Field Evaluation Of Herbivore-induced Plant

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FIELD EVALUATION OF HERBIVORE-INDUCED PLANT VOLATILES AS ATTRACTANTS FOR BENEFICIAL INSECTS: METHYL SALICYLATE AND THE GREEN LACEWING, Chrysopa nigricornis

DAVID G. JAMES1,∗ 1 Department of Entomology Irrigated Agriculture Research and Extension Center Washington State University 24105 North Bunn Road Prosser, Washington 99350, USA

(Received October 8, 2002; accepted March 17, 2003)

Abstract—Synthetic methyl salicylate (MeSA), a herbivore-induced plant volatile (HIPV), was demonstrated to be an attractant for the green lacewing, Chrysopa nigricornis, in two field experiments conducted in a Washington hop yard. Significantly greater numbers of C. nigricornis were trapped on MeSAbaited sticky cards (mean: 2.8 ± 0.4/card/week) than on unbaited cards (0.45 ± 0.15) during June–September. Cards baited with two other HIPVs, hexenyl acetate and dimethyl nonatriene, did not attract more C. nigricornis than did unbaited traps (0.30 ± 0.10, 0.44 ± 0.15, respectively). MeSA-baited Unitraps captured 1.9 ± 0.5 C. nigricornis/trap/week during July–August compared to 0.20 ± 0.20/trap/week in methyl eugenol-baited traps and 0.03 ± 0.03/trap/week in unbaited traps. The potential use of MeSA in enhancing C. nigricornis populations in Washington hop yards as an aid to conservation biological control of aphids and mites is discussed. Key Words—Herbivore-induced plant volatiles, methyl salicylate, Chrysopa nigricornis, attractant, predators, biological control, hops.

INTRODUCTION

Plants respond to herbivore damage by producing volatiles that attract natural enemies of the herbivores responsible for the damage (Dicke et al., 1990; Turlings et al., 1990; Vet and Dicke, 1992; Stowe et al., 1995; Takabayashi and Dicke, ∗

To whom correspondence should be addressed. E-mail: [email protected]

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1996). The qualitative and quantitative characteristics of herbivore-induced plant volatiles (HIPVs) can vary according to the herbivore involved, the plant species, and even the genotype (Turlings et al., 1993; Takabayashi et al., 1994). The phenolic compound, methyl salicylate (MeSA), has been identified in HIPV blends from at least 10 plant species attacked by herbivores, including lima bean damaged by spider mites, Tetranychus urticae Koch (Dicke et al., 1990; Ozawa et al., 2000a), tomato [T. urticae] (Dicke et al., 1998), cucumber [T. urticae] (Agrawal et al., 2002), cabbage [caterpillars, Pieris spp] (Geervliet et al., 1997), pear [Psyllidae] (Scutareanu et al., 1997), hops [hop aphid, Phorodon humuli Schrank] (Campbell et al., 1993), bird cherry [bird cherry oat aphid, Rhopalosiphum padi (L.)] (Glinwood and Pettersson, 2000; Ninkovic et al., 2003), potato [Colorado potato beetle, Leptinotarsa decemlineata (Say)] (Bolter et al., 1997), Nicotiana attenuata [caterpillars, leaf bugs, flea beetles] (Kessler and Baldwin, 2001), and Lotus japonicus [T. urticae] (Ozawa et al., 2000a). Tobacco plants innoculated with tobacco mosaic virus also produced MeSA (Shulaev et al., 1997). However, MeSA is not universally produced by herbivore-damaged plants, as evidenced by its absence in volatiles from caterpillar (Spodoptera exigua (Hubner)) damaged corn (Turlings et al., 1990) and lima bean (Ozawa et al., 2000b), spider-mite-infested apple trees (Llusia and Penuelas, 2001) and cotton and maize plants damaged by western tarnished plant bugs, Lygus hesperus Knight (Rodriguez-Saona et al., 2002). Other common HIPVs reported, particularly from spider-mite-damaged plants, include the terpene 3,7-dimethyl-1,3,6-octatriene, the methylene terpene 4,8-dimethyl-1,3,7-nonatriene, and the ester Z -3-hexenyl acetate (Dicke et al., 1990; Pare and Tumlinson, 1996). Laboratory studies have demonstrated MeSA to be attractive to the predatory mite, Phytoseiulus persimilis Athias-Henriot (Phytoseiidae) (Dicke and Sabelis, 1988; Dicke et al., 1990; Ozawa et al., 2000a) and the predatory bug, Anthocoris nemoralis (Fabricius) (Anthocoridae) (Drukker et al., 2000). In contrast, olfactometer studies showed MeSA to be repellent to the aphid plant pests, Aphis fabae Scop. and Sitobion avenae (Hardie et al., 1994; Petterson et al., 1994). Similarly, field experiments showed MeSA reduced trap catches of the aphid, Phorodon humuli Schrank, during spring colonization of hop yards (Losel et al., 1996). Ninkovic et al. (2003) demonstrated that MeSA significantly delayed establishment and reduced infestation of the bird cherry oat aphid (Rhopalosiphum padi) in oats treated with a pellet formulation of the semiochemical. Most of the research to date on HIPVs and response by natural enemies has been conducted under laboratory conditions (Hunter, 2002). If these compounds are to realize their potential in applied entomology (Sabelis et al., 1999), then we need to conduct more studies on HIPVs and natural enemy responses in the field environment. This study provides the first field evidence for attraction of a generalist predator in the Pacific Northwest of the United States, the green lacewing, Chrysopa nigricornis Burmeister (Neuroptera: Chrysopidae), to synthetic methyl salicylate.

