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Exposure of Solidago Altissima Plants to Volatile Emissions of an Insect Antagonist (Eurosta Solidaginis) Deters Subsequent Herbivory

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Exposure of Solidago Altissima Plants to Volatile Emissions of an Insect Antagonist (Eurosta Solidaginis) Deters Subsequent Herbivory Exposure of Solidago altissima plants to volatile emissions of an insect antagonist (Eurosta solidaginis) deters subsequent herbivory Anjel M. Helms, Consuelo M. De Moraes, John F. Tooker, and Mark C. Mescher1 Center for Chemical Ecology, Department of Entomology, The Pennsylvania State University, University Park, PA 16802 Edited by James H. Tumlinson, The Pennsylvania State University, University Park, PA, and approved November 19, 2012 (received for review October 25, 2012) Recent work indicates that plants respond to environmental odors. olfactory cues has been documented after exposure to herbivore- For example, some parasitic plants grow toward volatile cues from induced volatiles emitted either by neighboring plants (9, 10) or by their host plants, and other plants have been shown to exhibit other parts of the same plant (11, 14). The latter finding has given enhanced defense capability after exposure to volatile emissions rise to speculation that such mechanisms might have initially from herbivore-damaged neighbors. Despite such intriguing dis- evolved to overcome constraints on the within-plant transmission coveries, we currently know relatively little about the occurrence of wound signals imposed by the discontinuous architecture of and significance of plant responses to olfactory cues in natural plant vascular systems, with eavesdropping by neighboring plants systems. Here we explore the possibility that some plants may arising secondarily (11). respond to the odors of insect antagonists. We report that tall Defense priming also has been reported in response to (non- goldenrod (Solidago altissima) plants exposed to the putative sex olfactory) cues directly associated with the presence of herbivores, attractant of a closely associated herbivore, the gall-inducing fly including insect footsteps on leaves and broken trichomes (15, 16). Eurosta solidaginis, exhibit enhanced defense responses and re- However, direct plant perception of insect-derived olfactory cues duced susceptibility to insect feeding damage. In a field study, has not been reported previously, despite the many herbivores egg-laying E. solidaginis females discriminated against plants pre- emitting volatile chemicals that function in intraspecificcommu- viously exposed to the sex-specific volatile emissions of males; fur- nication [e.g., sex, aggregation, alarm pheromones (1-3)] or defense thermore, overall rates of herbivory were reduced on exposed [e.g., predator repellents (17)]. Furthermore, these compounds are plants. Consistent with these findings, laboratory assays docu- frequently released in substantial quantities and in proximity to mented reduced performance of the specialist herbivore Trirhabda plants on which feeding will subsequently occur (18, 19); thus, they virgata on plants exposed to male fly emissions (or crude extracts), would appear to provide a class of potentially reliable olfactory cues as well as enhanced induction of the key defense hormone jas- that plants might profitably use for defense priming or induction. monic acid in exposed plants after herbivory. These unexpected In light of these observations, in the present study we explored findings from a classic ecological study system provide evidence whether and how the antiherbivore defenses of tall goldenrod, for a previously unexplored class of plant–insect interactions in- Solidago altissima L., are influenced by exposure to chemical emis- volving plant responses to insect-derived olfactory cues. sions of its specialist herbivore Eurosta solidaginis (Fitch), a tephritid fruit fly(Fig.1A) whose larvae induce ball-shaped galls in the stems plant defense | plant olfaction of this plant species (Fig. 1B). The interactions of these two species have been studied for decades and suggest a tightly coevolved lfactory cues and signals play important roles in a diverse relationship (20, 21). Moreover, gall induction and feeding by Oarray of ecological interactions among plants and insects. E. solidaginis greatly reduce S. altissima growth and fitness (21), The best documented of these interactions include pheromonal implying that individual plants may benefitfromefficient de- signaling between conspecific insects and the use of plant-derived ployment of effective defenses. odors as foraging cues by insect pollinators, herbivores, and We specifically explored whether the chemical emissions of predators (1–7). Recent findings demonstrate that plants them- male E. solidaginis might induce or prime antiherbivore defenses selves can also perceive and respond to environmental odors; for in S. altissima, as the ecology of this system suggests that these example, parasitic plants in the genus Cuscuta use host-derived emissions may provide a salient cue reliably associated with volatiles to direct their growth toward preferred host plants (8)— impending attack. Male E. solidaginis begin to emerge before apparently using host plant odors as foraging cues in much the females (during