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Insect Herbivory Stimulates Allelopathic Exudation by an Invasive Plant and the Suppression of Natives

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Insect Herbivory Stimulates Allelopathic Exudation by an Invasive Plant and the Suppression of Natives Ecology Letters, (2005) 8: 209–217 doi: 10.1111/j.1461-0248.2004.00713.x LETTER Insect herbivory stimulates allelopathic exudation by an invasive plant and the suppression of natives Abstract Giles C. Thelen,1 Jorge M. Exotic invasive plants are often subjected to attack from imported insects as a method of Vivanco,2 Beth Newingham,3 biological control. A fundamental, but rarely explicitly tested, assumption of biological William Good,4 Harsh P. Bais,2 control is that damaged plants are less fit and compete poorly. In contrast, we find that 5 6 Peter Landres, Anthony Caesar one of the most destructive invasive plants in North America, Centaurea maculosa, exudes 1 and Ragan M. Callaway * far higher amounts of (±)-catechin, an allelopathic chemical known to have deleterious effects on native plants, when attacked by larvae of two different root boring biocontrol insects and a parasitic fungus. We also demonstrate that C. maculosa plants experimentally attacked by one of these biocontrols exhibit more intense negative effects on natives. Keywords Allelopathy, biocontrol insects, exotic invasion, herbivory, noxious weed, phytotoxic exudates, root exudates, spotted knapweed. Ecology Letters (2005) 8: 209–217 naturalized. However, despite the importance of biocontrols INTRODUCTION we know little about how they affect fundamental ecological Scientists, land managers and policy makers have been processes (McEvoy & Coombs 1999; Pearson & Callaway stymied by the inexorable success of highly invasive exotic 2003). plants around the world. These invaders threaten the Plants damaged by herbivores are typically at a biological diversity and ecological integrity of natural competitive disadvantage, which provides the logical and ecosystems and may cause more than US$34 billion damage theoretical basis for biocontrol. However, plant response to a year in the United States alone (Pimentel et al. 2000). The herbivory is not a simple zero sum game for carbon and remarkable success of some invasive plant species is thought nutrients. Plants may compensate for biomass lost to to be the result of the lack of specialist consumers in the herbivory by growing faster via mechanisms not yet regions they invade; known as the Ôenemy release hypothe- understood (Trumble et al. 1993; Agrawal 2000), increase sisÕ (Maron & Vila` 2001; Keane & Crawley 2002; Mitchell & reproductive output (Paige & Whitham 1987; Paige 1999), Power 2003). Based on this hypothesis, biological control and undergo complex biochemical changes in response to insects have become important tools used to combat exotic herbivory. For instance, plants can actively respond to invasive plants. Biological control is a powerful management insect herbivory by emitting volatile chemicals (Baldwin & tool that has proved effective at controlling some invasive Schultz 1983; Thaler 1999; Farmer 2001) and the induction species (DeLoach 1991; McFadyen 1998) and so far is the of chemical defences. Some induced defence chemicals only realistic option for controlling invaders that are widely may enhance the competitive ability of attacked plants by 1Division of Biological Sciences, The University of Montana, 5Aldo Leopold Wilderness Research Institute, PO Box 8089, Missoula, MT 59812, USA Missoula, MT 59807, USA 2Department of Horticulture and Landscape Architecture, 6USDA-ARS-Northern Plains Agricultural Research Laboratory, Colorado State University, Fort Collins, CO 80523-1173, USA Sidney, MT 59270, USA 3Department of Biological Sciences, 4505 Maryland Parkway, *Correspondence: E-mail: [email protected] University of Nevada, Las Vegas, NV 89154, USA 4Department of Biology, Montana Tech of the University of Montana, Butte, MT 59701, USA Ó2005 Blackwell Publishing Ltd/CNRS 210 G. C. Thelen et al. acting as allelopathic or phytotoxic agents (Siemens et al. reproduction of Centaurea plants in plots infested with 2002). Agapeta was higher than in uninfested plots, suggesting a Allelopathy may play a role in some exotic plant invasions compensatory response, and Callaway et al. (1999) showed (Rabotnov 1982; Hierro & Callaway 2003; Callaway & that infestation correlated with stronger competitive effects of Ridenour 2004; Vivanco et al. 2004) and the exceptional C. maculosa. In addition to these effects of biocontrols, leaf competitive and invasive success of Centaurea maculosa herbivory by the generalist leaf feeder, Trichoplusia ni (spotted knapweed) appears to be in part the result of (cabbage looper), on C. maculosa appeared to enhance the allelopathic chemicals exuded from its roots (Ridenour & invader’s competitive effects against the native Festuca Callaway 