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METHODS AND MATERIALS

One experiment was conducted in an unsprayed 1-ha hop yard at Washington State University – Prosser from April 11 to September 5, 2002 to determine whether selected HIPVs are attractive to field populations of beneficial arthropods. Yellow sticky cards (23 × 18 cm, Trece Incorporated, Salinas, CA) baited with 2-ml glass vials of candidate HIPV solutions were tied to wooden poles ∼2 m above the ground (poles in hop yards are used to carry wires for supporting hop plants). HIPVs tested were methyl salicylate [MeSA] (99%, Sigma-Aldrich, St. Louis, MO), (Z ) – 3 - hexenyl acetate (98%, Sigma-Aldrich, St. Louis, MO), 3,7- dimethyl – 1,3,6 – octatriene (Sigma-Aldrich, St. Louis, MO, 8 mg in 2-ml hexane) and 4,8 – dimethyl – 1,3,7 – nonatriene (synthesized by R. J. Bartelt, USDA, Peoria, IL, 10 mg in 2-ml hexane). Dimethyl octatriene was used until June 13. Thereafter, it was replaced by dimethyl nonatriene. These compounds were replaced weekly; MeSA and hexenyl acetate were replaced fortnightly. Bait vials were taped to the lower edge of the cards that were placed in a 3 × 4 grid with 10 m between the randomized treatments. Three replicates were run for each treatment. Sticky cards were replaced weekly and examined under a stereomicroscope for green lacewings (Chrysopidae). Lacewings were identified using the keys of Agnew et al. (1981) and Penny et al. (2000). A second experiment was conducted in the same hop yard as the first from July 2 to September 10 by using Universal Moth traps or Unitraps (Agrisense, Fresno, CA). Six traps were placed in separate rows, six rows apart with a minimum distance of 10 m between traps. Traps were alternately baited with MeSA or left unbaited (three replicates of each). Glass vials containing 2 ml of 99% MeSA were taped to the interior wall of traps. All traps were filled to a depth of ∼5 cm with water to drown trapped insects. Traps were checked weekly for insects, which were removed, identified, and counted. MeSA baits were changed monthly, and water was renewed weekly. From August 6, an additional three traps were placed in the yard (within the experimental area in “vacant” rows with a minimum distance of 10 m from other traps). These were baited with 2-ml glass vials of methyl eugenol (98%, Sigma-Aldrich, St. Louis, MO), a compound previously described as an attractant for two species of Chrysopa (Suda and Cunningham, 1970; Umeya and Hirao, 1975). Data were log (x + 1) transformed to equalize variance and analyzed using analysis of variance and Fisher’s least significant difference procedure. RESULTS

