghan MO, Mahanty HK, Willocks MJ. 1992. Pathogen to product-development of Serratia entomophila (Enterobacteriaceae) as a commercial biological control agent for the New Zealand Grass grub (Costelytra zealandica). In: Jackson TA, Glare TR, editors. Use of pathogens in scarab pest management. Andover (UK): Intercept Ltd. p. 191-198.
32. Keller S. 2000. Use of Beauveria brongniartii and its acceptance by farmers. IOBC/WPRS Bull. 23:67-71.
33. Kinoshita M, Yamanaka S. 1998. Development and prevalence of entomopathogenic nematodes in Japan. Jpn J Nematol. 28:42-45.
34. Klein MG. 1990. Efficacy against soil-inhabiting insect pests. In: Gaugler R, Kaya HK, editors. Entomopathogenic nematodes in biological control. Boca Raton (FL): CRC Press. p. 195-214.
35. Klein MG. 1992. Use of Bacillus popilliae in Japanese beetle control. In: Glare TR, Jackson TA, editors. Use of pathogens in scarab pest management. Andover(UK):Intercept. p. 179-189.
36. Klein MG. 1993. Biological control of scarabs with entomopathogenic nematodes. In: Bedding R, Akhurst R, Kaya H, editors. Nematodes and the biological control of insect pests. East Melbourne, Australia: CSIRO Press. p. 49-58.
37. Klein MG. 1995. Microbial control of turfgrass insects. In: Brandenburg RL, Villani MG, editors. Handbook of turfgrass insect pests. Lanham (MD): Entomological Society of America. p. 95-100.
38. Koppenhöfer AM, Baur ME, Kaya HK. 1996. Competition between two steinernematid nematode species for an insect host at different soil depths. J Parasitol. 82:34-40.
39. Koppenhöfer AM, Brown IM, Gaugler R, Grewal PS, Kaya HK, Klein MG. 2000a. Synergism of entomopathogenic nematodes and imidacloprid against white grubs: greenhouse and field evaluation. Biol Control. 19:245-251.
40. Koppenhöfer AM, Choo HY, Kaya HK, Lee DW, Gelernter WD. 1999. Increased field and greenhouse efficacy against scarab grubs with a combination of an entomopathogenic nematode and Bacillus thuringiensis. Biol Control. 14:37-44.
41. Koppenhöfer AM, Cowles RS, Cowles EA, Fuzy EM, Baumgartner L. 2002. Comparison of neonicotinoid insecticides as synergists for entomopathogenic nematodes. Biol Control. 24:90-97.
42. Koppenhöfer AM, Fuzy EM. 2003a. Steinernema scarabaei for the control of white grubs. Biol Control. 28:47-59.
43. Koppenhöfer AM, Fuzy EM. 2003b. Biological and chemical control of the Asiatic garden beetle, Maladera castanea (Coleoptera: Scarabaeidae). J Econ Entomol. 96:1076-1082.
44. Koppenhöfer AM, Fuzy EM. 2004. Effect of white grub developmental stage on susceptibility to entomopathogenic nematodes. J Econ Entomol. 97:1842-1849.
45. Koppenhöfer AM, Fuzy EM. 2008a. Early timing and new combinations to increase the efficacy of neonicotinoidentomopathogenic nematode (Rhabditida: Heterorhabditidae) combinations against white grubs (Coleoptera: Scarabaeidae). Pest Manag Sci. 64:725-735.
46. Koppenhöfer AM, Fuzy EM. 2008b. Effect of the anthranilic diamide insecticide, chlorantraniliprole, on Heterorhabditis bacteriophora (Rhabditida: Heterorhabditidae) efficacy against white grubs (Coleoptera: Scarabaeidae). Biol Control. 45:93-102.
47. Koppenhöfer AM, Fuzy EM, Crocker R, Gelernter W, Polavarapu S. 2004. Pathogenicity of Steinernema scarabaei, Heterorhabditis bacteriophora and S. glaseri to twelve white grub species. Biocontrol Sci Techn. 14:87-92.
48. Koppenhöfer AM, Grewal PS, Fuzy EM. 2006. Virulence of the entomopathogenic nematodes Heterorhabditis bacteriophora, H. zealandica, and Steinernema scarabaei against five white grub species (Coleoptera: Scarabaeidae) of economic importance in turfgrass in North America. Biol Control. 38:397-404.
