Metal hyperaccumulation in plants: mechanisms of defence against insect herbivores

1. To determine the mechanisms by which metal hyperaccumulation in plants could provide a chemical defence against insect herbivores, the feeding behaviour and performance of the desert locust, Schistocerca gregaria (Forskal), was investigated on plants of Thlaspi caerulescens J. & C. Presl containing different zinc concentrations, as well as on artificial food differing only in Zn content. 2. In choice experiments, locusts preferred T. caerulescens plants containing low foliar Zn concentrations (mean value 0.42 mg g(-1) dry biomass) compared with intermediate (1.50 mg g(-1)) or high (5.77 mg g(-1)) Zn concentrations. In no-choice experiments, there was no difference in the duration of the first meal, suggesting that locusts could not taste Zn directly, but total time spent feeding, amount of foliage eaten, and locust growth rate all decreased as foliar Zn concentration increased. 3. When presented with artificial food containing Zn concentrations of 0.5, 1.5 or 5.5 mg g(-1), locusts fed at a slower rate on intermediate- and high-Zn diets, and their development time from fourth to fifth stadium was proportionately longer. The total amount of food eaten over the fourth stadium was similar for the different treatments, but locust mass gain was inversely related to Zn concentration in the diet. This was reflected in lower nutrient-utilization efficiencies in locusts on a high-Zn diet. 4. In choice experiments with artificial food, locusts showed very similar feeding behaviour to that on plants, consuming more of the low-Zn food. Experiments using food flavoured with coumarin, provided with or without Zn, showed that the locusts' aversion to Zn develops by a post-ingestive feedback mechanism involving associative learning. 5. These results support the notion that metal hyperaccumulation in plants can provide a defence against insect herbivores, and demonstrate that metal concentration per se can account for the deterrent effect of high-Zn foods. Aversion responses were evoked by Zn concentrations in the range 0.5-5 mg g(-1), an order of magnitude lower than those commonly observed in the foliage of T. caerulescens. This suggests that comparatively small elevations in Zn concentration could confer an adaptive advantage on plants by influencing the feeding behaviour of polyphagous insect herbivores, thereby contributing to evolution of the metal-hyperaccumulation trait.