The role of biotic interactions in determining metal hyperaccumulation in plants

Abstract

Abstract Heavy metal hyperaccumulation (MH) is a rare trait found in plant species that inhabit metal‐contaminated soils. Two main hypotheses proposed to explain the selective advantage of MH are the elemental defence hypothesis and elemental allelopathy hypothesis. The elemental defence hypothesis suggests that MH functions as defence against herbivores while the elemental allelopathy hypothesis suggests that MH acts to inhibit the growth of neighbours. Nevertheless, these hypotheses are not likely to be mutually exclusive. Here, we present the first study to test both hypotheses simultaneously. We examined these hypotheses with the Cd hyperaccumulator, Arabidopsis halleri, which inhabits both metalliferous and non‐metalliferous soils, thus providing an opportunity to test the hypotheses of both habitats. Arabidopsis halleri plants originating from several populations in both metalliferous and non‐metalliferous soils were grown in a greenhouse in soils with or without cadmium (Cd). Their leaves were used in a feeding experiment with a specialist herbivore and in a set of leaf‐leachate experiments that tested their effect on seed germination and seedling establishment of species co‐occurring with A. halleri. Finally, a field survey in several A. halleri populations was conducted to compare herbivore load between A. halleri and neighbours from metalliferous versus non‐metalliferous soils. Results of the feeding experiment and field survey suggest that Cd accumulation in A. halleri leaves could provide it with defence against herbivores. Results of the leaf‐leachate experiments reveal that Cd accumulation has no effect on seed germination of neighbouring species but inhibits seedling establishment, particularly of plant species originating from non‐metalliferous soils. Our results suggest that both herbivores and competing neighbours may jointly select for MH in plants. Moreover, MH could provide a selective advantage particularly in non‐metalliferous soils, where neighbouring plants lack metal tolerance. These results highlight the importance of including different origins and populations of both the target species and its neighbouring plant species when studying the ecological role of MH. A free Plain Language Summary can be found within the Supporting Information of this article.