Abstract
We examined the toxicity of a fungicide, sulfur, to the egg parasitoid Anagrus erythroneurae (Hymenoptera: Mymaridae) Trjapitsyn and Chiapini and the vineyard leafhopper pest Erythroneura elegantula Osborn (Homoptera: Cicadellidae) and tested whether or not the use of sulfur in the field affects biological control of E. elegantula. Using field cage bioassays, we demonstrated that sulfur is toxic to adult A. erythroneurae parasitoids, but not toxic to adult E. elegantula leafhoppers. We nonetheless found in a field experiment that sulfur produced no changes in rates of parasitism or E. elegantula egg density, and generated only a very small increase in the density of E. elegantula nymphs. These results suggest that sulfur, although toxic to A. erythroneurae, is not highly disruptive of E. elegantula biological control in vineyards. Our results suggest that simple bioassays of acute toxicity may not accurately predict the impact of agricultural chemicals on biological control.
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Caboni P, Cabras M, Angioni A, Russo M, Cabras P (2002) Persistence of azadirachtin residues on olives after field treatment. J Agric Food Chem 50:3491–3494
Campbell CD, Walgenback JF, Kennedy GG (1991) Effects of parasitoids on lepidopterous pests in insecticide-treated and untreated tomatoes in western North Carolina. J Econ Entomol 84:1662–1667
Corbett A, Rosenheim JA (1996a) Impact of a natural enemy overwintering refuge and its interaction with the surrounding landscape. Ecol Entomol 21:155–164
Corbett A, Rosenheim JA (1996b) Quanitifying movement of a minute parasitoid, Anagrus epos (Hymenoptera: Mymaridae), using fluorescent dust marking and recapture. Biol Control 6:35–44
Costello MJ, Daane KM (1998) Arthropods. In: Ingels CA, Bugg RL, McGourty GT, Christensen LP (eds) Cover cropping in vineyards, a grower’s handbook, publication 3338. The Regents of the University of California, Division of Agriculture and Natural Resources, Oakland, California, pp 93–106
Cronin JT, Haynes KJ (2004) An invasive plant promotes unstable host-parasitoid patch dynamics. Ecology 85:2772–2782
Croft BA (1990) Arthropod biological control agents and pesticides. Wiley, New York
Delye C, Laigret F, CorioCostet MF (1997) New tools for studying epidemiology and resistance of grape powdery mildew to DMI fungicides. Pestic Sci 51:309–314
Doutt RL, Nakata J (1965) Overwintering refuge of Anagrus epos (Hymenoptera: Mymaridae). J Econ Entomol 58:586
Doutt RL, Nakata J (1973) The Rubus leafhopper and its egg parasitoid: An endemic biotic system useful in grape-pest management. Environ Entomol 2:381–386
Elzen GW (1989) Sublethal effects of pesticides on beneficial parasitoids. In: Jepson PC (eds) Pesticides and non-target invertebrates. Intercept Ltd, Wimborne, Dorset, pp 129–150
English-Loeb G, Rhainds M, Martinson TE, Ugine T (2003) Influence of flowering cover crops on Anagrus parasitoids (Hymenoptera: Mymaridae) and Erythroneura leafhoppers (Homoptera: Cicadellidae) in New York vineyards. Agric Entomol 5:173–181
Fauziah I (1990) Studies on the resistance to acylurea compounds in P. xylostella L. (Lepidoptera: Yponomeutidae). PhD Thesis, University of London, 259p
Flaherty DL, Wilson LT, Stern VM, Kido H (1985) Biological control in San Joaquin Valley vineyards. In: Herzog DC, Hoy MA (eds) Biological control of agricultural IPM systems. Wiley, New York, pp 501–520
Flaherty DL, Christensen PL, Lanini WT, Marois JJ, Phillips PA, Wilson LT (1992) Grape pest management 2nd edn. publication 3343. The Regents of the University of California, Division of Agriculture and Natural Resources, Oakland, California, pp 140–152
Hanna R, Zalom FG, Wilson LT, Leavitt GM (1997) Sulfur can suppress mite predators in vineyards. Calif Agric 51:19–21
James DG, Price TS, Wright LC, Perez J (2002) Abundance and phenology of mites, leafhoppers, and thrips on pesticide-treated and untreated wine grapes in southcentral Washington. J Agric Urban Entomol 19:45–54
Jepsen SJ, Rosenheim JA, Matthews CE (in press) The impact of sulfur on the reproductive success of Anagrus spp. parasitoids in the field. Biocontrol. DOI: 10.1007/s10526-006-9056-y
