Associational Resistance and Associational Susceptibility: Having Right or Wrong Neighbors

Specific plant associations may decrease (associational resistance, AR) or increase (associational susceptibility, AS) the likelihood of detection by, and/or vulnerability to, herbivores. We discuss presumed mechanisms leading to AR and AS, suggest others, and conduct meta-analyses on plant and herbivore traits affecting AR and AS, and the effects of habitat. Specific plant associations determine the likelihood of detection and/or vulnerability of focal plants to herbivores. AS is more likely with insects and AR more likely with mammals. Unpalatable neighbors increase the likelihood of AR. An herbivore’s feeding guild, diet breadth, and habitat type do not influence the likelihood of AR or AS. The effectiveness of AR in reducing herbivore abundance is independent of whether neighboring plants are within a plot of focal crops or along the edge of a plot. AR and AS may be applicable to associations among herbivores, and may be appropriately studied from a landscape perspective. 1 Review in Advance first posted online on August 25, 2009. (Minor changes may still occur before final publication online and in print.) A nn u. R ev . E co l. E vo l. Sy st . 2 00 9. 40 . D ow nl oa de d fr om a rj ou rn al s. an nu al re vi ew s. or g by M ic hi ga n St at e U ni ve rs ity L ib ra ry o n 09 /2 2/ 09 . F or p er so na l u se o nl y. ANRV393-ES40-01 ARI 18 August 2009 19:53 INTRODUCTION: THE HISTORY OF THE CONCEPTS OF ASSOCIATIONAL RESISTANCE AND ASSOCIATIONAL SUSCEPTIBILITY In this review, we focus on direct and indirect interactions between plants in close proximity, in which the influence of one plant on another (hereafter referred to as the focal plant) increases (associational susceptibility, henceforth AS) or decreases (associational resistance, AR) the likelihood of detection by, and/or vulnerability of a focal plant to, herbivores (above and beyond its innate ability to avoid detection or damage owing to herbivory). The outcomes of these plant-plant interactions are viewed from a phytocentric perspective and, thus, typically measured as changes in the degree of herbivory and/or abundance of herbivores. Root and colleagues (Root 1973, Tahvanainen & Root 1972) were among the earliest to affirm the importance of specific plant-plant associations in the likelihood that a plant will be detected and/or vulnerable to herbivory. Atsatt & O’Dowd (1976) discussed AR, stressing the importance of the right kind of diversity, that is, suggesting that not all plant species diversity results in changes in detection by, and/or vulnerability to, herbivores. They also suggested [and Evans 1983, Wada et al. 2000, and Karban & Maron (2002) later demonstrated] that adjacent plants conferring AR could be conspecifics that differ in some fashion, as well as individuals of different species. To date, AR and AS have been demonstrated in terrestrial plants affected by vertebrate (Hjältén et al. 1993, McNaughton 1978) and invertebrate herbivores (Finch et al. 2003), in marine algaemesograzer interactions (Hay 1986, Pfister & Hay 1988) and in mussel-plant epiphyte interactions (Laudien & Wahl 1999), and speculated for sponges (Wulff 1997) and phytoplankton (Steiner 2001). Thus, AR and AS are widespread ecological interactions, although AS has been reported less frequently (but see Parker & Root 1981, Rand 1999, Thomas 1986, White & Whitham 2000). Contrasting Associational Resistance, Associational Susceptibility, and Other Basic Ecological Interactions Fundamental ecological associations include consumer-resource interactions, competition, mutualism, amensalism, commensalism, facilitation, epibiosis, and, we would add, AR and AS. All of these interactions are commonly contrasted based on whether the interaction is favorable, detrimental, or neutral for the interacting species (that is, +/−, +/+, −/−, +/0, −/0). Thus, consumer-resource interactions are +/−, competitive interactions −/−, amensalisms −/0, and commensalism +/0. AR, AS, and the two closely related interactions, facilitation and epibiosis can be similarly described. In AR, the outcome of the interaction is + for a focal plant, with regard to avoidance of detection and reduction of herbivore damage, and – in AS. The impact on neighboring plants can be 0, +, or −. Epibiosis is a relationship in which one (epiphytic) organism lives attached to another and may be benefited or harmed as a result of the intimate relationship, depending on the influence of the substrate species (Wahl & Hay 1995). Facilitation involves associations between species that benefit at least one species and cause no harm to the associated species (Stachowicz 2001). Thus, some facilitation interactions can be described as AR if the benefit accrued is protection from herbivory (Callaway 1995) and some epibiosis can result in AR or AS if attachment increases or decreases herbivory of the plant epiphyte (Hay 1986, Wahl & Hay 1995). (For further details see Supplemental Text 1. Follow the Supplemental Material link in the online version of this article or at http://www.annualreviews.org/.) Although AR and AS (like other interactions such as consumer-resource interactions, competition, mutualism, and so on) involve interactions between two organisms (that is, plants), the outcome of the interactions affect, and is affected by, a third (herbivorous) species. We previously 2 Barbosa et al. R E V I E W S