Root herbivory affects oviposition and feeding behavior of a foliar herbivore

Behavioral Ecology doi:10.1093/beheco/arr124 Advance Access publication 16 July 2011 Original Article Root herbivory affects oviposition and feeding behavior of a foliar herbivore P. Anderson,a M.M. Sadek,a,b and F.L. Wäckersc Division of Chemical Ecology, Department of Plant Protection Biology, Swedish University of Agricultural Sciences, Box 102, SE-230 53 Alnarp, Sweden, bDepartment of Zoology, Faculty of Science, Assiut University, Assiut 71516, Egypt, and cSustainable Agriculture Centre, Lancaster Environmental Centre, Lancaster University, Lancaster LA1 4YQ, UK a Performance and distribution of phytophagous insects are driven by direct and indirect competitive interactions. Plant-feeding arthropods have been shown to interact indirectly through the plants’ response to herbivory. In the case of systemically induced plant responses, this interaction extends to herbivores inhabiting different parts of a plant, for example, above- and belowground herbivores. Plant-induced responses elicited by root herbivores have been shown to affect feeding and development of aboveground herbivores. However, little is known about how root feeding affects host choice behavior of aboveground herbivores, including both adult oviposition behavior and larval host acceptance. Here, we report that root feeding by the wireworm, Agriotes lineatus, influences oviposition decisions and larval leaving rate of an aboveground herbivore, Spodoptera littoralis. In choice experiments, female S. littoralis deposited more and larger egg batches on undamaged plants when compared with wireworminfested plants. In a larval feeding experiment, a higher percentage S. littoralis larvae moved away from the wireworm-infested plant onto a neighboring undamaged plant as compared with larvae feeding on previously undamaged plants. Larvae did not show an increased tendency to leave when feeding on plants previously exposed to conspecific larvae. Our results show that indirect interactions between belowground and aboveground herbivores extend to behavioral avoidance, both in terms of oviposition and larval feeding decisions. This allows the foliar herbivore to avoid systemic plant responses elicited by root herbivory, which likely represent reduced food quality and increased apparency toward natural enemies. Key words: aboveground–belowground interactions, induced resistance, interspecific competition. [Behav Ecol 22:1272–1277 (2011)] INTRODUCTION erbivorous insects need to find suitable host plants for oviposition and larval feeding. In addition to finding the right plant species, they also need to assess the quality of the individual plants within a given species. Host plant choice in insects is governed by many factors (Bernays 2001). Factors directly relating to the nutritional quality of the food plant include the levels of primary as well as secondary metabolites. Although the former category includes basic nutrients, secondary metabolites can interfere with digestion or act as toxins. In addition, host plant choice may be driven by ecological factors, such as competition and mortality risk. Inter- and intraspecific competitive interactions have recently been identified as important drivers of the performance and distribution of phytophagous insects (Kaplan and Denno 2007). These interactions can be direct, for example, through interference and exploitative competition. However, many interactions between herbivores were found to be indirect, often mediated by plant responses to herbivory (Ohgushi 2005; Kaplan and Denno 2007). These indirect interactions depend on the spatial distribution and the temporal persistence of the plant response (Wäckers and Bezemer 2003; Kaplan and Denno 2007). H Address correspondence to P. Anderson. E-mail: peter.anderson@ slu.se. Received 20 December 2010; revised 3 June 2011; accepted 13 June 2011.
The Author 2011. Published by Oxford University Press on behalf of the International Society for Behavioral Ecology. All rights reserved. For permissions, please e-mail: Many plants respond to herbivory by activating induced resistance mechanisms. Induced resistance may benefit plants in 3 ways. First, it can reduce the plant’s attractiveness to ovipositing herbivores. Second, it can reduce herbivory by the phytophagous stages (larvae and/or adults). Third, it may allow plants to unload larval herbivores onto neighboring plants with which the induced plant competes for light and nutrients (Edwards and Wratten 1983; Tuomi et al. 1994; van Dam et al. 2001). Induced resistance mechanisms include the production of both volatile and nonvolatile secondary metabolites (Karban and Baldwin 1997; Turlings and Wäckers 2004). These herbivore-induced compounds can be a key factor in mediating herbivore–herbivore interactions and in structuring insect communities (Kessler and Baldwin 2004). Only few studies to date have linked plant-mediated competition between herbivores to the well-documented induction of plant secondary metabolites in response to herbivory (Kaplan and Denno 2007). For example, it has been shown that wild radish plants damaged by Pieris rapae show increased glucosinolate levels, corresponding with poorer performances by Lepidoptera, aphids, and a leafminer (Agrawal 1999). Herbivore damage induced volatiles as well as extrafloral nectar have been shown to be widely exploited by natural enemies of herbivorous insects to locate plants with host prey (e.g., Dicke et al. 2003; Turlings and Wäckers 2004). There are also examples showing that these volatiles can be attractive or deterrent to herbivorous insects (e.g., Bolter et al. 1997; De Moraes et al. 2001; Kessler and Baldwin 2001). However, relatively, little is known about how herbivores respond to Anderson et al. • Root herbivory affects foliar herbivore behaviors damage-induced changes in plant chemistry during host plant choice (Dicke et al. 2003). Most studies on host plant choice have focused on aboveground interactions (van Dam et al. 2003). There is increasing appreciation that induced plant responses can also drive interactions between organisms below- and aboveground (e.g., van der Putten et al. 2001; Wardle et al. 2004; Bezemer and van Dam 2005; Erb et al. 2008). There are now many examples showing that the growth and development, and one example where oviposition decisions (Soler et al. 2010), of aboveground herbivores are affected by belowground herbivory. Furthermore, it has been shown that belowground herbivory can induce changes in the plant that influence the behavior and performance of natural enemies of aboveground herbivores (Wäckers and Bezemer 2003; Rasmann and Turlings 2007; Soler et al. 2007). In cotton, a number of studies have linked secondary metabolite induction to adverse fitness consequences for the inducing herbivore (Alborn et al. 1996; McAuslane and Alborn 2000; Bezemer et al. 2003). Induction of terpenoid aldehydes in cotton has also been reported to underlie plant-mediated in (...truncated)