Biological Control 56 (2011) 98–105 Contents lists available at ScienceDirect Biological Control journal homepage: www.elsevier.com/locate/ybcon Evaluation of herbivore-induced plant volatiles for monitoring green lacewings in Washington apple orchards ⇑ Vincent P. Jones a, , Shawn A. Steffan a, Nik G. Wiman a, David R. Horton b, Eugene Miliczky b, Qing-He Zhang c, Callie C. Baker a a Department of Entomology, Tree Fruit Research and Extension Center, Washington State University, 1100 N. Western Ave., Wenatchee, WA 98801, United States b USDA-ARS, Yakima Agricultural Research Laboratory, 5230 Konnowac Pass Road, Wapato, WA 98951, United States c Sterling International Inc., 3808 N. Sullivan Rd., Bldg 16BV, Spokane, WA 99216-1630, United States article info abstract Article history: We evaluated five herbivore-induced plant volatiles plus a male-produced pheromone as attractants for Received 17 June 2010 adult green lacewings in Washington apple orchards in 2008. We found at least five attractants or com- Accepted 6 October 2010 binations of attractants were attractive to the three most abundant green lacewing species in our trials. Available online 14 October 2010 Chrysopa nigricornis and Chrysopa oculata were attracted to the combination of methyl salicylate and iridodial with iridodial alone being the second best attractant. Chrysoperla plorabunda was found in lower Keywords: numbers than C. nigricornis and C. oculata, but did exhibit a significant attraction to benzaldehyde. In HIPV mid-summer, we added the herbivore-induced plant volatile squalene to the study and found it to Squalene be exceedingly attractive, but only to male C. nigricornis. Whether alone or in combination, squalene Methyl salicylate Iridodial attracted 4–5-fold more C. nigricornis than any other compound tested. Our data have revealed Chrysopa nigricornis C. nigricornis to be an abundant orchard predator that can be readily monitored with squalene-baited Chrysopa oculata traps. Despite the obvious promise of HIPVs in biological control programs, we urge caution in their Chrysoperla plorabunda deployment as large-scale attractants, at least until further studies have investigated potential disruption of natural enemy population dynamics. Ó 2010 Elsevier Inc. All rights reserved. 1. Introduction 2008). Most studies have been preliminary steps towards field application, either by pairing a particular volatile (or mixture of While sex pheromone based monitoring programs for key pests them) with a trap to determine the types of natural enemies at- in agriculture or forest environments has been common for dec- tracted, or by testing individual HIPVs in small plots to evaluate ef- ades, the discovery and use of practical attractants for monitoring fects on natural enemy diversity and abundance (James, 2005; Lee, natural enemies has been a slower process that has focused on 2010). These approaches have been used to evaluate HIPVs as attr- plant volatiles induced by herbivore feeding (known as herbi- actants in hops (James, 2003a,b, 2005; James and Price, 2004), vore-induced plant volatiles or HIPVs). Most of these compounds grapes (James and Price, 2004), cotton (Williams et al., 2008; Yu were discovered by chemical ecologists who compared volatile et al., 2008), pear (Scutareanu et al., 1997), cherry (Toth et al., profiles released by herbivore-damaged plants to those of undam- 2009), corn and sorghum (Kahn et al., 2008), and strawberry (Lee, aged control plants; specific combinations of volatiles were then 2010). From these studies and others, it is apparent that green lace- assayed in behavioral studies to determine activity (Dicke et al., wings (Neuroptera: Chrysopidae) as a group respond to a large 2003; Turlings et al., 1998). The literature on HIPVs shows that number of HIPVs, but two attractants generally stand out in the re- the ecological roles and behavioral interactions mediated by them cent literature. The first is the HIPV methyl salicylate (MS), which is is considerably broader and more complex than those mediated by considered to be attractive to a wide range of other natural enemies sex pheromones alone (see reviews by Paré and Tumlinson (1999) (James, 2003a, 2005, 2006). The second compound is iridodial, and Vet and Dicke (1992)). which is a male-produced male aggregation pheromone for certain Studies of HIPVs in agricultural systems have recently increased lacewing species. Iridodial has been reported to attract (at various in number, with the goal of using them as tools to induce host plant levels) several lacewing species including Chrysopa oculata Say, resistance and/or to concentrate natural enemies in areas for pur- Chrysopa nigricornis Burmeister, Chrysopa coloradensis Banks, Chrysopa poses of biological control (Gurr and Kvedaras, 2010; Kahn et al., quandripunctanta Burmeister, and Chrysopa septempunctata Wesmael (Chauhan et al., 2007, 2004; Zhang et al., 2004, 2006a,b). ⇑ Corresponding author. Fax: +1 509 662 8714. Another powerful lacewing attractant was accidentally discov- E-mail address: [email protected] (V.P. Jones). ered in