Pest Management Science Pest Manag Sci 61:555–566 (2005 ) DOI: 10.1002/ps.1030 Conservation of natural enemies in cotton: comparative selectivity of acetamiprid in the management of Bemisia tabaci†‡ Steven E Naranjo∗ and David H Akey USDA-ARS, Western Cotton Research Laboratory, 4135 East Broadway Road, Phoenix, AZ 85040, USA Abstract: The integrated control concept emphasizes the importance of both chemical and biological control for pest suppression in agricultural systems. A two-year field study was conducted to evaluate the selectivity of acetamiprid for the control of Bemisia tabaci (Gennadius) in cotton compared with a proven selective regime based on the insect growth regulators (IGRs) pyriproxyfen and buprofezin. Acetamiprid was highly effective in controlling all stages of B tabaci compared with an untreated control, and generally produced lower pest densities than the IGR regime. Univariate analyses indicated that nine of 17 taxa of arthropod predators were significantly depressed with the use of acetamiprid compared with an untreated control, including common species such as Geocoris punctipes (Say), Orius tristicolor (White), Chrysoperla carnea Stephens sensu lato, Collops vittatus (Say), Hippodamia convergens Guerin-´ Meneville,´ and Drapetis nr divergens. Compared with results from independent, concurrent studies using mixtures of broad-spectrum insecticides at the same research site, acetamiprid depressed populations of fewer predator taxa; but, for eight predator taxa significantly affected by both regimes, the average population reduction was roughly equal. In contrast, only four taxa were significantly reduced in the IGR regime compared with the untreated control and three of these were omnivores that function primarily as plant pests. Principal response curves analyses (a time-dependent, multivariate ordination method) confirmed these patterns of population change for the entire predator community. Predator:prey ratios generally increased with the use of both IGRs and acetamiprid compared with an untreated control, but ratios were consistently higher with IGRs. Parasitism by aphelinid parasitoids was unaffected or depressed slightly in all insecticide regimes compared with the control. Because of its high efficacy, acetamiprid may play an important role in later stages of B tabaci control where less emphasis is placed on selectivity. However, our results suggest that acetamiprid would be a poor substitute for the currently used IGRs in the initial stage of control where insecticide selectivity is crucial to a functional integrated control program for B tabaci in cotton. Published in 2005 for SCI by John Wiley & Sons, Ltd. Keywords: Bemisia argentifolii; arthropod predators; aphelinid parasitoids; insect growth regulators; integrated control; principal response curves 1 INTRODUCTION biological control for pest suppression in agricultural Many factors may cause agricultural environments systems. A fundamental tenet of this approach is the to be unsuitable for insect biological control agents, application of insecticides only as needed, coupled including adverse climate, scarcity of required nutri- with the use of selective materials and/or selective ents, competition, intraguild predation, physical and application methods that minimize disruption of the chemical properties of the crop plant, lack of shelter natural enemy community.3,4 and breeding sites, and perhaps most importantly, the The sweetpotato whitefly, Bemisia tabaci (Genna- indiscriminate use of insecticides.1,2 None the less, dius) Biotype B (=BargentifoliiBellows & Perring) is insecticides have had and continue to play a critical a pest of world-wide significance causing damage to role in pest control in many crops. Over forty years ago, many field and horticultural crops.5 In the southwest- Stern et al3 formalized the integrated control concept ern USA this insect has been a been a key pest of cotton that emphasized the importance of both chemical and and vegetable crops since the early 1990s. Historically, ∗ Correspondence to: Steven E Naranjo, USDA-ARS, Western Cotton Research Laboratory, 4135 E Broadway Rd, Phoenix, AZ 85040, USA E-mail: [email protected] †This article presents the results of research only. Mention of a proprietary product does not constitute endorsement or recommendation for its use by USDA ‡This article is a US Government work and is in the public domain in the USA Contract/grant sponsor: Rhone-Poulenc Ag Company, Durham, NC, USA (Received 19 April 2004; revised version received 5 November 2004; accepted 8 November 2004) Published online 15 February 2005 Published in 2005 for SCI by John Wiley & Sons, Ltd. 555 SE Naranjo, DH Akey B tabaci has been difficult to control with insecticides6 which both foliar and systemic