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Extraordinarily high leaf metal concentrations in metal hyperaccumulator plants may serve as an elemental defence against herbivores. However, mixed results have been reported and studies using comparative approaches are missing. We investigated the deterrent and toxic potential of metals employing the hyperaccumulator Arabidopsis halleri. Effects of zinc (Zn) and cadmium (Cd) on the preferences of three Brassicaceae specialists were tested in paired-choice experiments using differently treated plant material, including transgenic plants. In performance tests, we determined the toxicity and joint effects of both metals incorporated in an artificial diet on the survival of a generalist. Feeding by all specialists was significantly reduced by metal concentrations from above 1000 μg Zn g−1 DW and 18 μg Cd g−1 DW. By contrast, metals did not affect oviposition. Generalist survival decreased with increasing concentrations of individual metals, whereby the combination of Zn and Cd had an additive toxic effect even at the lowest applied concentrations of 100 μg Zn g−1 and 2 μg Cd g−1. Metal hyperaccumulation protects plants from herbivory resulting from deterrence and toxicity against a wide range of herbivores. The combination of metals exacerbates toxicity through joint effects and enhances elemental defence. Thus, metal hyperaccumulation is ecologically beneficial for plants.

Some plants are able to accumulate in their shoots metals at levels that are toxic to most other organisms. This ability may serve as a defence against herbivores. Therefore, both metal-based and organic defences may affect herbivores. However, how metal accumulation affects the interaction between herbivores and organic plant defences remains overlooked. To fill this gap, we studied the interactions between tomato ( ), a model plant that accumulates cadmium, and two spider-mite species, and that, respectively, induce and suppress organic plant defences, measurable via the activity of trypsin inhibitors. We exposed plants to different concentrations of cadmium and measured its effects on mites and plants. In the plant, despite clear evidence for cadmium accumulation, we did not detect any cadmium effects on traits that reflect the general response of the plant, such as biomass, water content, and carbon/nitrogen ratio. Still, we found effects of cadmium upon the quantity of soluble sugars and on leaf reflectance, where it may indicate structural modifications in the cells. These changes in plant traits affected the performance of spider mites feeding on those plants. Indeed, the oviposition of both spider mite species was higher on plants exposed to low concentrations of cadmium than on control plants, but decreased at concentrations above 0.5 mM. Therefore, herbivores with contrasting responses to organic defences showed a similar hormetic response to metal accumulation by the plants. Additionally, we show that the induction and suppression of plant defences by these spider-mite species was not affected by the amount of cadmium supplied to the plants. Furthermore, the effect of cadmium on the performance of spider mites was not altered by infestation with or . Together, our results suggest no interaction between cadmium-based and organic plant defences, in our system. This may be useful for plants living in heterogeneous environments, as they may use one or the other defence mechanism, depending on their relative performance in each environment.

Soil pollution by metals and metalloids as a consequence of anthropogenic industrialisation exerts a seriously damaging impact on ecosystems. However, certain plant species, termed hyperaccumulators, are able to accumulate extraordinarily high concentrations of these metal(loid)s in their aboveground tissues. Such hyperaccumulation of metal(loid)s is known to act as a defence against various antagonists, such as herbivores and pathogens. We investigated the influences of metal(loid)s on potential defence traits, such as foliar elemental, organic and mechanical defences, in the hyperaccumulator plant species Arabidopsis halleri (Brassicaceae) by artificially amending the soil with common metallic pollutants, namely cadmium (Cd) and zinc (Zn). Additionally, unamended and metal-amended soils were supplemented with the metalloid silicon (Si) to study whether Si could alleviate metal excess. Individuals originating from one non-/low- and two moderately to highly metal-contaminated sites with different metal concentrations (hereafter called accessions) were grown for eight weeks in a full-factorial design under standardised conditions. There were significant interactive effects of metal amendment and Si supplementation on foliar concentrations of certain elements (Zn, Si, aluminium (Al), iron (Fe), potassium (K) and sulfur (S), but these were accession-specific. Profiles of glucosinolates, characteristic organic defences of Brassicaceae, were distinct among accessions, and the composition was affected by soil metal amendment. Moreover, plants grown on metal-amended soil contained lower concentrations of total glucosinolates in one of the accessions, which suggests a potential trade-off between inorganic defence acquisition and biosynthesis of organic defence. The density of foliar trichomes, as a proxy for the first layer of mechanical defence, was also influenced by metal amendment and/or Si supplementation in an accession-dependent manner. Our study highlights the importance of examining the effects of co-occurring metal(loid)s in soil on various foliar defence traits in different accessions of a hyperaccumulating species.

Elemental hyperaccumulation may have several functions, including plant defense against natural enemies. A total of 34 studies, including 72 experimental tests, have been conducted to date. At least some tests have demonstrated defense by hyperaccumulated As, Cd, Ni, Se and Zn, but relatively few plant taxa and natural enemies have been investigated. Defense by hyperaccumulated Ni has been shown for most leaf/root chewing herbivores and pathogens tested (20 of 26 tests) but not for herbivores of other feeding modes (1 of 8 tests). Most tests (5 of 6) using Ni concentrations below accumulator levels found no defensive effect, and the single test using plants in the accumulator range also found no effect. For Zn, mixed results have been reported for both hyperaccumulator (3 of 6 tests showed defense) and accumulator levels (3 of 4 tests showed defense). These tests have focused exclusively on leaf chewing/scraping herbivores: no herbivores of other feeding modes, or pathogens, have been tested. Both hyperaccumulator and accumulator concentrations of Se generally have shown defensive effects (12 of 14 tests). Most (75%) of these positive results used plants with accumulator Se concentrations. The three tests of Cd showed defensive effects in two cases, one for hyperaccumulator and one for sub-accumulator Cd concentrations. Arsenic has been tested only once, and was found effective against a leaf-chewing herbivore at a concentration much less than the hyperaccumulator level. Defense studies have used a variety of experimental approaches, including choice and no-choice experiments as well as experiments that use artificial diet or growth media. Investigations of hyperaccumulation as a defense against natural enemies have led to two emerging questions. First, what is the minimum concentration of an element sufficient for defense? Evidence suggests that plants other than hyperaccumulators (such as accumulators) may be defended by elements against some natural enemies. Second, do the effects of an element combine with the effects of organic defensive compounds in plants to produce enhanced joint defensive effects? Recent investigation of this “joint effects hypothesis,” using Ni and secondary plant compounds in artificial insect diet, has demonstrated joint effects. Initial answers to both these questions suggest that defensive effects of elements in plants are more widespread than previously believed. These results also suggest an evolutionary pathway by which elemental hyperaccumulation may have evolved from accumulation. In this “defensive enhancement” scenario, defensive benefits of elevated levels of elements may have led to stepwise increases in element concentrations that further magnified these benefits. This series of steps could have led to increased accumulation, and ultimately hyperaccumulation, of elements by plants.