Abstract
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.
Highlights
IntroductionThe mechanisms that allow them to survive these adversities imply physiological and structural transformations that can be costly to the plants, affecting negatively their growth and fitness (Boyer, 1982; Wang et al, 2003)
Plants are exposed to an array of abiotic and biotic stresses
Significant differences were detected for the SC index (R1100/R810), (Table 1) on plants exposed to 2 mM or 10 mM of Cd (Table 2), suggesting structural changes in the leaf cells
Summary
The mechanisms that allow them to survive these adversities imply physiological and structural transformations that can be costly to the plants, affecting negatively their growth and fitness (Boyer, 1982; Wang et al, 2003) One such stress is high bioavailable metal concentrations in soil, either naturally (geochemical anomalies) or due to anthropogenic activities. The stress caused by metal toxicity may lead to disturbances in the carbon and nitrogen metabolism, affecting the nutritional status of various plant parts (Larbi et al, 2002; Chaffei et al, 2004; Wahid et al, 2007), and potentially changing the accumulation of soluble sugars, either leading to increased (Devi et al, 2007; Rosa et al, 2009; Mishra et al, 2014) or decreased (Scheirs et al, 2006; Shackira and Puthur, 2017) sugar concentrations in the shoots. These physiological changes in the plant may affect the performance of the herbivores feeding on those plants (White, 1984; Scheirs et al, 2006)
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