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Neuroptera: Chrysopidae) Approach but Seldom Enter Traps Baited with the Male-Produced Compound Iridodial

Neuroptera: Chrysopidae) Approach but Seldom Enter Traps Baited with the Male-Produced Compound Iridodial

RAPID COMMUNICATION Female Goldeneyed Lacewings (: ) Approach but Seldom Enter Traps Baited with the Male-Produced Compound Iridodial

1,2 1 3 1 KAMLESH R. CHAUHAN, VICTOR LEVI, QING-HE ZHANG, AND JEFFREY R. ALDRICH

J. Econ. Entomol. 100(6): 1751Ð1755 (2007) ABSTRACT Earlier, we identiÞed (1R,2S,5R,8R)-iridodial as a male-speciÞc compound of the goldeneyed lacewing, oculata Say (Neuroptera: Chrysopidae), but traps baited with this compound caught almost exclusively males. In the present report, we demonstrated by sweep-net sampling and observation in the vicinity of pheromone lures that C. oculata females, and males, are strongly attracted to iridodial. Aggregation activity of C. oculata adults occurred between dusk and dawn. This research demonstrates that iridodial may be useful to induce goldeneyed lacewings to lay in targeted plant patches for .

KEY WORDS , biocontrol, goldeneyed lacewing, aggregation pheromone

In 2004, we identiÞed (1R,2S,5R,8R)-iridodial from iments in 2004 and 2005 to monitor the responses of males of the goldeneyed lacewing, goldeneyed lacewing females to the male-produced Say (Neuroptera: Chrysopidae), and we showed that compound (1R,2S,5R,8R)-iridodial and to its diaste- the synthetic compound (Chauhan et al. 2004; Zhang reomer (1R,2S,5R,8S)-iridodial. et al. 2004) strongly attracted conspeciÞc males in the Þeld. This discovery indicated that the attraction of Materials and Methods lacewings in the Chrysopa to the phero- mone components Z,E-nepetalactol and Z,E-nepeta- Three Þeld experiments were carried out from early lactone (Boo et al. 1998, 2003; Hooper et al. 2002) may May through early September of 2004 at two locations be due to impurities of iridodial in synthetic aphid on the Beltsville Agricultural Research Center pheromone formulations. However, in our earlier (BARC), Beltsville, MD, and a follow-up experiment studies on C. oculata and other Chrysopa was conducted in 2005 from June to August. Isomeric (Zhang et al. 2006a, 2006b), we failed to demonstrate iridodials (Fig. 1) were synthesized as described by attraction of Chrysopa females to iridodial, calling into Chauhan et al. (2004): (1R,2S,5R,8R)-iridodial (IRI-R; question the role of this lacewing semiochemical. 92% with Ϸ8% of 8S isomer), the C. oculata male- Various green lacewings are attracted to host plant produced compound; and the unnatural, but anten- volatiles (Suda and Cunningham 1970, Flint et al. 1979, nally active diastereomer (1R,2S,5R,8S)-iridodial Zhu et al. 1999, Hooper et al. 2002, Pai et al. 2004, Zhu (IRI-S; 88% with Ϸ12% of 8R isomer). Lures were et al. 2005), particularly methyl salicylate (James prepared by applying 5 mg of iridodial per 50 ␮lof 2003a, 2003b; James and Price 2004; James 2006). How- heptane to the well of gray rubber septa (5-mm sleeve- ever, synthetic iridodial is a much more powerful type, The West Co., Lititz, PA). attractant for males of Chrysopa species (Zhang et al. An initial survey experiment was carried out in a 2004, 2006a, 2006b) than are plant-produced attract- meadow at BARC-East and a soybean, Glycine max (but see Hyeon et al. 1968). For practical utility, (L.) Merr., Þeld on the BARC North Farm from 9 to and to fully appreciate the complex acoustic and 31 May 2004 to determine which site had the highest pheromonal communication system of green lacew- lacewing population for future experiments. Two pairs ings in general, it is essential to know whether and how of Jackson Delta traps with sticky inserts (Agrisense, Chrysopa females respond to volatiles released by con- Fresno, CA) baited with either lacewing pheromone speciÞc males. Therefore, we conducted Þeld exper- lures or the solvent control septa were deployed at each site. Traps were hung about Ϸ1 m above the Mention of commercial products does not constitute an endorse- ground on metal stakes, Ϸ10 m apart between the ment by USDA. treatment and control traps within a pair, and Ϸ15 m 1 USDAÐARS Invasive Biocontrol & Behavior Laboratory, between sets of pairs. Pheromone lures and sticky B-007, BARC-West, Beltsville, MD 20705. inserts were refreshed, and their trap positions within 2 Corresponding author, e-mail: [email protected]. 3 Sterling International Inc. 3808 N. Sullivan Road, Building 16BV, the pairs were shifted every week. Based on this pilot Spokane, WA 99216. survey, subsequent experiments were carried out in 1752 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 100, no. 6

