A Herbivorous Mite Down-Regulates Plant Defence and Produces Web to Exclude Competitors Renato A. Sarmento 1,2 , Felipe Lemos 3 , Cleide R. Dias 3 , Wagner T. Kikuchi 1 , Jean C. P. Rodrigues 1 , Angelo Pallini 3 , Maurice W. Sabelis 2 , Arne Janssen 2 * 1 Graduate Programme in Plant Science, Federal University of Tocantins (UFT), Gurupi, Tocantins, Brazil, 2 Section Population Biology, Institute for Biodiversity and Ecosystem Dynamics, University of Amsterdam, Amsterdam, The Netherlands, 3 Department of Entomology, Federal University of Vic ¸osa, Vic ¸osa, Brazil Abstract Herbivores may interact with each other through resource competition, but also through their impact on plant defence. We recently found that the spider mite Tetranychus evansi down-regulates plant defences in tomato plants, resulting in higher rates of oviposition and population growth on previously attacked than on unattacked leaves. The danger of such down- regulation is that attacked plants could become a more profitable resource for heterospecific competitors, such as the two- spotted spider mite Tetranychus urticae. Indeed, T. urticae had an almost 2-fold higher rate of oviposition on leaf discs on which T. evansi had fed previously. In contrast, induction of direct plant defences by T. urticae resulted in decreased oviposition by T. evansi. Hence, both herbivores affect each other through induced plant responses. However, when populations of T. evansi and T. urticae competed on the same plants, populations of the latter invariably went extinct, whereas T. evansi was not significantly affected by the presence of its competitor. This suggests that T. evansi can somehow prevent its competitor from benefiting from the down-regulated plant defence, perhaps by covering it with a profuse web. Indeed, we found that T. urticae had difficulties reaching the leaf surface to feed when the leaf was covered with web produced by T. evansi. Furthermore, T. evansi produced more web when exposed to damage or other cues associated with T. urticae. We suggest that the silken web produced by T. evansi serves to prevent competitors from profiting from down- regulated plant defences. Citation: Sarmento RA, Lemos F, Dias CR, Kikuchi WT, Rodrigues JCP, et al. (2011) A Herbivorous Mite Down-Regulates Plant Defence and Produces Web to Exclude Competitors. PLoS ONE 6(8): e23757. doi:10.1371/journal.pone.0023757 Editor: Anna Traveset, Institut Mediterrani d’Estudis Avanc ¸ats (CSIC/UIB), Spain Received April 21, 2011; Accepted July 24, 2011; Published August 24, 2011 Copyright: ß 2011 Sarmento et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This research was supported in part by CNPq-Brazil. RAS received a scholarship from WOTRO-NWO (project W82-281), AJ received a scholarship from FAPEMIG, Brazil (PVE), AP from CNPq, Brazil. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: arne.janssen@uva.nl Introduction Interspecific competition occurs when adding individuals of one species reduces the population size of another species that shares the same resource [1,2]. Herbivores may directly affect individuals of other species that share the same host plant through inter- ference competition and indirectly by reducing the food quantity of the shared host (exploitative competition). Herbivores compet- ing for plants may also affect individuals of the other species indirectly by altering the quality of the shared host plant [3] through induction of changes in the primary and secondary chemistry of the shared host plant, which in turn affects the competitor’s performance [4,5,6,7]. For instance, herbivores are known to induce plant defences [5,8,9,10,11], and these plant defences may negatively affect the performance of other her- bivores on the same plant [3,12]. The induction of such plant defences and the tolerance to them by a herbivore species may determine the outcome of its competition with other, less tolerant herbivores. Alternatively, plants can also become more susceptible to attacks by herbivores after previous attacks by other species of herbivores [5]. In these cases, negative cross-talk between defensive pathways may be involved [13]. In this article, we report on the interactions between the herbivorous spider mite Tetranychus evansi Baker & Pritchard (Acari: Tetranychidae) and Tetranychus urticae Koch (Acari: Tetranychidae) on tomato plants. It is well known that T. urticae induces plant defences resulting in reduced performance on previously attacked plants [3], including tomato [10,14,15]. We recently found that T. evansi down-regulates plant defences in the leaves of tomato plants, resulting in an increased performance of T. evansi on plants attacked by conspecifics [16]. Hence, this is exactly the opposite pattern as for T. urticae and many other species [17,18,19]. The danger of such down-regulation is that plants could also become a more profitable resource for heterospecific competitors such as T. urticae. We investigated whether this competing species could indeed profit from the changes in tomato plants induced by T. evansi, and how T. evansi can prevent its competitors from profiting. In many parts of the world, both T. evansi and T. urticae are important pests of solanaceous crops, and attack tomato plants (Solanum lycopersicum), on which they can potentially compete [20,21,22]. Many spider mites produce a silken web over the leaves they feed on and the offspring they produce [23]. This web is hypothesized to serve as a defence against predators, and indeed, many predator species are incapable of penetrating the dense web produced by some spider mite species [24]. However, it is possible that the web also affects interspecific interactions among herbivore species, i.e. that it also offers protection against competitors [25]. PLoS ONE | www.plosone.org 1 August 2011 | Volume 6 | Issue 8 | e23757