Selenium hyperaccumulators facilitate selenium-tolerant neighbors via phytoenrichment and reduced herbivory

Abstract

Background: Soil surrounding selenium (Se) hyperaccumulator plants was shown earlier to be enriched in Se, impairing the growth of Se-sensitive plant species. Because Se levels in neighbors of hyperaccumulators were higher and Se has been shown to protect plants from herbivory, we investigate here the potential facilitating effect of Se hyperaccumulators on Se-tolerant neighboring species in the field.

Results: We measured growth and herbivory of Artemisia ludoviciana and Symphyotrichum ericoides as a function of their Se concentration and proximity to hyperaccumulators Astragalus bisulcatus and Stanleya pinnata. When growing next to hyperaccumulators, A. ludoviciana and S. ericoides contained 10- to 20-fold higher Se levels (800-2,000 mg kg(-1) DW) than when growing next to nonaccumulators. The roots of both species were predominantly (70%-90%) directed toward hyperaccumulator neighbors, not toward other neighbors. Moreover, neighbors of hyperaccumulators were 2-fold bigger, showed 2-fold less herbivory damage, and harbored 3- to 4-fold fewer arthropods. When used in laboratory choice and nonchoice grasshopper herbivory experiments, Se-rich neighbors of hyperaccumulators experienced less herbivory and caused higher grasshopper Se accumulation (10-fold) and mortality (4-fold).

Conclusions: Enhanced soil Se levels around hyperaccumulators can facilitate growth of Se-tolerant plant species through reduced herbivory and enhanced growth. This study is the first to show facilitation via enrichment with a nonessential element. It is interesting that Se enrichment of hyperaccumulator neighbors may affect competition in two ways, by reducing growth of Se-sensitive neighbors while facilitating Se-tolerant neighbors. Via these competitive and facilitating effects, Se hyperaccumulators may affect plant community composition and, consequently, higher trophic levels.