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Male-Produced Pheromone of the Green Lacewing, Chrysopa Nigricornis

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Male-Produced Pheromone of the Green Lacewing, Chrysopa Nigricornis J Chem Ecol (2006) 32: 2163–2176 DOI 10.1007/s10886-006-9137-5 Male-Produced Pheromone of the Green Lacewing, Chrysopa nigricornis Qing-He Zhang & Rodney G. Schneidmiller & Doreen R. Hoover & Kevin Young & Dewayne O. Welshons & Armenak Margaryan & Jeffrey R. Aldrich & Kamlesh R. Chauhan Received: 26 January 2006 / Revised: 26 May 2006 / Accepted: 27 May 2006 /Published online: 13 September 2006 # Springer Science + Business Media, Inc. 2006 Abstract Gas chromatographic–electroantennographic detection (GC–EAD) analysis showed that male antennae of the green lacewing, Chrysopa nigricornis Burmeister, the most common lacewing species in the U.S. Pacific Northwest, consistently responded to two compounds in thoracic extracts of conspecific males: 1-tridecene and (1R,2S,5R,8R)- iridodial. These compounds were not detected in extracts of the abdominal cuticle, and no other antennally active compounds were found in the abdominal samples. In field-trapping experiments, traps baited with iridodial significantly attracted large numbers of C. nigricornis males (both western and eastern forms) during summer and early fall, plus a few individuals of conspecific females only in early fall. Iridodial also attracted males of the goldeneyed lacewing, C. oculata Say, and, to a lesser extent, C. coloradensis Banks males. Methyl salicylate (MS), reported as an attractant for both sexes of C. nigricornis and C. oculata, was inactive by itself at the concentration tested in our study, but in a few instances slightly enhanced the responses of Chrysopa spp. to iridodial. However, MS alone and its binary blend with iridodial seemed to attract the hoverfly, Metasyrphus americanus (Weidemann). 2-Phenylethanol, a reported attractant for another lacewing, Chrysoperla plorabunda (Fitch) [= carnea (Say)], did not capture any lacewings. Our assays indicated that the lacewing pheromone, iridodial, loaded onto either rubber septa or as a binary blend with MS in polyethylene bags could last at least 5 wk in the field during the summer season. Q.-H. Zhang (*) : R. G. Schneidmiller : D. R. Hoover : K. Young : D. O. Welshons : A. Margaryan Sterling International, Inc., 3808 North Sullivan Road, Building 16BV, Spokane, WA 99216, USA e-mail: [email protected] J. R. Aldrich : K. R. Chauhan USDA-ARS Chemicals Affecting Insect Behavior Laboratory, BARC-West, B-007, 10300 Baltimore Avenue, Beltsville, MD 20705, USA 2164 J Chem Ecol (2006) 32: 2163–2176 Based on this study, a new attractant system for green lacewings is being developed for both domestic and international markets. Keywords Hoverfly . Attractant . Pheromone . Iridodial . Methyl salicylate . 2-phenylethanol . Nepetalactone . Nepetalactol . 1-tridecene . GC–EAD . Field flight behavioral assay Introduction Lacewings (Chrysopidae) are important predators of aphids and other soft-bodied insects (New, 1975; Tauber et al., 2000). Furthermore, because of their commercial availability and resistance to insecticides, green lacewings are also among the most commonly released predators for augmentative biological control (Ridgway and Murphy, 1984; Tulisalo, 1984; Aldrich, 1999). However, methods are still needed to retain the predators near augmentation sites and/or to attract wild predators to target areas (Baker et al., 2003). Lacewings are attracted to semiochemicals from different trophic levels, including host plant volatiles (Flint et al., 1979; Zhu et al., 1999, 2005; Hooper et al., 2002); herbivore- induced plant volatiles, such as methyl salicylate (MS; James, 2003a,b, 2006; James and Price, 2004); and sex pheromones of scale insects (Mendel et al., 2003) and aphids (Boo et al., 1998, 2003; Hooper et al., 2002). In particular, some lacewings are attracted to certain isomers of nepetalactone and nepetalactol, which are components of aphid pheromones and are also found in the catnip plant (Lamiaceae: Nepeta cataria L.; McElvain et al., 1941). Recently, we identified a male-produced pheromone from the goldeneyed lacewing, Chrysopa oculata Say, the first pheromone for any lacewing (Zhang et al., 2004). The synthetic pheromone, (1R,2S,5R,8R)-iridodial (IRI; Chauhan et al., 2004), outperformed all other reported attractants for the green lacewings in the genus Chrysopa, and has potential for manipulating lacewings for pesticide-free control of garden and agricultural pest insects (Zhang et al., 2004). Chrysopa nigricornis Burmeister is a large green lacewing distributed throughout the United States (Agnew et al., 1981). Similar to C. oculata, both the adults and larvae are predacious. It is the most common green lacewing species in the U.S. Pacific Northwest and is a useful component of integrated pest management programs in tree and vine crops such as hops (James, 2003a). To develop a pheromone-based attractant for this beneficial insect, we carried out a series of experiments in 2004 that focused on (1) pheromone production and perception in C. nigricornis with gas chromatographic–electroantenno- graphic detection (GC–EAD) and gas chromatographic (GC)–mass spectrometric analyses; (2) field testing the newly identified pheromone and other known lacewing semiochemicals, such as MS, Z,E-nepetalactone (ZE-lactone), Z,E-nepetalactol (ZE-lactol), 2-phenylethanol (2PE), and various combinations of these compounds in garden and orchard environments; and (3) dispenser technology, including dispenser types and the duration of attraction. Methods and Materials Adult Insects and Preparation of Extracts Adult lacewings for GC–EAD and GC–mass spectrometric analyses were collected during summer 2004 from either sticky Delta traps or nonsticky grapefruit-shaped plastic traps in J Chem Ecol (2006) 32: 2163–2176 2165 Spokane, WA. Lacewings recovered quickly from sticky surfaces of the traps and were still viable for EAD recordings. C. nigricornis, C. oculata, C. coloradensis Banks, and the common green lacewing, Chrysoperla plorabunda (Fitch; = carnea) were collected for EAD recordings, but only male C. nigricornis were collected from nonsticky traps for dissection and GC–mass spectrometer. Adults of these lacewings were processed within 6 to 20 hr of capture for GC–EAD and GC–mass spectrometric analyses. Adult male C. nigricornis were anesthetized with CO2, eviscerated under tap water, and their thoracic cuticle was separated from their abdominal cuticle so that each body portion could be extracted individually in 50 μl of methyl tert-butyl ether. No head extracts were made because no glands had been previously reported from the heads of lacewings. All extracts were kept at −20°C until they were analyzed. Gas Chromatographic–EAD and GC–Mass Spectrometric Analyses Lacewing extracts and chemical standards were analyzed in splitless mode with a Varian CP-3800 GC equipped with a polar column (CP-Wax 52CB; 1.0 μm film thickness, 30 m × 0.53 mm i.d., Varian, Inc., Middelburg, the Netherlands), and a 1:1 effluent splitter that allowed simultaneous flame ionization detection and EAD of the separated volatile compounds. Helium was used as the carrier gas, and the injector temperature was 220°C. The column temperature was 30°C for 2 min, rising to 240°C at 10°C/min, and then held for 10 min. The outlet for the EAD was held in a humidified airstream flowing at 0.5 m/sec over an antennal preparation. EAD recordings were made by using silver wire-glass capillary electrodes filled with Beadle-Ephrussi Ringer (Zhang et al., 2000) on freshly cut antennae. The antennal signals were stored and analyzed on a PC equipped with a serial IDAC interface box and the program EAD version 2.5 (Syntech, Hilversum, the Netherlands). Antennally active peaks in the lacewing extracts were identified with a GC–mass spectrometer (Varian CP-3800 GC coupled to a Varian Saturn 2000 mass selective detector) operated in split mode (1:10) with a CP-Wax 52CB column (0.25 μm film thickness, 60 m × 0.25 mm i.d., Varian, Inc.), programmed at 30°C for 2 min, increasing to 240°C at 10°C/min, and then held for 10 min. Compounds were identified by comparison of mass spectra and retention times to those of authentic standards. In addition, EAD responses from male antennae of the four species noted above were recorded to a synthetic mixture (100 ng/μl each) containing five C. oculata-produced compounds (1-tridecene, nonanal, nonanol, nonanoic acid, and IRI); three compounds associated with aphid prey [(1R,4aS,7S,7aR)-nepetalactol, (4aS,7S,7aR)- nepetalactone (both sex pheromone components), and (4aS,7S,7aS)-nepetalactone (non- pheromone compound)]; and three herbivore-induced plant volatiles [MS, (Z)-3-hexenyl acetate (Z3HA), and benzaldehyde (BA)]. Chemical Standards 1-Tridecene (97%), 1-nonanol (97%), skatole (98%), MS (99%), 2PE (99%), Z3HA (98%), and BA (99.5%) were obtained from Aldrich Chemical (Milwaukee, WI); nonanal (99%) and nonanoic acid (98%) were from Emery Industries (Cincinnati, OH). (4aS,7S,7aR)- Nepetalactone and (4aS,7S,7aS)-nepetalactone are often referred to as Z,E- and E,Z- nepetalactone, respectively, in the literature (e.g., Hooper et al., 2002). ZE-lactone (98%), E,Z-nepetalactone (96%), (1R,4aS,7S,7aR)-nepetalactol [ca. 90% Z,E-isomer (Hooper et al., 2002) with ca. 2% impurity of iridodial isomers], and the lacewing pheromone, IRI [80%; with 20% of (1R,2S,5R,8S)-iridodial as an impurity] were isolated or synthesized as described by Chauhan et al. (2004). 2166 J Chem Ecol (2006) 32: 2163–2176 Field Trapping Field-trapping experiments were carried out from early May through the end of September 2004 in either garden or small orchard environments in Spokane by using Pherocon VI traps (Trécé, Inc., Adair, OK) with removable sticky inserts. Traps were hung 1.0 to 1.5 m above the ground on either garden stakes or the branches of cherry (Prunus)/apple (Malus) trees ca. 5 to 10 m apart within each trap line. For each trapping experiment, two sets of traps (each set contained all treatments) were deployed with treatments allocated randomly to their initial trap positions within a set. The treatments were then systematically rotated among trap positions within a set after each replicate so that treatments appeared at least once per location (Latin-square design; Byers, 1991).
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