Management of Bemisia Resistance to Growth Regulator, Neonicotinoid, and Pyrethroid Insecticides
Cotton Incorporated Cary, North Carolina
Maricopa Agricultural Center
J. C. Palumbo
Yuma Valley Agricultural Center
Arizona produces cotton, melon, winter vegetable, and forage crops through the year. Whiteflies, Bemisia tabaci biotype B (a.k.a. B. argentifolii1), develop on many of these crops but can be severe pests of cotton, melons, and ornamentals. Spring and fall melons provide an excellent host for whitefly development and serve as a biological bridge for whitefly movement between summer cotton and winter crops. Throughout the world, whiteflies have developed resistance to many insecticides2. Following widespread whitefly problems in Arizona melons and vegetables in 1992, the neonicotinoid insecticide, imidacloprid, was registered for use. Though used intensively since 1993, imidacloprid continues to provide exceptional control of whiteflies in melons and vegetables, and successfully disrupts the year-round cycle of whitefly development3. However, whitefly problems in cotton persisted and by 1995, mixtures of pyrethroid and organophosphate insecticides met with widespread resistance4. The following year, The 1996 Whitefly Resistance Management Program for Arizona Cotton5 was implemented after the insect growth regulators (IGR), pyriproxyfen and buprofezin, were granted emergency exemptions in cotton for once per season use. Both IGRs have been pivotal in Arizona cotton’s successful whitefly control program since that time6. Pyriproxyfen use in Arizona cotton continues to be limited to once per year. However, its uses have been expanded to greenhouses and citrus. Buprofezin use in cotton has been limited (Fig. 1) , but new registrations include leafy greens, melons, and glasshouse tomatoes. At present, whitefly control in Arizona is satisfactory, but continues to be vulnerable to resistance. Changing patterns of insecticide use in our diverse cropping systems have increased the likelihood of future resistance problems. Foremost in this regard are: 1) more extensive use of imidacloprid, buprofezin, and pyriproxyfen; and 2) new registrations of neonicotinoid insecticides, including acetamiprid, and thiamethoxam. Avoiding resistance will require disciplined use of insecticides and harmonization of whitefly control recommendations across commodities7. In this poster we summarize data from statewide monitoring (Fig. 2) that chronicle seven years of successful management of whitefly resistance in Arizona cotton and highlight vulnerabilities regarding future resistance problems. We then report new cross-commodity guidelines that extend resistance management of whiteflies to the cropping system level.
Synergized Pyrethroid Insecticides
Use of synergized pyrethroid treatments declined dramatically in cotton after 1995 (Fig. 1) , due to decreased efficacy (Fig. 3) and the striking success of the IGRs8, 13-15. The 1996 resistance management program limited pyrethroids used against whiteflies in cotton to late in the season, and to no more than two treatments5. Resistance to synergized pyrethroids declined from 1995 until 2001 (Fig. 3) and use remained low. Regained efficacy of synergized pyrethroids, combined with their low cost, prompted their greater use in 2000 and 2001 (Fig. 1). Increases in the frequency of resistance to synergized pyrethroids resulted (Fig. 3) . Cotton fields with more than 20% of whiteflies surviving a diagnostic dose of fenpropathrin + acephate increased from 2 of 19 (11%) in 2001 to 6 of 12 (50%) in 2002. However, resistance frequencies statewide continued to be much lower than they were at the height of the 1995 crisis (Fig. 3) .
