Associational antiherbivore defense promotes the coexistence of hairy and glabrous plants

Background/Question/Methods

Evidence is now accumulating that herbivory risk depends not only on a plant’s own phenotype but also on those of neighboring plants. Such “associational effects” of antiherbivore defense play a key role in the coexistence of multiple plant species because they may cause local frequency dependence in plant defense and growth. This view of associational effects has rarely been applied to defense polymorphism within a plant species. In this context, trichome-producing (hairy) and trichomeless (glabrous) plants of Arabidopsis halleri subsp. gemmifera provide a suitable system to examine intraspecific associational effects, owing to their genetically determined, visible, and discrete phenotype. The purpose of this study was to test whether associational effects can cause a rare-type advantage in the defense and/or growth of hairy and glabrous plants. First, in a herbivore feeding assay and greenhouse experiment, we manipulated the frequency of hairy and glabrous phenotypes. Then, in a field survey, we examined the relationship between leaf damage and the frequency of the two plant types in a series of small patches. As a herbivore species, we used an oligophagous leaf beetle, Phaedon brassicae, which is an important herbivorous insect of natural populations of A. halleri.

Results/Conclusions

The feeding assay illustrated that adult beetles avoided hairy leaves when glabrous leaves became abundant, whereas the preference of the beetles did not differ when hairy leaves were abundant. Consistent with the feeding assay, our greenhouse experiment showed that hairy plants harbored fewer adult beetles only when hairy plants were rare. Hairy plants also incurred less herbivory when they were rare in the greenhouse experiment. In this experiment, we found the rare-type advantage in the biomass production of both hairy and glabrous plants. In a natural population where the leaf beetle was predominant, leaf damage on hairy plants decreased as the frequency of glabrous plants increased in a patch. Conversely, there was no significant relationship between the leaf damage on glabrous plants and the frequency of glabrous plants. Furthermore, the frequency of rare types of plants increased within a patch between two years. In terms of the rare-type advantage in herbivory and growth, we suggest that associational effects may be potentially important as an ecological mechanism maintaining polymorphism in a physical defense trait.