49. Koppenhöfer AM, Grewal PS, Kaya HK. 2000b. Synergism of imidacloprid and entomopathogenic nematodes against white grubs: the mechanism. Entomol Exp Appl. 94:283-293.
50. Koppenhöfer AM, Kaya HK. 1996. Coexistence of two steinernematid nematode species (Rhabditida: Steinernematidae) in the presence of two host species. Appl Soil Ecol. 4:221-230.
51. Koppenhöfer AM, Kaya HK. 1997. Additive and synergistic interaction between entomopathogenic nematodes and Bacillus thuringiensis for scarab grub control. Biol Control. 8:131-137.
52. Koppenhöfer AM, Kaya HK. 1998. Synergism of imidacloprid and an entomopathogenic nematode: a novel approach to white grub (Coleoptera: Scarabaeidae) control in turfgrass. J Econ Entomol. 91:618-623.
53. Koppenhöfer AM, Wilson MG, Brown I, Kaya HK, Gaugler R. 2000c. Biological control agents for white grubs (Coleoptera: Scarabaeidae) in anticipation of the establishment of the Japanese beetle in California. J Econ Entomol. 93:71-80.
54. Kunkel BA, Held DW, Potter DA. 1999. Impact of halofenozide, imidacloprid, and bendiocarb on beneficial invertebrates and predatory activity in turfgrass. J Econ Entomol. 92:922-930.
55. Kunkel BA, Held DW, Potter DA. 2001. Lethal and sublethal effects of bendiocarb, halofenozide, and imidacloprid on Harpalus pennsylvanicus (Coleoptera: Carabidae) following different modes of exposure in turfgrass. J Econ Entomol. 94:60-67.
56. Lee DW, Choo HY, Kaya HK, Lee SM, Smitley DR, Shin HK, Park CG. 2002. Laboratory and field evaluation of Korean entomopathogenic nematode isolates against the oriental beetle Exomala orientalis (Coleoptera: Scarabaeidae). J Econ Entomol. 95:918-926.
57. Mannion CM, Winkler HE, Shapiro DI, Gibb T. 2000. Interaction between halofenozide and entomopathogenic nematode Heterorhabditis marelatus for control of Japanese beetle (Coleoptera: Scarabaeidae) larvae. J Econ Entomol. 93:48-53.
58. McGraw BA, Koppenhöfer AM. 2008. Evaluation of two endemicandfivecommercialentomopathogenicnematode species (Rhabditida: Heterorhabditidae and Steinernematidae) against annual bluegrass weevil (Coleoptera: Curculionidae) larvae and adults. Biol Control. 46:467-475.
59. Ministère du développement durable, de l'environnement et des parcs du Québec. 2005. Code de gestion des pesticides. Québec (Québec); [cited 2009 Jan 4]. Available from: http://www.mddep.gouv.qc.ca/pesticides/permis/code-gestion/index.htm.
60. Moscardi F. 1999. Assessment of the application of baculoviruses for control of Lepidoptera. Annu Rev Entomol. 44:257-289.
61. Oestergaard J, Belau C, Strauch O, Ester A, van Rozen K, Ehlers R-U. 2006. Biological control of Tipula paludosa (Diptera: Nematocera) using entomopathogenic nematodes (Steinernema spp.) and Bacillus thuringiensis supsp. israelensis. Biol Control. 39:525-531.
62. Parkman JP, Smart GC, Jr. 1996. Entomopathogenic nematodes, a case study: introduction of Steinernema scapterisci in Florida. Biocontrol Sci Techn. 6:413-419.
63. Peters A, Ehlers R-U. 1994. Susceptibility of leatherjackets (Tipula paludosa and T. oleracea; Tipulidae: Nematocera) to the entomopathogenic nematode Steinernema feltiae. J Invertebr Pathol. 63:163-171.
64. Power KT, An R, Grewal PS. 2009. Effectiveness of Heterorhabditis bacteriophora strain GPS11 applications targeted against different instars of the Japanese beetle Popillia japonica. Biol Control. 48:232-236.
65. Prater CA, Redmond CT, Barney W, Bonning BC, Potter DA. 2006. Microbial control of black cutworm (Lepidoptera: Noctuidae) in turfgrass by using Agrotis ipsilon Multiple Nucleopolyhedrovirus. J Econ Entomol. 99: 1129-1137.
66. Racke KD. 2000. Pesticides for turfgrass management: uses and environmental issues. In: Clark JM, Kenna MP, editors. Fate and management of turfgrass chemicals, ASC Symposium Series 743, American Chemical Society, Washington (DC). p. 45-64.
