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  • Effect of Cadmium Accumulation on the Performance of Plants and of Herbivores That Cope Differently With Organic Defenses
    Publication . Godinho, Diogo Prino; Serrano, Helena Cristina; Da Silva, Anabela Bernardes; Branquinho, Cristina; Magalhães, Sara
    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 (Solanum lycopersicum), a model plant that accumulates cadmium, and two spider-mite species, Tetranychus urticae and Tetranychus evansi 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 T. urticae or T. evansi. 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.
  • Concurrent herbivory and metal accumulation: The outcome for plants and herbivores
    Publication . Godinho, Diogo; Serrano, Helena Cristina; Magalhães, sara; Branquinho, Cristina
    The effects of metals on plants and herbivores, as well as the interaction among the latter, are well documented. However, the effects of simultaneous herbivory and metal accumulation remain poorly studied. Here, we shed light on this topic by infesting cadmium-accumulating tomato plants (Solanum lycopersicum), either exposed to cadmium or not, with herbivorous spider mites, Tetranychus urticae or T. evansi during 14 days. Whereas on plants without cadmium T. evansi had higher growth rate than T. urticae, on plants with cadmium both mite species had similar growth rates, which were lower than on plants without metal. Plants were affected by both cadmium toxicity and by herbivory, as shown by leaf reflectance, but not on the same wavelengths. Moreover, changes in leaf reflectance on the wavelength affected by herbivores were similar on plants with and without cadmium, and vice versa. Long-term effects of cadmium and herbivory did not affect H2O2 concentrations in the plant. Finally, plants infested with spider mites did not accumulate more cadmium, suggesting that metal accumulation is not induced by herbivory. We thus conclude that cadmium accumulation affects two congeneric herbivore species differently and that the effects of herbivory and cadmium toxicity on plants may be disentangled, via leaf reflectance, even during simultaneous exposure.
  • Intraspecific variability in herbivore response to elemental defences is caused by the metal itself
    Publication . Godinho, Diogo; Branquinho, Cristina; Magalhães, sara
    Some plants are able to accumulate on their leaves metals taken from the soil, using this as a defence against herbivorous arthropods. However, herbivore response to metal accumulation in plants is known to be variable. While some species and taxonomic groups are less affected than others, hormetic effects have also been observed in spider mites, herbivorous crop pests. Still, knowledge on the range and causes of intraspecific variation in the response of herbivores to metal accumulation is lacking. Here, using two species of spider mites, Tetranychus urticae and Tetranychus evansi, we tested the variation in 17 populations in response to cadmium-accumulating tomato plants and the drivers of such variation. We observed a nonlinear, hormetic response of mites to plants with cadmium in some, but not all, populations. The same pattern was recaptured in artificial diets with different concentrations of cadmium but not in artificial diets with sugars, which change in the plant in response to cadmium. This indicates that herbivores on metal-accumulating plants respond to metals, not to the variations in leaf carbohydrates. Therefore, metals exert different effects on herbivores according to the amount accumulated, but independently of other studied plant traits. This knowledge is key to the understanding of the mechanisms underlying herbivore responses to metal-based plant defences and to pesticides containing heavy metals. Additionally, our findings draw attention to the need of considering intraspecific variation and nonlinearities when studying the effects of metals and other contaminants on herbivorous arthropods.