application method and has developed resistance to many insecticide have been shown to be generally toxic22– 26 to several classes.7 Much of the early effort in developing control insect predators and parasitoids in laboratory and strategies for B tabaci in the southern tier of the USA field residual bioassays. The few laboratory and field has focused on screening new and existing compounds residual bioassay studies that have addressed the non- for efficacy.8,9 Subsequent research defined action target effects of acetamiprid suggest that it is toxic thresholds for using mixtures of pyrethroids with car- to some natural enemies,23,26– 29 but relatively non- bamates or organophosphates,10,11 but over-reliance toxic to others.30,31 These findings suggest that effects on these compounds led to reduced susceptibility to are species- and system-dependent and in need of pyrethroids in central Arizona by 1995.9,12 In 1996, further investigation. To our knowledge, no studies two insect growth regulators (IGRs), buprofezin and have examined the effects of acetamiprid on natural pyriproxyfen, were approved for use in Arizona under enemies under field conditions using threshold-based an emergency registration (United States Environmen- decision guidelines for insecticide application. tal Protection Agency (US-EPA), Section 18) and the Controlled field studies were conducted in 1997 use of these now fully registered compounds forms and 1998 to examine the comparative efficacy and the foundation of current recommendations for white- selectivity of acetamiprid for control of B tabaci fly and insecticide resistance management in Arizona in Arizona cotton relative to a known efficacious and California.13,14 This strategy relies on threshold- and selective insecticide regime based on the initial based applications of insecticides in three sequential use of pyriproxyfen and buprofezin. In this paper stages beginning with selective IGRs (Stage I) followed we compare the suppression of B tabaci,the by non-pyrethroid mixtures (Stage II) and finally abundance of arthropod predators, predator:ratios, pyrethroid mixtures (Stage III) near the end of the and parasitism by aphelinid parasitoids between growing season. Stage II insecticides were primarily management strategies using acetamiprid and IGRs. selected to enhance preservation of pyrethroid activ- ity against B tabaci and less emphasis was placed on selectivity. Because of the high efficacy and selectivity 2 MATERIALS AND METHODS of the IGRs,15,16 this strategy ensures that the activity 2.1 Study site and experimental design of natural enemies, primarily arthropod predators, is All studies were conducted at the University of maximized during a substantial portion of the growing Arizona, Maricopa Agricultural Center, Maricopa, season. Since the introduction of this strategy in 1996, AZ,USA.Cotton,Gossypium hirsutum L (cv Deltapine insecticide use in Arizona cotton has declined nearly 5415 in 1997, Deltapine NuCOTN 33B in 1998), was 85% from 1995 to 1999.17 The use of these IGRs planted in early to mid-April each year, and grown along with transgenic Bt cotton has enabled a truly according to standard agronomic practices for the integrated control system for B tabaci on cotton. area. None the less, even though the IGRs are generally Similar experimental designs were used in both limited to a single use each during the cotton years and consisted of a randomized complete block growing season,14 resistance to these compounds has replicated six times in 1997 and four times in 1998. been observed in other parts of the world18,19 and Individual plots were 12 rows (1 m centers) by the proactive development of alternative insecticide 18.3 m long in 1997 and 12 rows (1 m centers) by regimes is warranted. In the past 10–15 years several 33.2 m long in 1998. In 1997 treatments consisted of new chemistries with novel modes of action, aside from acetamiprid 700 g kg−1 WP (NI-25, Rhone-Poulenc, the IGRs, have been introduced for whitefly control, Research Triangle Park, NC) at 56 and 84 g active the most significant of these being the neonicotinoids.9 ingredient (AI) ha−1, a commercial standard consisting The neonicotinoids, primarily imidacloprid, have seen of the initial use of insect growth regulators (IGRs), widespread use in vegetables and several products and an untreated control. One additional treatment are registered for use in cotton. In general, the (acetamiprid at 112 g AI ha−1) was added in 1998. neonicotinoids are considered to have a relatively All insecticide applications were made on the basis broad spectrum of activity, although non-target of weekly insect sampling (see Section 2.2). For exposure is thought to be minimized somewhat acetamiprid applications an action threshold of five