67. Redmond CT, Potter DA. 1995. Lack of efficacy of in vivo-and putatively in vitro-produced Bacillus popilliae against field populations of Japanese beetle (Coleoptera: Scarabaeidae) grubs in Kentucky. J Econ Entomol. 88:846-854.
68. Rosa JS, Simões N. 2004. Evaluation of twenty-eight strains of Heterorhabditis bacteriophora isolated in Azores for biological control of the armyworm, Pseudaletia unipunctata (Lepidoptera: Noctuidae). Biol Control. 29:409-417.
69. Sharpe ES, Detroy RW. 1979. Fat body depletion, a debilitating result of milky disease in Japanese beetle larvae. J Invertebr Pathol. 34:92-94.
70. Simard L, Bélair G, Brodeur J. 2001. Susceptibility of the European chafer (Coleoptera: Scarabaeidae) to entomopathogenic nematodes (Rhabditida: Steinernematidae, Heterorhabditidae). Suppl J Nematol. 33:297-301.
71. Simard L, Bélair G, Brodeur J. 2002. Susceptibility of cranberry girdler to entomopathogenic nematodes. Can Entomol. 134:329-330.
72. Simard L, Bélair G, Gosselin ME, Dionne J. 2006. Virulence of entomopathogenic nematodes (Rhabditida: Steinernematidae, Heterorhabditidae) against Tipula paludosa (Diptera: Tipulidae), a turfgrass pest on golf courses. Biocontrol Sci Techn. 16:789-801.
73. Smith KA. 1994. Control of weevils with entomopathogenic nematodes. In: Smith KA, Hatsukade M, editors. Control of insect pests with entomopathogenic nematodes. Food and Fertilizer Technology Center, Republic of China in Taiwan. p. 1-13.
74. Smits PH, Vlug HJ, Wiegers GL. 1993. Biological control of leatherjackets with Bacillus thuringiensis. Proc Exp Appl Entomol, N.E.V. Amsterdam 4:187-192.
75. Suzuki N, Hori H, Tachibana M, Asano S. 1994. Bacillus thuringiensis strain Buibui for control of cupreous chafer, Anomala cuprea (Coleoptera: Scarabaeidae), in turfgrass and sweet potato. Biol Control. 4:361-365.
76. Swier SR, Rollins A, Carney B. 1997. Control of black cutworm on a bentgrass nursery, 1996. Arthropod Manage Tests 22:354.
77. Tanada Y, Kaya HK. 1993. Insect pathology. San Diego (CA): Academic Press.
78. The Food Quality Protection Act (FQPA) 1996. United States Environmental Proctection Agency, Office of Pesticide Research. [cited 2009 Jan 4]. Available from: http://www.epa.gov/pesticides/regulating/laws/fqpa/.
79. Thurston G, Kaya HK, Gaugler R. 1994. Characterizing the enhanced susceptibility of milky disease-infected scarabaeid grubs to entomopathogenic nematodes. Biol Control. 4:67-73.
80. Thurston GS, Kaya HK, Burlando TM, Harrison RE. 1993. Milky disease bacterium as a stressor to increase susceptibility of scarabaeid larvae to an entomopathogenic nematode. J Invertebr Pathol. 61:167-172.
81. Villani MG, Allee LL, Preston-Wilsey L, Consolie N, Xia Y, Brandenburg RL. 2002. Use of radiography and tunnel castings for observing mole cricket (Orthoptera: Gryllotalpidae) behavior in soil. Am Entomol. 48:42-50.
82. Villani MG, Krueger SR, Schroeder PC, Consolie F, Consolie NH, Preston-Wilsey LM, Roberts DW. 1994. Soil application effects of Metarhizium anisopliae on Japanese beetle (Coleoptera: Scarabaeidae) behavior and survival in turfgrass microcosms. Environ Entomol. 23: 502-513.
83. Vittum PJ, Luce NJ, Brocklesby LJ. 2007. Field efficacy of several insecticides applied curatively against first generation annual bluegrass weevil, golf course fairway, 2006. Arthropod Manage Tests 32:G27.
84. Yu SJ. 2008. The toxicology and biochemistry of insecticides. Boca Raton (FL): CRC Press.
85. Zhang J, Hodgman TC, Krieger L, Schnetter W, Schairer HU. 1997. Cloning and analysis of the first cry gene from Bacillus popilliae. J Bacteriol. 179:4336-4341.