Good neighbors make good defenses: associational refuges reduce defense investment in African savanna plants

Abstract

Intraspecific variation in plant defense phenotype is common and has wide-ranging ecological consequences. Yet prevailing theories of plant defense allocation, which primarily account for interspecific differences in defense phenotype, often fail to predict intraspecific patterns. Furthermore, although individual variation in defense phenotype is often attributed to ecological interactions, few general mechanisms have been proposed to explain the ubiquity of variable defense phenotype within species. Here, we show experimentally that associational refuges and induced resistance interact to create predictable intraspecific variation in defense phenotype in African savanna plants. Physically defended species from four families (Acanthaceae, Asparagaceae, Cactaceae, and Solanaceae) growing in close association with spinescent Acacia trees had 39-78% fewer spines and thorns than did isolated conspecifics. For a subset of these species, we used a series of manipulative experiments to show that this variability is maintained primarily by a reduction in induced responses among individuals that seldom experience mammalian herbivory, whether due to association with Acacia trees or to experimental herbivore exclusion. Unassociated plants incurred 4- to 16-fold more browsing damage than did associated individuals and increased spine density by 16-38% within one month following simulated browsing. In contrast, experimental clipping induced no net change in spine density among plants growing beneath Acacia canopies or inside long-term herbivore exclosures. Associated and unassociated individuals produced similar numbers of flowers and seeds, but seedling recruitment and survival were vastly greater in refuge habitats, suggesting a net fitness benefit of association. We conclude that plant-plant associations consistently decrease defense investment in this system by reducing both the frequency of herbivory and the intensity of induced responses, and that inducible responses enable plants to capitalize on such associations in heterogeneous environments. Given the prevalence of associational and induced defenses in plant communities worldwide, our results suggest a potentially general mechanism by which biotic interactions might predictably shape intraspecific variation in plant defense phenotype.

Intraspecific neighbourhood effect: Population‐level consequence of aggregation of highly defended plants

“…As a result, intraspecific neighbourhood effects varied unimodally with respect to aggregation of high‐nicotine plants, with a peak at intermediate density. Although a number of studies have discussed potential mechanisms of neighbourhood effects (mostly interspecific effects; Andow, ; Barbosa et al, ), a very few studies have reported the operation of multiple mechanisms that simultaneously work in a spatial context (but see Coverdale et al, ; Kim & Underwood, ). Kim and Underwood () stressed that frequency‐dependent neighbourhood effects could be nonlinear.…”

“…resource concentration; Root, 1973) and delay a patch-leaving decision (Stephens & Krebs, 1986;Waage, 1979). Thus, neighbourhood effects caused by the repellent effects of nicotine varied depending on aggregation of highly Andow, 1991;Barbosa et al, 2009), a very few studies have reported the operation of multiple mechanisms that simultaneously work in a spatial context (but see Coverdale et al, 2018;Kim & Underwood, 2015). Kim and Underwood (2015)…”

“…associational effect; Underwood et al, 2014), there has been less attention to conspecific neighbours (Agrawal, Lau, & Hambäck, 2006;Andow, 1991;Barbosa et al, 2009). In this context, more recent studies have argued that intraspecific variations in biological environments caused by local spatial distribution of plants and their phenotypic and/or genotypic variations can also induce neighbourhood effects (Coverdale, Goheen, Palmer, & Pringle, 2018;Ida et al, 2018;Koricheva & Hayes, 2018;Sato & Kudoh, 2015). For instance, plant genotypic diversity could influence visits of arthropods, including herbivores and predators, to host plants and alter associated arthropod communities (Crutsinger et al, 2006;Wetzel, Aflitto, & Thaler, 2018).…”

A thorny issue: Woody plant defence and growth in an East African savanna

“…The lack of investment in N‐free secondary metabolites by the second broad‐leaved species, G. tenax , was also surprising, but consistent with our finding that growth of this species is severely negatively affected by large browsers, and with previous work showing substantial declines in all size classes of G. tenax in the presence of browsers in this savanna (Augustine & McNaughton, ; Sankaran et al, ). Rather than employing any form of costly chemical defence, this species appears to coexist (uneasily) with browsers by increasing the complexity of its branching architecture (BI), and growing in close association with other thorny species that create structural refugia where G. tenax saplings are protected from browsers (personal observation by all authors, see also Coverdale, Goheen, Palmer, & Pringle, ). One value of this strategy is that when browsing pressure is removed or low, the lack of investment in costly defences, combined with high leaf N, allows for rapid growth.…”

Defensive chemicals of neighboring plants limit visits of herbivorous insects: Associational resistance within a plant population

“…Most previous studies have considered only associational effects involved in interspecific interactions, such as plant species diversity (e.g., Andow, 1991). Similar arguments on associational effects would also apply to intraspecific interaction, that is, interactions among conspecific plants with different phenotypes and/or genotypes (Champagne et al, 2018;Coverdale, Goheen, Palmer, & Pringle, 2018). For example, within a population of Solidago altissima, genotypic diversity of co-occurring plants decreased herbivory on the focal plants (i.e., associational resistance), although the mechanism was unclear (Genung, Crutsinger, Bailey, Schweitzer, & Sanders, 2012).…”