early summer 2007 when one of us (NGW) evaluated 1049-9644/$ - see front matter Ó 2010 Elsevier Inc. All rights reserved. doi:10.1016/j.biocontrol.2010.10.001 V.P. Jones et al. / Biological Control 56 (2011) 98–105 99 several HIPVs as possible attractants for adult tachinid parasitoids attractant on each wick at these rates: 0.5 ml per dispenser for of obliquebanded leafroller, Choristoneura rosaceana (Harris) (Lep- benzaldehyde; 4 mg for iridodial; and 2 ml for all other materials. idoptera: Tortricidae). In those evaluations, squalene-baited traps After the attractant was dispensed, the bag was heat-sealed at the were found to be highly attractive to the lacewing C. nigricornis open end. If combinations of attractants were to be used, the indi- (NGW, unpublished). The choice of squalene in this initial screen- vidual attractants were each placed in its own lure, and multiple ing was prompted by the work of Dutton et al. (2002, 2000), who lures were placed in each trap. We used white plastic delta traps showed that the chemical was released from golden delicious ap- (Trécé, Inc.; Adair, OK) to capture lacewings that approached the ples as the fruit was fed upon by the leafminer, Phyllonorycter lures. The final size of the attractant-containing section of the lure pomonella Zeller (Lepidoptera: Gracillariidae), and showed also lures; the 1.5 cm excess (i.e., unsealed) portion of the tubing was that the chemical attracted the leafminer parasitoid Pholetesor bi- used to attach the lure to the delta trap. Once constructed, lures color Ness (Hymenoptera: Braconidae). Squalene was provided to were stored in impermeable heat sealed metalized barrier pouches Curtiss (2008) (by NGW), who further evaluated it as an attractant (Associated Bag Company, Milwaukee, WI) and frozen at À20 °C in ecological studies of the movement of natural enemies into ap- until use. Control lures were constructed the same way, but in- ple and pear orchards. Curtiss’s studies showed the potential of the cluded distilled water in place of attractant. attractant as a monitoring tool and compared squalene to MS and a combination of MS + squalene. His results clearly showed that MS 2.2. Evaluation of lure release rates by itself had limited attraction for C. nigricornis compared to either squalene by itself or the combination of MS + squalene. Release rates for lures dispensing benzaldehyde, cis-3-hexene- Our studies were designed to evaluate several promising HIPVs, 1-ol, cis-3-hexenyl acetate, MS, squalene, and iridodial were the lacewing pheromone iridodial, and squalene as tools for mon- determined for 3–4 weeks under field conditions. Lures were itoring abundance, diversity, and phenology of lacewings in tree placed inside delta traps, and traps were placed in the canopy of fruits. This focus was chosen as a way to expand our understanding large (3.5–4.5 m tall) apple trees in an orchard at the Washington of the ecological role of the different natural enemy species and to State University Tree Fruit Research and Extension Center in enhance biological control through conservation and potentially Wenatchee, WA. Lures were periodically brought into the labora- spatial manipulation of natural enemy populations. tory, weighed with an Ohaus Pioneer analytical balance (0.1 mg accuracy) (Pine Brooke, NJ) and returned to the field. Tests were run during the early spring (16 May to 13 June), summer (30 July 2. Materials and methods to 27 August) and fall (3 October to 17 October) of 2008. We used four packets per lure/attractant combination and calculated aver- 2.1. Lure construction age weight loss per day over a period extending to 28 d. If cumula- tive weight loss of a lure leveled out before the full 28 d had We examined efficacy and release rates for six chemicals elapsed, we considered the lure to be depleted at the time the (Table 1). The products were selected on the basis of literature ac- change occurred. We used linear regression to determine the rela- counts suggesting that each might have some attractive properties tionship between cumulative weight loss and time; the slope of the to some natural enemies. Lures were constructed using 5 cm wide regression provides an estimate the mean daily release rate. The polyethylene tubing (PE) that were either 0.106 or 0.152 mm thick longevity of the lure was calculated by dividing the total attractant (Associated Bag Company, Milwaukee, WI). We examined two weight by the average weight loss per day. types of wicking material, either a 4 Â 4 cm piece of polyester felt (Kunin Group, Hampton, NH), or a single 3.8 cm long dental wick (large size – 12.5 mm dia.; Patterson Dental, St. Paul, MN). Wick 2.3. Long-term comparison of different attractants choice was based on the total volume of attractant needed for lure longevity; dental wicks provided a greater capacity to absorb attr- The 2008 field studies were conducted using a randomized actants than the felt material, but the felt provided a greater sur- block design with the lures tested, orchard locations, test dura- face area for release of volatiles at low volumes.