Revisiting the functional strategy of herbaceous metallophytes helps understanding leaf metal accumulation

Abstract

Plant physiological adaptations to metal-rich soils consist either in metal exclusion or in metal (hyper)accumulation in leaves and aboveground tissues. However, the relationship between these adaptations and the functional strategies developed by metallophytes to sustain their development is unknown. Here, given the soil instability often occurring in metalliferous ecosystems, we assumed that many metallophyte species should present ruderal-like syndromes. Additionally, because leaf metal accumulation requires resources and energy, we assumed that metal-accumulating species should be found among fast-growing acquisitive species. We studied functional traits related to the two major plant functional dimensions (size and leaf resource economics) for 107 herbaceous species in eight metalliferous sites (four calamine, three serpentine, and one copper-rich ecosystem) in Europe, Central Africa, and Japan. Zinc (Zn), nickel (Ni), or copper (Cu) accumulation ability was determined for all species. Soil instability was evaluated in one site in the Pyrenees through rockiness characterization and slope steepness calculated from a high-resolution digital elevation model. Results showed that soil-metal availability and slope steepness impacted vegetation development in the Pyrenees. Consistently, plant size was reduced in the most polluted areas, and many species were acquisitive, exhibiting the expected ruderal-like syndromes. This pattern was confirmed along a soil-Cu gradient in Central Africa. At the global scale, plant size reduction was confirmed for calamine and Cu-rich environments, and was more variable in serpentine ones. In all sites, a mix of acquisitive and conservative species was observed. This variability was correlated with leaf metal accumulation, acquisitive species showing high accumulation, and conservative species showing high metal exclusion. Notably, hyperaccumulating species were always found among acquisitive species. These findings offer new perspectives regarding the evolution of metal hyperaccumulation, suggesting that high photosynthetic activity is a prerequisite to handle the cost of metal hyperaccumulation. They also complete the main hypotheses explaining the ecological advantage of hyperaccumulation, that is, the defense against herbivores and allelopathic interference with neighbors through litter decomposition. Acquisitive species are indeed preferentially chosen by herbivores and produce a fast-decomposing litter. Further studies should test the generality of these results for other accumulated elements, and for woody Ni hyperaccumulators in tropical serpentine areas.