50 A ally around traps. Eight pairs of pheromone or blank 45 rubber septa dispensers were deployed on metal SE Males; Σ=1227; N=24

± 40 Females; Σ=28; N=24 stakes for the sweep netting experiment, but instead of sampling with a net, the soybean plants in a 5-m radius 35 around the dispensers were gently shaken using a CHO 30 CHO yardstick in the early morning. The numbers and sex / trap week 25 CHO CHO of the lacewings that ßew were counted and identi- 20 Þed. A lacewing was identiÞed as female if its abdomen IRI-R IRI-S 15 was swollen upon observation after it landed. Lacew- C. oculata ings that ßew far away or were not found after they 10 # of B alighted could not be determined, and they were only 5 a bbC counted. 0 Due to heterogeneity of variances among treat- IRI-R IRI-S Blank ments, trap catch data were analyzed using the non- Fig. 1. Captures of C. oculata adults in traps baited with parametric KruskalÐWallis analysis of variance the lacewing pheromone IRI-R, its unnatural isomer IRI-S, or (ANOVA) on rank test, followed by the StudentÐ solvent only (14 JuneÐ6 August 2004, Beltsville, MD). Bars NewmanÐKuels all pairwise comparison to separate with the same letter for each sex are not signiÞcantly differ- means (Zar 1984). Data from the net sweeping and ent (P Ͼ 0.05) by KruskalÐWallis ANOVA on ranks, followed by the StudentÐNewmanÐKeuls all pairwise comparison. visual check experiments were analyzed by paired t-tests at ␣ ϭ 0.05 level. soybean Þelds on the BARC North Farm. No herbicide Results or pesticide treatments were applied in these Þelds. For the test comparing isomeric iridodials, trans- In the initial survey experiment, 132 C. oculata males parent bucket traps (Aldrich et al. 1984) with lures in total were caught in sticky traps, but no females placed in the bottom of traps were deployed from 11 were captured during this entire test. The number of June to 6 August 2004. This experiment consisted of C. oculata males per visit per trap baited with IRI-R four sets of traps (a set is one line of three traps) hung (mean Ϯ SE ϭ 7.69 Ϯ 0.94; N ϭ 16) was signiÞcantly Ϸ15 m apart from stakes as described above, with Ϸ30 greater than that for the blank control traps (mean Ϯ m between trap lines. Initially, the positions of treat- SE ϭ 0.56 Ϯ 0.16; N ϭ 16). More than twice as many ments within a set of traps were allocated randomly, goldeneyed lacewings were captured at the BARC and then the treatments (IRI-R, IRI-S, and blank) North Farm soybean Þeld (⌺ϭ91) than the BARC- were systematically rotated among trap positions East meadow (⌺ϭ41); therefore, future experiments within a set after each replicate so that treatments were conducted at the BARC North Farm. were placed at least once per location (Latin-square In total, 1,227 C. oculata males and 28 females were design; Byers 1991). The traps were visited on every captured during the experiment comparing isomeric Monday, Wednesday, and Friday during the testing iridodials. Traps baited with the synthetic lacewing period; thus, each replicate lasted 2Ð3 d. Captured pheromone IRI-R captured signiÞcantly more males lacewings were taken to the laboratory for species and and females of C. oculata adults than did the traps gender determination, and counting. Dispensers were treated with the unnatural enantiomer IRI-S or blank refreshed every second week. control traps (Fig. 1). The IRI-SÐbaited traps also In experiments run from 10 July to 9 September 2004 caught signiÞcantly more males than did the control and 11 June to 26 August 2005, lacewings in the vicinity traps, but the number of females caught was not sig- of heptane-treated control and IRI-R pheromone dis- niÞcant from that for control traps (Fig. 1). The num- pensers (rubber septa inserted in open 1-ml plastic ber of females caught in traps baited with IRI-R was centrifuge vials) were monitored by sweep netting 40 times less than that of the males, but it was still around dispensers in soybean Þelds. Four pairs of signiÞcantly greater than the number of females IRI-R pheromone and heptane control dispensers caught in IRI-SÐbaited or blank control traps (Fig. 1). were hung from metal stakes as described above, with Also, four males of Burmeis- Ϸ20 m between dispenser pairs and Ϸ30 m between ter were captured in traps baited with IRI-R, and three sets of pairs. Sweep samples (Ϸ10 sweeps) were col- male and one female rufilabris (Burmeis- lected twice per week between 6:00 and 8:00 a.m. in a ter) were caught in control traps. 5-m radius around the stakes baited with either pher- Impressive numbers of female lacewings were cap- omone lures or blank controls. The positions of pher- tured by sweep netting around pheromone-treated omone lure and blank control within a pair were dispensers. In the 2004 experiment, in total 661 males shifted after each sampling, and captured lacewings and 226 females of C. oculata were captured in the were taken to the laboratory for processing as de- vicinity of pheromone-treated dispensers (male:fe- scribed above. male ratio ϭ 2.9:1), whereas only 19 males and one Simultaneously with the 2004 sweep-netting exper- female of C. oculata were captured nearby blank con- iment, another experiment was conducted in another trol dispensers. For each sampling week and overall, area of the soybean Þeld from 26 June to 14 July by signiÞcantly more C. oculata males and females were counting (but not collecting) lacewings spotted visu- collected around pheromone dispensers than around December 2007 CHAUHAN ET AL.: LACEWING AGGREGATION PHEROMONE 1753

