Associational effects against a leaf beetle mediate a minority advantage in defense and growth between hairy and glabrous plants

Abstract

Based on the accumulation of evidence, the risk of herbivory depends not only on the traits of a plant but also on those of neighboring plants. Despite the potential importance of frequency-dependent interactions in the evolutionary stability of anti-herbivore defense, we know little about such associational effects between defended and undefended plants within a species. In this study, we determined whether the intraspecific associational effects against the oligophagous leaf beetle, Phaedon brassicae, caused a minority advantage in defense and growth between trichome-producing (hairy) and trichomeless (glabrous) plants of Arabidopsis halleri subsp. gemmifera. We experimentally demonstrated that the magnitude of herbivory and the number of adult beetles on hairy plants decreased when hairy plants were a minority, whereas the leaf damage and the beetle abundance did not differ between hairy and glabrous plants when glabrous plants were a minority. By contrast, the larvae of P. brassicae occurred less when hairy plants were a majority. We also found a reciprocal minority advantage in the biomass production for both hairy and glabrous plants. Additionally, the adults tended to attack glabrous leaves more rapidly than hairy ones, particularly when the beetles were starved or experienced glabrous diets. Furthermore, in the absence of herbivory, the growth of hairy plants tended to be slower than glabrous plants, which indicated a cost for the production of trichomes. Our study suggests that associational effects are a mechanism for the maintenance of trichome dimorphism by contributing to negative frequency-dependent growth.

Strong but opposing effects of associational resistance and susceptibility on defense phenotype in an African savanna plant

“…The Mpala Research Centre and Conservancy (MRC) encompasses ~20 000 ha of thorn‐scrub savanna and dry woodland in Kenya's Laikipia County (0°36′4″N, 36°87′8″E), two‐thirds of which is underlain by red sandy loams (Pringle et al ). The plant community on this soil type consists of a discontinuous overstory dominated by spinescent Acacia trees ( A. brevispica , A. etbaica and A. mellifera ) and an understory comprising various species of grasses, forbs and subshrubs (Goheen et al 2013).…”

“…Although spines and thorns are known to deter large mammals from browsing savanna trees and shrubs (Cooper and Owen‐Smith , Charles‐Dominique et al ), the efficacy of physical defenses against large browsers in understory plants has received less study. We therefore tested 1) whether prickles are an effective deterrent against herbivores, 2) whether leaves with more prickles have less undefended area at the leaf tip and 3) whether the presence of prickles confined herbivory to the tips of leaves.…”

“…Refuge and non‐refuge habitats differ not only in browsing pressure, but also various abiotic conditions (e.g. photosynthetically available radiation, soil moisture, soil nutrients) which may contribute to variation in defense phenotype (Coverdale et al , 2018). Thus, to assess whether variation in herbivory damage alone was sufficient to drive intraspecific patterns of defense investment within versus outside associational refuges, we measured average prickle density on unassociated S. campylacanthum plants in the fenced exclosure plots and unfenced control plots of the GLADE (n = 15 plants/plot × two blocks) and southern UHURU (n = 10 plants/plot × three blocks) exclosure experiments.…”

“…We investigated whether associational resistance and associational susceptibility cause predictable shifts in plant defense phenotype in a semi‐arid Kenyan savanna. At our study site, proximity to physically defended Acacia trees significantly reduces herbivory on understory plants (Coverdale et al , 2018), whereas plants growing in clearings dominated by palatable, short‐statured grasses are exposed to more intense mammalian herbivory (Augustine and McNaughton , Veblen 2012, Ford et al 2014). Here, we quantified the effects of associational resistance (occurring at the scale of individual Acacia tree canopies; ~ 5–20 m 2 ) and susceptibility (occurring at the scale of treeless, grassy clearings; ~ 5000–20 000 m 2 ) on the defense phenotype of Solanum campylacanthum .…”

“…This abundant, perennial subshrub produces recurved prickles (~ 5 mm long) along the leaf midrib and stems as a primary physical defense (Pringle et al 2014). Because the efficacy of physical defenses in understory plants has not been as well characterized as those of trees and shrubs in African savannas (Young , Gowda et al , Charles‐Dominique et al ), we began by investigating the hypothesis (H 1 ) that S. campylacanthum prickles deter large mammalian browsers. We then used a combination of surveys and experimental manipulations to characterize patterns of defense investment across associational contexts.…”