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Specificity in Induced Plant Responses Shapes Patterns of Herbivore Occurrence on Solanum Dulcamara Author(S): Danush V

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Specificity in Induced Plant Responses Shapes Patterns of Herbivore Occurrence on Solanum Dulcamara Author(S): Danush V Specificity in Induced Plant Responses Shapes Patterns of Herbivore Occurrence on Solanum dulcamara Author(s): Danush V. Viswanathan, Anita J. T. Narwani, Jennifer S. Thaler Source: Ecology, Vol. 86, No. 4 (Apr., 2005), pp. 886-896 Published by: Ecological Society of America Stable URL: http://www.jstor.org/stable/3450842 Accessed: 05/11/2008 19:17 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=esa. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit organization founded in 1995 to build trusted digital archives for scholarship. We work with the scholarly community to preserve their work and the materials they rely upon, and to build a common research platform that promotes the discovery and use of these resources. For more information about JSTOR, please contact [email protected]. Ecological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Ecology. http://www.jstor.org Ecology, 86(4), 2005, pp. 886-896 ? 2005 by the Ecological Society of America SPECIFICITY IN INDUCED PLANT RESPONSES SHAPES PATTERNS OF HERBIVORE OCCURRENCE ON SOLANUM DULCAMARA DANUSH V. VISWANATHAN,' ANITA J. T. NARWANI, AND JENNIFER S. THALER2 Departmentof Botany, Universityof Toronto,25 WillcocksStreet, TorontoM5S 3B2, Canada Abstract. Interspecific competition between phytophagous insects can occur when plant responses induced by an early-season herbivore alter host quality for later colonizers. Recent evidence for specificity in the elicitation of induced plant responses by different attackers suggests that dynamics of host use in the field may be more complex than previously anticipated, because host suitability for colonizing herbivores may depend on which her- bivore species has initially damaged a plant. In each of two years, we manipulated the first herbivore to attack Solanum dulcamara plants in an experimental population using several different arthropod species and subsequently monitored colonization by natural herbivores over the course of the growing season. We additionally performed weekly herbivore counts in wild S. dulcamara populations following natural variation in herbivore arrival. Plant- mediated interactions occurred primarily between two leaf-feeding beetles, Psylliodes affinis and Plagiometriona clavata. In both manipulative and observational experiments, P. clavata oviposition was reduced on plants initially damaged by P. affinis (or a third leaf-feeding beetle, Lema trilinea) relative to plants that were initially undamaged. Lowered P. clavata occurrence continued through subsequent life-history stages, resulting in decreased emer- gence of second-generation P. clavata adults on these plants. The occurrence of P. affinis was also lowered on plants damaged by conspecifics in both manipulative and observational experiments. Resistance against P. affinis also followed applications of jasmonic acid, an elicitor of plant defensive responses. Conversely, early-season damage by P. clavata did not influence plant quality for either later conspecifics or P. affinis. Initial herbivory by the spittlebug Aphrophora saratogensis or generalist taildropper slugs (Prophysaon sp.) likewise had no influence on P. clavata and P. affinis colonization, whereas L. trilinea damage did not affect later arriving P. affinis. Hence, only a subset of early-season damagers influenced herbivore occurrence on S. dulcamara. Preference tests examining P. affinis feeding and P. clavata oviposition confirmed that specificity in elicitation of induced plant responses produced the divergent herbivore occurrence patterns observed in the field. Over- all, the existence of plant-mediated competitive asymmetry between herbivore species on S. dulcamara highlights the dynamic nature of plant resistance and its potential role in organizing herbivore communities. Key words: bittersweetnightshade; competition; herbivory; induced responses;phytophagous insect communities;Plagiometriona clavata; plant-mediated interactions; Psylliodes affinis; Solanum dulcamara;specificity. INTRODUCTION work has begun to extend these results to other feeding et al. and further that Increasingly widespread documentation of induced guilds (Denno 2000), suggests induced a in her- plant responses to herbivory has fostered interest in the responses may play part structuring bivore