Males around an IRI-R lure Males around a blank 20 Females around an IRI-R lure *** Females around a blank *** *** *** A 15 *** SE *** ±

10 *** *** *** *** *** *** 5 *** ***

0 20 *** *** / sweep-net sampling

15 *** B *** ***

*** *** *** C. oculata *** 10 *** *** *** # of # of 5 *** ***

0 1st 2nd 3rd 4th 5th 6th 1st-6th Week Fig. 2. Captures of C. oculata adults by sweep netting in a soybean Þeld at Beltsville, MD, around dispensers containing the lacewing pheromone IRI-R or solvent only. (A) 10 JulyÐ9 September 2004 (N ϭ 8 for each week; N ϭ 48 for weeks 1Ð6). (B) 11 JuneÐ26 August 2005 (N ϭ 8 for each week; N ϭ 48 for weeks 1Ð6). Asterisks indicate signiÞcant differences (paired t-tests at P Ͻ 0.001) in the numbers of C. oculata captured around treatment and control dispensers. blank control dispensers (P Ͻ 0.001) (Fig. 2A). The and quantiÞed. We also demonstrated that the diaste- same pattern of catches was observed in the follow-up reomer IRI-S is much less attractive to goldeneyed experiment carried out in 2005 (Fig. 2B). Captured lacewings than is IRI-R. In fact, the signiÞcant catches females usually laid eggs in collection vials and labo- of goldeneyed lacewings in the IRI-SÐbaited traps ratory cages soon after they were caught. In the experiment in which lacewings were visually observed for sex determination and counted, 597 C. oculata in total were recorded. Lacewing males, fe- 12 SE *** males, and undetermined sex were all signiÞcantly ± IRI-R lure more abundant around iridodial dispensers than 10 Blank around blank control dispensers (P Ͻ 0.001) (Fig. 3). The male:female sex ratio observed for this experi- 8 ment was 4.5:1. Eggs and larvae also were frequently seen on soybean plants near pheromone dispensers 6 but not around untreated control dispensers. *** 4 *** Discussion 2 Female goldeneyed lacewings are attracted to the # of green lacewings / lure / sampling / / sampling lure lacewings green # of vicinity of lures containing IRI-R, a compound pro- 0 Males Females Sex Unknown duced by conspeciÞc males (Zhang et al. 2004), but females seldom enter pheromone-baited traps. Male Fig. 3. C. oculata adults observed after being shaken from C. oculata are more powerfully attracted to IRI-R, plants around dispensers containing the lacewing phero- mone IRI-R or solvent only (26 JuneÐ14 July 2004, in a possibly because they form leks as do some soybean Þeld at Beltsville, MD) (N ϭ 8 replicate dispensers ϫ (Neuroptera: Myrmeleontidae) (Yasseri et al. 1998). 4 sampling dates ϭ 32). Lacewing numbers for each sex or In the course of the current study, lacewing eggs and unknown sex between IRI-R and blank control were ana- larvae were observed on soybean leaves nearby IRI-R lyzed by paired t-tests; asterisks indicate signiÞcant differ- dispensers, but these observations need to be repeated ences at P Ͻ 0.001. 