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Front. Plant Sci. | doi: 10.3389/fpls.2018.01723

Effect of cadmium accumulation on the performance of plants and of herbivores that cope differently with organic defences

  • 1Centro de Ecologia, Evolução e Alterações Ambientais, Faculdade de Ciências, Universidade de Lisboa, Portugal
  • 2Instituto de Biossistemas e Ciências Integrativas (BioISI), Portugal

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 T. 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, on our system. This character 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.

Keywords: Metal accumulating plants, plant defence, Tomato, spider mites, elemental defence hypothesis

Received: 08 Aug 2018; Accepted: 06 Nov 2018.

Edited by:

Merijn Kant, University of Amsterdam, Netherlands

Reviewed by:

Robert S. Boyd, Auburn University, United States
Caroline Müller, Bielefeld University, Germany  

Copyright: © 2018 Godinho, Serrano, Silva, Branquinho and Magalhães. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Dr. Sara Magalhães, Centro de Ecologia, Evolução e Alterações Ambientais, Faculdade de Ciências, Universidade de Lisboa, Lisbon, Portugal,