Intraspecific interaction of host plants leads to concentrated distribution of a specialist herbivore through metabolic alterations in the leaves

Abstract

Recent studies suggest that changes in leaf traits due to interactions between plants affect resource utilisation by herbivores, as well as herbivore distribution. However, this has not yet been confirmed experimentally. Here, we investigated the effects of phenotypic plasticity in leaf traits of Rumex obtusifolius (host plant) in response to intraspecific and interspecific interactions on the distribution of two leaf beetles, Gastrophysa atrocyanea (specialist herbivore) and Galerucella grisescens (generalist herbivore). We investigated the local population density of R. obtusifolius plants and the presence of leaf beetles on the plants at five study sites. Leaf chemicals (condensed tannins and total phenolics) were compared between aggregated and solitary R. obtusifolius plants. To clarify the effects of the interaction environment of R. obtusifolius plants on their leaf traits and on resource utilisation by the leaf beetles, we compared leaf chemicals and preferences of adult leaf beetles among treatments where R. obtusifolius experienced intraspecific interaction, interspecific interaction or no interaction in cultivation experiments. Finally, we evaluated the independent and combined effects of patch size and intraspecific interaction on leaf beetle distribution in mesocosm experiments. In the field, the presence of the specialist leaf beetle G. atrocyanea was positively correlated with the local population density (rosette overlap ratio) of R. obtusifolius plants; however, there was no correlation in the case of the generalist leaf beetle G. grisescens. In the cultivation experiments, plants in the intraspecific interaction treatment increased their leaf concentrations of condensed tannins and total phenolics, and G. atrocyanea consumed more of these leaves than leaves in other treatments. Similar results were observed in the field. In the mesocosm experiments, larger numbers of G. atrocyanea were distributed on R. obtusifolius plants exposed to below‐ground intraspecific interaction than on plants not exposed to intraspecific interaction. Our results provide experimental evidence that leaf‐trait changes in response to intraspecific interaction between host plants influence specialist herbivore distribution. This highlights the need to integrate plant–plant interactions into our understanding of plant–animal interactions. A free Plain Language Summary can be found within the Supporting Information of this article.

Effects of indirect plant–plant interaction via root exudate on growth and leaf chemical contents in Rumex obtusifolius

“…More specifically, we hypothesized that the concentrations of secondary chemicals in leaves of R. obtusifolius are increased in response to exposure to root exudates from plants of the same species, but not to those from plants of other species. Conversely, if our previous results 9 depended not only on indirect interactions mediated by root exudates but also on other interactions, such as direct contact and resource competition, the effects of these indirect root-exudate-mediated interactions on leaf traits may differ from those of direct plant–plant interactions.…”

“…The experiment duration, water and soil conditions, and growth conditions were similar to those in the direct interaction experiment in our previous work. 9 …”

“…Plant–plant interactions are an important part of terrestrial ecosystems because they affect not only the outcome of competition between plants, 1 , 2 but also functional leaf traits, 3–7 hervibory, 8 , 9 and herbivore distributions. 9 In a previous study, we experimented with Rumex obtusifolius (Polygonaceae) to examine the effects of intraspecific, interspecific, and no belowground direct interactions on leaf chemical content and herbivore distribution. 9 Plants exposed to intraspecific direct interaction had increased total phenolic and condensed tannin concentrations in their leaves, and induced a concentrated specialist herbivore distribution on the leaves.…”

“… 9 In a previous study, we experimented with Rumex obtusifolius (Polygonaceae) to examine the effects of intraspecific, interspecific, and no belowground direct interactions on leaf chemical content and herbivore distribution. 9 Plants exposed to intraspecific direct interaction had increased total phenolic and condensed tannin concentrations in their leaves, and induced a concentrated specialist herbivore distribution on the leaves. A wide variety of plant parts (e.g., leaves, roots, and seeds) and media (e.g., volatile chemicals, nonvolatile chemicals, light, and soil microorganisms) are involved in plant–plant interactions.…”

“… 13 Moreover, similar root behavior was observed in an experiment in which root exudate reduced both root growth and clonal reproduction in non-self, competitor plants. On the basis of these findings, we hypothesized that, if these results depend on indirect interactions mediated by root exudates, R. obtusifolius leaf chemical contents, which are linked to herbivore distribution in an ecosystem, 9 depend on the recognition of conspecific neighbors via root exudates . More specifically, we hypothesized that the concentrations of secondary chemicals in leaves of R. obtusifolius are increased in response to exposure to root exudates from plants of the same species, but not to those from plants of other species.…”