1754 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 100, no. 6 might simply be due to the 12% impurity of IRI-R in Acknowledgments the synthetic sample of IRI-S. We thank Oliver S. Flint, Jr. (Section of Entomology, Before the realization that C. oculata males produce Smithsonian Institution, Washington, DC) for identiÞcation an aggregation pheromone, it was suggested that of the lacewing species and Robert Carlson (USDAÐARSÐ green lacewings in the genus Chrysopa are attracted to SEL, Beltsville, MD) for facilitating identiÞcations. We also nepetalactone and nepetalactol, because these com- thank Rod Schneidmiller (Sterling International Inc, Spo- pounds (also found in catnip, Nepeta cataria L. [Lami- kane, WA) for support. aceae]) are key components of many aphid sex pher- omones (e.g., Goldansaz et al. 2004). Hooper et al. (2002), after investigating a report that the Asian plant References Cited known as silver leaf, Actinidia polygama (Sieb. et Zucc.) (Actinidiaceae), is highly attractive to various Aldrich, J. R., J. P. Kochansky, W. R. Lusby, and J. D. Sexton. 1984. 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Iri- interesting blends of monoterpenoids and unsatur- dodials: enantiospeciÞc synthesis and stereochemical as- ated secondary alcohols that likely serve as aggre- signment of the pheromone for the goldeneyed lacewing, gation pheromones. In C. oculata, iridodial appar- Chrysopa oculata (Neuroptera: Chrysopidae). Tetrahe- dron Lett. 45: 3339Ð3340. ently comes from thousands of elliptical epidermal Flint, H. M., S. S. Salter, and S. Walters. 1979. Caryo- glands found only on the abdominal sternites of phyllene: an attractant for the green lacewing Chrysopa males (Zhang et al. 2004). carnea. Environ. Entomol. 8: 1123Ð1125. Green lacewings have a long history of use in bio- Goldansaz, S. H., S. Dewhirst, M. A. Birkett, A. M. Hooper, logical control of soft-bodied pests (Henry D.W.M. Smiley, J. A. Pickett, L. Wadhams, and J. N. and Wells 2007), and species in the genus Chrysoperla McNeil. 2004. IdentiÞcation of two sex pheromone com- are commercially available. 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Proc. continuing to search for pheromones potentially use- Entomol. Soc. Wash. 84: 191Ð203. ful for biological control in other species of Chrysopi- Henry, C. S., and M. M. Wells. 2007. Can what we donÕt dae and in brown lacewings () and know about lacewing systematics hurt us? Am. Entomol. other predacious . 53: 42Ð47. December 2007 CHAUHAN ET AL.: LACEWING AGGREGATION PHEROMONE 1755

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