Kido H, Flaherty DL, Bosch D, Valero KA (1984) French prune trees as overwintering sites for the grape leafhopper egg parasite. Am J Enol Viticult 35:156–160
Martinson T, Williams L III, English-Loeb G (2001) Compatibility of chemical disease and insect management practices used in New York vineyards with biological control by Anagrus spp. (Hymenoptera: Mymaridae), parasitoids of Erythroneura Leafhoppers. Biol Control 22:227–234
Murphy BC, Rosenheim JA, Granett J (1996) Habitat diversification for improving biological control: abundance of Anagrus epos (Hymenoptera: Mymaridae) in grape vineyards. Environ Entomol 25:495–504
Murphy BC, Rosenheim JA, Dowell RV, Granett J (1998) Testing a habitat diversification tactic for improving biological control: parasitism of the western grape leafhopper, Erythroneura elegantula (Homoptera: Cicadellidae). Entomol Exp Appl 87:225–235
Nowbahari B, Thibout E (1992) Defensive role of allium sulfur-compounds for leek moth Acrolepiopsis assectella Z (Lepidoptera) against generalist predators. J Chem Ecol 18:1991–2002
Nichols CI, Parrella M, Altieri MA (2001) The effects of a vegetational corridor on the abundance and dispersal of insect biodiversity within a northern California organic vineyard. Landsc Ecol 16:33–146
Penman DR, Chapman RB, Bowie MH (1986) Direct toxicity and repellent activity of pyrethroids against Tetranychus urticae (Acari: Tetranychidae). J Econ Entomol 79:1183–1187
Prischmann DA, James DG, Wright LC, Teneyck RD, Snyder WE (2005) Effects of chlorpyrifos and sulfur on spider mites (Acari: Tetranychidae) and their natural enemies. Biol Control 33:324–334
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Robertson JL, Haverty MI (1981) Multiphase laboratory bioassays to select chemicals for field testing on western spruce budworm. J Econ Entomol 74:148–153
Robertson JL, Worner SP (1990) Population toxicology: suggestions for laboratory bioassays to predict pesticide efficacy. J Econ Entomol 83:8–12
Rosenheim JA, Hoy MA (1988) Sublethal effects of pesticides on the parasitoid Aphytis melinus (Hymenoptera: Aphelinidae). J Econ Entomol 81:476–483
SAS Institute (2000) JMP User’s Manual, Version 4.0.2. SAS Institute, Cary, NC
Settle WH, Wilson LT (1990) Invasion by the variegated leafhopper and biotic interactions: Parasitism, competition, and apparent competition. Ecology 71:1461–1470
Stark JD, Banks JE (2003) Population-level effects of pesticides and other toxicants on arthropods. Annu Rev Entomol 48:505–519
Teodoro AV, Fadini MAM, Lemos WP, Guedos RNC, Pallini A (2005) Lethal and sub-lethal selectivity of fenbutatin oxide and sulfur to the predator Iphiseiodes zuluagai (Acari: Phytoseiidae) and its prey, Oligonychus ilicis (Acari: Tetranychidae), in Brazilian coffee plantations. Exp Appl Acarol 36:61–70
Theiling KM, Croft BA (1988) Pesticide side-effects on arthropod natural enemies: a database summary. Agric Ecosyst Environ 21:191–218
Williams MD, Gill G (1996) Evaluation of pesticides for side effects on the leafhopper parasitoid Anagrus atomus with particular reference to protected crops. Annu Appl Biol Sci 128:98–99
Wright DJ, Verkerk RHJ (1995) Integration of chemical and biological control systems for arthropods: Evaluation in a multitrophic context. Pestic Sci 44:207–218
Acknowledgments
We thank Rand Schaal for the use of his vineyard and Mark Rubald for the use of the Village Homes vineyard. We would also like to thank Jeff Granett, Rick Karban and the members of the Rosenheim lab for helpful comments (Andy Zink, Jason Harmon, Ken Spence, and Maggie Sherriffs). Chris Matthews, Jill Hodgen, Katherine Chmiel, Matt Judd, Erin Duffy and Mike Kabler contributed greatly to the natural history observations. Doug Gubler’s advice on powdery mildew is appreciated. Wilbur Ellis, Syngenta and Bayer kindly donated fungicides for testing. This project was funded by a grant from the Viticulture Consortium: AVF-ROS 4588.
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Jepsen, S.J., Rosenheim, J.A. & Bench, M.E. The effect of sulfur on biological control of the grape leafhopper, Erythroneura elegantula, by the egg parasitoid Anagrus erythroneurae . BioControl 52, 721–732 (2007). https://doi.org/10.1007/s10526-006-9058-9
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DOI: https://doi.org/10.1007/s10526-006-9058-9