mid-May in the northeastern US), and after same way that insect herbivores do (5, 6). In other systems, plants emergence typically perch on the upper leaves of S. altissima appear to perceive the characteristic odors emitted from herbi- ramets, often for hours at a time (20, 21), and emit copious vore-damaged plant tissues as warning cues indicating the pres- amounts (mean ± SD, ∼70 ± 20 μg over 24 h) of a volatile blend ence of potential attackers (9–11). Thus, the perception of volatile that we hypothesize functions as a sex attractant. Through GC- chemical cues appears to play important roles in plant ecology, MS analysis, the blend was found to be dominated by spiroacetals, although our understanding of the prevalence and significance of whose biological significance as insect-derived volatiles remains plant olfaction in natural systems remains quite limited. largely undocumented but with known functions as pheromones, Most previous work on plant responses to odor cues has kairomones, or allomones in some systems (22). Females begin addressed “priming” of induced defense responses. Plants fre- searching for oviposition sites immediately after mating and have quently employ defenses that are induced by environmental stimuli, been observed to oviposit into stems of the same goldenrod genet rather than being expressed constitutively, in environments where the occurrence of particular antagonists (e.g., herbivores, patho- gens) is not entirely predictable—presumably to conserve resour- Author contributions: A.M.H., C.M.D.M., J.F.T., and M.C.M. designed research; A.M.H. and ces and maintain the flexibility to precisely target defense responses J.F.T. performed research; A.M.H., C.M.D.M., J.F.T., and M.C.M. analyzed data; and A.M.H., against specific attackers (12). Still further economy may be ach- C.M.D.M., J.F.T., and M.C.M. wrote the paper. The authors declare no conflict of interest. ieved through priming responses, in which induced defenses are ECOLOGY made ready for deployment in response to cues reliably associated This article is a PNAS Direct Submission. with impending attack (10, 11, 13, 14). Priming of plant defenses by 1To whom correspondence should be addressed. E-mail: [email protected]. www.pnas.org/cgi/doi/10.1073/pnas.1218606110 PNAS | January 2, 2013 | vol. 110 | no. 1 | 199–204 Downloaded by guest on September 29, 2021 Plant Exposure to Volatile-Emitting E. solidaginis Males Reduces Subsequent Rates of Ovipuncture by E. solidaginis Females and Overall Levels of Herbivory in the Field. To test the hypothesis that exposure to the male E. solidaginis emission enhances S. altissima defense responses, we conducted a large-scale field study comparing the oviposition preferences of E. solidaginis females for plants with previous exposure to male E. solidaginis or various controls. We also assessed overall rates of herbivory on these plants. Randomly selected S. altissima plants on which male E. solidaginis were caged for 3 d subsequently demonstrated sig- nificantly reduced rates of ovipuncture by E. solidaginis females [i.e., insertion of the ovipositor into plant tissues as assessed by characteristic patterns of tissue damage (20, 21, 23, 24)] compared with control plants similarly exposed to female E. solidaginis, common houseflies, or empty cages (Fig. 2A; χ2 test of in- 2 dependence, χ 3 = 12.5, P = 0.006). The female E. solidaginis and housefly controls were designed to account for the effects of fly- associated cues other than the male volatile emission. The pro- portion of ovipunctured plants observed in the control treatments was 3.7–4.8 times higher than that of plants exposed to E. solid- aginis males, whereas no significant differences were observed among the three control treatments [post hoc relative risk analysis assessing the risk of each control group receiving an ovipuncture relative to the male E. solidaginis treatment, with associated 95% confidence intervals: male vs. female: 3.80 (1.35–10.65); male vs. housefly: 4.75 (1.73–13.03); male vs. empty net: 3.68 (1.31–10.39)]. Thus, egg-laying E. solidaginis females appear to actively discrim- inate against plants previously exposed to male flies. Female E. solidaginis are known to assess host plant quality before ovipo- sition by tasting bud tissue with chemoreceptors located on their feet and mouthparts, and often reject more resistant plant geno- Fig. 1. (A) Male E. solidaginis fly perching on its host plant, S. altissima, and types (21, 24, 25). Because E. solidaginis females so rarely ovi- releasing a volatile blend attractive to potential mates. (B) Developing posited on exposed plants in our field study, our data do not allow E. solidaginis gall on stem of S. altissima. (Photo credits: Ian Grettenberger.) us to assess the effects of exposure on gall development after ovi- position. However, levels of foliar damage by chewing and leaf- mining insects were dramatically reduced on plants previously ex- on which mating occurs, frequently within 30 min (20). Eggs – posed to E. solidaginis males compared with each of the control typically hatch 5 8 d later (20, 21), and galls become visually groups (Fig. 2B; negative binomial regression: male vs. female: apparent within 3 wk; thus, it seems plausible that exposure to the t = 3.794, P = 0.0002; male vs.
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