2001; Bais et al. 2003) and its ability to compensate idahoensis. In artificial herbivory experiments, defoliation of for herbivore damage. Centaurea maculosa was introduced potted C. maculosa (up to four times in c. 6 months and up to from Eurasia, where it is not common, to North America, intensities of 75% of the leaves) had no effect on the final where it can form virtual monocultures (Ridenour & biomass of the defoliated plants (Kennett et al. 1992). Callaway 2001). It now occupies over 7 million acres in Many biological control insects are root feeders; however, the US (http://www.fs.fed.us/database/feis/plants/forb/ most ecological research on herbivory has focused on cenmac/all.html). Centaurea maculosa roots produce an insects that feed on aboveground tissues. For example, of enantiomeric compound, (±)-catechin, with clearly docu- 292 peer-reviewed articles recently published on insect mented phytotoxic properties (Bais et al. 2003). Greenhouse herbivory only four focused on root-feeding insects (Hunter experiments have demonstrated inhibitory effects of 2001). Despite the weak effects reported for Agapeta on C. maculosa roots on the roots and overall growth of a Centaurea, root-feeding insects can have dramatic deleterious native North American grass, and activated carbon added as effects on their hosts (Reichman & Smith 1991; Strong et al. a purification agent ameliorates these inhibitory effects 1995; Grayston et al. 2001). Of the 16 species of biocontrol (Ridenour & Callaway 2001), and experiments show the insects that have been introduced since the 1970s to limit inhibition of the growth and germination of native species the competitive effects of C. maculosa and its similar in field soils at natural concentrations of the allelochemical congener, C. diffusa (diffuse knapweed), five feed on the (Bais et al. 2003). ())-Catechin shows cell-specific targeting roots. The mechanisms by which moderate levels of root against meristmatic and elongation zone cells in the roots of herbivory on C. maculosa can stimulate the weed’s growth target plants, induction of reactive oxygen species (ROS)- (Mu¨ller-Scha¨rer 1991; Ridenour & Callaway 2003; Steinger related signalling that leads to rhizotoxicity in susceptible &Mu¨ller-Scha¨rer 1992) and more importantly, increase its plants, and allelochemical-induced genome-wide changes in competitive effects (Callaway et al. 1999) is not known. gene expression patterns. The concentrations of catechin Here, we ask if response of C. maculosa to herbivory is reported as phytotoxic on naı´ve species did not have an linked to its allelopathic effects, and explore the hypothesis effect on C. maculosa plants (Bais et al. 2003). that shoot herbivory, fungal infection and root herbivory by There is correlative evidence that biocontrol root two widely established biocontrol insects on C. maculosa may herbivores have at least weak negative effects on C. maculosa increase the competitive effects of the weed by stimulating populations (Story et al. 2000), but in general biocontrol the exudation of the allelopathic chemical (±)-catechin. insects have not yet been effective against the weed (Mu¨ller- Scha¨rer & Schroeder 1993). Furthermore, some evidence indicates that biocontrol herbivory may actually stimulate METHODS compensatory growth and may have counterintuitive and Experiment 1 unwanted effects. Mu¨ller (1989) found that C. maculosa plants increased fine root growth when infected by the Centaurea maculosa was planted from seed (n ¼ 44) in 2.4 L biocontrol insect, Agapeta zoegana, and did not decrease in pots filled with 25% field soil from Montana and 75% fecundity. Steinger & Mu¨ller-Scha¨rer (1992) found that the 20/30 grit sand. After allowing the plants to grow for biomass of C. maculosa seedlings grown in pots was not 40 days in the greenhouse we subjected them to two affected by Agapeta feeding, and attributed the lack of effect different biocontrol insect treatments, or to no herbivory. to compensatory root growth. In other experiments in the First, leaf damage was caused by or subjecting C. maculosa same study, however, the root-feeding weevil Cyphocleonus rosettes to herbivory by the cabbage looper moth (T. ni, achates reduced whole-plant biomass. In other field family Lepidoptera; a generalist native to Eurasia, wide- experiments in Switzerland, Mu¨ller-Scha¨rer (1991) found spread in the US but not used as a biocontrol for that low levels of Agapeta herbivory increased survival, shoot C. maculosa). We removed T. ni after 50% of the leaf tissue number and fecundity of C. maculosa, but the effects of was consumed, but if after 7 days plants had not lost 50% of herbivory were highly complex and were negative under their leaf tissue they were clipped to standardize 50% leaf other conditions. Ridenour & Callaway (2003) reported that loss. All plants in this treatment, however, experienced Ó2005
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