Sticky, Cards. Significantly greater numbers of the green lacewing, C. nigricornis, were trapped on MeSA-baited sticky cards than on the other HIPVbaited or unbaited cards (F = 20.2, df = 3, 42, P = 0.00; Figure 1). A mean of 2.8 (±0.4) C. nigricornis/card/week was captured during 13 June – 5 September on the MeSA- baited cards compared to 0.45 (±0.15), 0.30 (±0.10), and 0.44 (±0.15)

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FIG. 1. Weekly mean (±SE) number of adult Chrysopa nigricornis trapped on yellow sticky cards baited with methyl salicylate, dimethyl octatriene, dimethyl nonatriene, hexenyl acetate, or left unbaited, during April 11 – September 5, 2002 in a Washington hop yard.

on the unbaited, dimethyl nonatriene-, and hexenyl acetate-baited cards, respectively. Attraction of C. nigricornis to MeSA-baited cards appeared to be greatest from mid-June to mid-July, decreasing in August. Chrysoperla plurabunda (Stephens) was seen occasionally in the hop yard, but none were trapped on sticky cards. Unitraps. During the 10-week period that the second experiment was conducted, only one C. nigricornis was recorded from the unbaited Unitraps (mean = 0.03/trap/week). In contrast, a total of 67 C. nigricornis was recorded from the MeSA-baited traps (mean = 1.9/trap/week). Both sexes of C. nigricornis were trapped (female- to-male ratio = 2:1, N = 33) with numbers declining during late August (Figure 2). Three C. nigricornis were recorded from a methyl eugenol trap on August 20. No C. plurabunda were trapped. DISCUSSION

Hunter (2002) in a review of plant volatile–natural enemy interactions makes the point that although laboratory evidence for plants manipulating the foraging of natural enemies by volatile emission is now overwhelming, few studies have been published showing natural enemy responses to plant volatiles under field conditions. In addition, the few outdoor studies that have been published are often correlative (higher densities of predators around pest-infested plants than uninfested plants (e.g., Drukker et al., 1995; Shimoda et al., 1997), or involve inducing HIPVs from plants (without other prey-associated cues) and measuring responses by natural enemies (e.g., Thaler, 1999; Ockroy et al., 2001). The current study,

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FIG. 2. Weekly mean (±SE) number of adult Chrysopa nigricornis captured in Unitraps baited with methyl salicylate, methyl eugenol or left unbaited, during July 2 – September 10 2002 in a Washington hop yard. Note, methyl eugenol used only during August 6 – September 10.

demonstrating field attraction of a beneficial insect species to a synthetic formulation of an HIPV, joins a much smaller list of similar studies using synthetic formulations (e.g., Flint et al., 1979; Sabelis et al., 1999; Zhu et al., 1999). Demonstrating bioactivity of commercially available, synthetic HIPVs in field experiments is an important step towards practical application of these semiochemicals in pest management. This study is also the first demonstration of attraction of a green lacewing species to MeSA. Chrysopa nigricornis is a large green lacewing, distributed throughout the United States (Agnew et al., 1981) that is predatory as an adult as well as a larva. It is common in the Pacific Northwest and is a useful component of Insect Pest Management (IPM) programs in tree and vine crops and hops. In hops, early season recruitment of predators like C. nigricornis has been identified as a key factor in better utilizing conservation biological control of aphids and mites within an IPM program (James et al., 2001, 2003). The use of commercially available HIPVs, like MeSA, may have potential for enhancing spring recruitment of beneficial arthropod populations in crops. However, developing semiochemical formulations that combine practicality, efficacy, and longevity remains a challenge (Dicke et al., 1990). The results of this study indicate that MeSA is an attractant for C. nigricornis. In contrast, there was no evidence that C. nigricornis was attracted to hexenyl acetate or dimethyl nonatriene. Dimethyl octatriene also appeared not to be attractive although results for this HIPV are less conclusive because of the limited