communities Gonzalez-Me- possibility of plant-mediated interactions between dif- (Tscharntke 1999, Gomez Van Zandt and ferent herbivores (Faeth 1986, Denno et al. 1995). Such gias and 2003, Agrawal 2004). Plant-mediated interactions between herbivore indirect effects may occur when physical or chemical spe- cies are therefore as an mechanism plant responses induced by a given herbivore affect emerging important of in To resource quality for subsequent foragers (Karban and competition many systems. date, however, most field studies have examined Baldwin 1997). Indeed, a review by Denno et al. (1995) experimental only whether a can in- found that induced responses were involved in over single early-season inducing agent fluence later and Niemela half of the published studies in which competition oc- foragers (e.g., Haukioja curred between mandibulate herbivores. More recent 1979, Faeth 1986, Hanhimaki 1989, Karban 1993, Tha- ler et al. 2001, Wise and Weinberg 2002). This ap- Manuscriptreceived 13 February2004; revised 15 June2004; proach mimics natural conditions in systems where a 23 accepted August2004. CorrespondingEditor: K. C. Larson. is the exclusive or early- I E-mail: danush@ particular species predominant botany.utoronto.ca season In however, several 2 Present address: Departmentof Entomology, Cornell damager. many systems, University, 3128 Comstock Hall, Ithaca, New York 14853 different herbivore taxa feed abundantly on a common USA. host plant species during its early growth phase. The 886 April2005 SPECIFICITYOF PLANT RESPONSES 887 dynamics of host use over a growing season may be substantially more complex than previously expected if the host plant exhibits specificity in induced respons- es to different early-season attackers. Specificity in plant response has two components: effect and elicitation. Specificity of effect occurs when herbivore species are differently affected by a given induced response (Stout et al. 1998, Agrawal 2000; see ? '4 also Hartley and Lawton 1987). Experiments assessing colonization of treated and untreated plants by natural assemblages of herbivores following early-season in- PLATE. 1. Plagiometriona clavata (tortoise beetle) adult duction frequently find some degree of specificity of feeding on Solanumdulcamara (bittersweet nightshade) leaf. effect (e.g., Hunter 1987, Inbar et al. 1998, Agrawal Photo credit: D. Viswanathan. 1999, Agrawal and Sherriffs 2001, Thaler et al. 2001, Riihimaki et al. 2003). Conversely, specificity of elic- itation occurs when herbivore species differentially in- to induce pathogenesis-related proteins, peroxidases, duce phenotypic responses in a particular host plant polyphenol oxidases, and cell necrosis in response to (Stout et al. 1994, 1998, Agrawal 2000, Traw and Daw- herbivory by gall mites (Bronner et al. 199 la, b). These son 2002). In the field, specificity of elicitation is ev- responses reduce intraspecific gall mite damage to the ident when a given attacker varies in abundance across plant (Westphal et al. 1991), exert negative interspecific plants initially damaged by different herbivore species. effects on rust mite fecundity (Westphal et al. 1991), Using lab preference tests, Hartley and Lawton (1987) and positive interspecific effects on spider mite fecun- revealed specificity of elicitation in field-collected dity (Westphal et al. 1992). Additionally, herbivory by birch leaves damaged by different herbivores. Addi- Lema trilinea (three-lined potato beetle) induces tionally, Inbar et al. (1998) showed that different chem- changes in polyphenol oxidase and proteinase inhibitor ical elicitors of induced plant responses varied in their activity, which can influence the growth rate of L. tri- ability to influence the colonization of tomato plants linea larvae (Viswanathan and Thaler 2004). by specific herbivores. Otherwise, however, field col- Natural populations of S. dulcamara occur at the onization of plants treated with different damage types Koffler Scientific Reserve at Jokers Hill (hereafter Jok- has been explicitly compared only between plants with ers Hill), King City, Ontario, Canada, where all field herbivore vs. mechanical damage (e.g., Agrawal 1999, experiments were conducted. Several herbivore species Agrawal and Sherriffs 2001; but see Van Zandt and feed on S. dulcamara at Jokers Hill, five of which were Agrawal 2004). examined in this study: two univoltine native special- In this we two of field data from paper, present years ists on solanaceous plants, Lema trilinea White and whether the iden- manipulative
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