Pyriproxyfen is highly effective against whiteflies in Arizona cotton and currently is the insecticide that most producers elect to use9, 13-15 when whiteflies first exceed treatment thresholds (Fig. 1). However, previous experience in cotton in Israel indicated that pyriproxyfen had a relatively high risk of resistance development10. For this reason, pyriproxyfen use was limited to once per season in Arizona cotton. Statewide monitoring first detected pyriproxyfen-resistant whiteflies in 1999 (Fig. 4a) . Mean mortality in bioassays of field-collected populations exposed to pyriproxyfen concentrations of 0.01 and 0.1 ug/ml remained unchanged from 1996-98, but declined significantly thereafter (Fig. 4a) . The percentage of whiteflies surviving bioassays of 0.1 ug pyriproxyfen/ml varied from 0.0 to over 25% in 2002 (Fig. 4b) , depending on location. Furthermore, whiteflies collected in 2002 from cotton in Queen Creek, Arizona, and exposed to pyriproxyfen in the laboratory, yielded a strain with dramatically reduced susceptibility (Fig. 4c) . While pyriproxyfen remains effective against whiteflies in Arizona cotton, these findings underscore the importance of using it judiciously to delay resistance buildup.
Buprofezin use has been relatively limited in Arizona cotton since its introduction in 19969, 13-15. Fewer than 70 thousand acres have been treated annually; less than 30% of Arizona cotton (Fig. 1) . As with pyriproxyfen, the Arizona whitefly resistance management program promotes use of buprofezin when whitefly populations first exceed thresholds in the season, but limits use to one application per season. Despite the limited use, monitoring revealed statistically significant reductions from 1996 to 1998 in whitefly mortality observed in bioassays of 8.0 and 100 ug/ml buprofezin. However, this trend was not sustained in subsequent years (Fig. 5). Intensive exposure of field collections of whiteflies in the laboratory has not yielded substantial resistance (data not shown). Field efficacy of buprofezin remains high.
Imidacloprid has been used in Arizona since 1993, chiefly in melons, vegetables, and greenhouses. Although it is registered for use in cotton, it is seldom used on this crop, and then only as a foliar treatment. In melons, imidacloprid is soil-applied at planting, and provides 45-60 days of control11. Repeated foliar treatments and/or soil drenches are common in greenhouses. Susceptibility of whiteflies collected from different hosts in 1999 reflected these differences in exposure to imidacloprid (Fig. 6a ) . Greenhouse collections were the least susceptible, and cotton and fall melons the most susceptible to imidacloprid12. Statewide monitoring of whiteflies from cotton revealed a 4-year trend of declining mean susceptibility to imidacloprid from 1995-1998 (Fig. 6b) . However, this trend was reversed from 1999 to 2002. All whiteflies collected from Arizona cotton in 2002 were highly susceptible to imidacloprid (Fig. 6b) , as well as to two other important neonicotinoids, acetamiprid and thiamethoxam.
Cross-Commodity Coordination of Insecticide Use in Arizona
Management of whitefly resistance in Arizona could be undermined by poorly planned use of neonicotinoids, pyriproxyfen, or buprofezin. For this reason a major initiative was undertaken to expand to the cropping system level integrated resistance management strategies that have been so successful in cotton7. Agricultural producers, commodity group representatives, and chemical industry representatives joined university and government researchers and pest control advisors during each of the past four years to achieve this difficult task. Neonicotinoid insecticides were the focal point.
The goal is to avoid producer losses associated with whitefly resistance by sustaining the efficacy of neonicotinoid insecticides. This will be promoted by: 1) placing reasonable limitations on neonicotinoid use in the major crops affected by whiteflies, and 2) diversifying and harmonizing all insecticides used against whiteflies in the cropping system.
Defining Crop Communities
Communities were defined based on presence throughout the year of host crops that are economically impacted by whiteflies. Three distinct communities were identified in Arizona and recommendations were tailored for each: 1) multi-crop community, 2) cotton/melon community, and 3) cotton-intensive community.
Detailed recommendations for each crop community and their underlying rationale can be found in The University of Arizona Cooperative Extension bulletin, IPM Series No. 17. Fig. 7a illustrates guidelines for the multi-crop community. In this system neonicotinoid insecticides are not recommended for use in cotton, but are reserved for melons and vegetables7. Summary guidelines for neonicotinoid use in all three crop communities are detailed in Fig. 7b .
- Perring, T.M., A.D. Cooper, R.J. Rodriguez, C.A. Farrar, and T.S. Bellows. 1993. Identification of a whitefly species by genomic and behavioral studies. Science 259: 74-77.