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period of use in the experiment. This study was designed to answer the simple question of whether any of four common components of identified HIPV blends possess field attraction to any beneficial insect(s) in a Washington hop yard. Now that bioactivity of synthetic MeSA to at least one predatory insect species in the field has been established, it will be prudent to investigate effective concentration levels/release rates and the effect of using HIPV blends. Although the population of C. nigricornis in the hop yard was small (weekly canopy beating samples (9 vines/week) yielded only two C. nigricornis adults during June – August), significant numbers of adults were trapped on MeSA-baited sticky cards and in the Unitraps. Interestingly, the smaller green lacewing species, C. plurabunda, was also present in the yard (similar low numbers in canopy samples) but was not attracted to MeSA-baited traps. The decline in trapped C. nigricornis observed during August may have been the result of a diminishing population rather than a decline in response to MeSA. Canopy sampling indicated greatly increasing populations of C. plurabunda during September (>100 individuals), but this species was still not detected in MeSA-baited traps (James, unpublished observation). C. nigricornis was absent in September canopy samples. A possible explanation for MeSA attraction of C. nigricornis and not C. plurabunda may lie in the fact that the former is a carnivore as an adult while the latter is only carnivorous as a larva. HIPVs presumably have more immediate benefits to predators that are carnivorous in the prey-locating adult life stage than to predators that are carnivores only as larvae. C. nigricornis has not been studied previously for its response to HIPVs, although Caltagirone (1969) showed that a mixture of terpenyl acetate, dark brown cane sugar, and water was attractive. C. plurabunda is known to respond to 2phenylethanol and (E)-β-farnesene (Zhu et al., 1999), isomers of tryptophan and its breakdown products (Van Emden and Hagen, 1976) and β-caryophyllene (Flint et al., 1979). Monoterpene alcohols isolated from a Japanese vine (Actinidia polygama Miq) were shown to be attractive to males of Chrysopa septempunctata Wesmael and Chrysopa japana Okomoto (Sakan et al., 1970). Methyl eugenol was reported by Suda and Cunningham (1970) and Umeya and Hirao (1975) to attract Chrysopa basalis Walker and an unidentified Chrysopa sp., respectively. In the current study, no clear evidence of attraction of C. nigricornis to methyl eugenol was obtained, although this compound was only used for a limited period. Campbell et al. (1993) showed that aphids (Phorodon humuli) feeding on hop leaves induced release of MeSA, (E)-2-hexenal and β-caryophyllene. The latter two components were attractive to aphids in laboratory tests, while MeSA appeared to be repellent. Subsequently, Losel et al. (1996) showed MeSA reduced trap catches of P. humuli in a hop yard. A similar result was achieved by Ninkovic et al. (2003), who delayed field establishment and reduced population levels of the bird cherry oat aphid, Ropalosiphum padi, by distributing wax pellets containing MeSA. Aphid (P. humuli) numbers in the hop yard used in this study were low (0–2 per leaf)

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for most of the season apart from three weeks in June when numbers reached 20 per leaf. Elevated numbers of C. nigricornis in MeSA-baited traps were first seen at this time (presumably as a consequence of greater numbers of aphids) but continued through July and August when aphids were virtually absent in the yard. The spider mite, Tetranychus urticae, was the other major herbivore in the yard during the experiments and although mites are known to induce production of MeSA in other plants (e.g., Dicke et al., 1990; Ozawa et al., 2000a), it is unknown whether they do in hops. The use of synthetic MeSA in hop yards may conceivably have two benefits to pest management; enhanced recruitment of beneficial insects like C. nigricornis and repellence of the aphid pest, P. humuli. Field evidence for attraction of other beneficial insect species to MeSA and hexenyl acetate is being collected and will be reported in due course (James, in preparation, 2003). The efficacy, potential, and practicality of using controlled release dispensers containing MeSA as an enhancement for conservation biological control in Washington hops is currently being examined. Acknowledgments—Tanya Price is thanked for identifying the lacewings. This research was partially funded by the Hop Research Council and the Washington Hop Commission.

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