- Denholm, I., M. Cahill, T.J. Dennehy, and A.R. Horowitz. 1998. Challenges with managing insecticide resistance in agricultural pests exemplified by the whitefly Bemisia tabaci. Phil. Trans. R. Soc. (Lond. B) 353(1376): 1757-1767.
- Palumbo, J.C., A.R. Horowitz, and N. Prabhaker. 2001. Insecticidal control and resistance management of Bemisa tabaci. In S.E. Naranjo and P.C. Ellsworth eds. Special Issue: Challenges and Opportunities for Pest Management of Bemisia tabaci in the New Century. Crop Protection 20(9): 739-765.
- Dennehy, T.J., and Livy Williams, III. 1997. Management of resistance in Bemisia in Arizona cotton. Pestic. Sci. 51: 398-406.
- Dennehy, T.J., P.C. Ellsworth, and R.L. Nichols. 1996. The 1996 whitefly resistance management program for Arizona cotton. University of Arizona IPM Series No. 8. 16 pp.
- Ellsworth, P.C., and J.L. Martinez-Carrillo. 2001. IPM for Bemisia tabaci: a case study from North America. In S.E. Naranjo and P.C. Ellsworth eds. Special Issue: Challenges and Opportunities for Pest Management in Bemisia tabaci in the New Century. Crop Protection 20(9): 853-869.
- Palumbo, J.C., P.C. Ellsworth, T.J. Dennehy, and R.L. Nichols. 2003. Cross-commodity guidelines for neonicotinoid insecticides in Arizona. IPM Series No. 17, Pub. AZ1319. Cooperative Extension, College of Agriculture and Life Sciences, University of Arizona, Tucson, AZ. 4 pp. URL: http://cals.arizona.edu/pubs/insects/az1319.pdf
- Ellsworth, P.C., T.J. Dennehy, and R.L. Nichols. 1996. Whitefly management in Arizona cotton – 1996. IPM Series No. 3. Cooperative Extension Publication #196004, College of Agriculture and Life Sciences, University of Arizona, Tucson, AZ. 2 pp. URL:http://cals.arizona.edu/crops/cotton/insects/wf/cibroch.html
- Agnew, G.K. and P.B. Baker. 2001. Pest and pesticide usage patterns in Arizona cotton. Proc. 2001 Beltwide Cotton Conferences. National Cotton Council, Memphis, TN. Pp. 1046-1054.
- Horowitz, A.R., S. Kontsedalov, I. Denholm, and I. Ishaaya. 2002. Dynamics of insecticide resistance in Bemisia tabaci: a case study with the insect growth regulator pyriproxyfen. Pest Management Sci. 58:1096-1100.
- Kerns, D.L. and J.C. Palumbo. 1995. Using Admire™ on desert vegetable crops. IMP Series No. 5. Cooperative Extension Publication #195017, College of Agriculture and Life Sciences, University of Arizona, Tucson, AZ. 2 pp. URL:http://cals.arizona.edu/crops/vegetables/insects/wf/admire.html
- Li, Y., T.J. Dennehy, X. Li, and M.E. Wigert. 2000. Susceptibility of Arizona whiteflies to chloronicotinyl insecticides and IGRs: new developments in the 1999 season. Proc. 2000 Beltwide Cotton Conferences. National Cotton Council, Memphis, TN. Pp. 1325-1332.
- Shanley, E.H. and P.B. Baker. 2002. 2001 update on pesticide use in Arizona cotton. Proc. 2002 Beltwide Cotton Conferences. National Cotton Council, Memphis, TN. 11 pp.
- Shanley, E.H. and P.B. Baker. 2003. Pesticide update in Arizona cotton for 2002. Proc. 2003 Beltwide Cotton Conferences. National Cotton Council, Memphis, TN. 12 pp.
- IGR use data for the period during which pyriproxyfen and buprofezin required full reporting, under the terms of the Section 18 exemption, were obtained from Dr. Edwin Minch, Arizona Department of Agriculture.