Selenium protects the hyperaccumulator Stanleya pinnata against black-tailed prairie dog herbivory in native seleniferous habitats.

Elemental hyperaccumulation in plants is hypothesized to represent a plant defense mechanism. The objective of this study was to determine whether selenium (Se) hyperaccumulation offers plants long-term protection from the black-tailed prairie dog (Cynomys ludovicianus). Prairie dogs are a keystone species. The hyperaccumulator Stanleya pinnata (prince's plume) co-occurs with prairie dogs in seleniferous areas in the western United States. Stanleya pinnata plants pretreated with high or low Se concentrations were planted on two prairie dog towns with different levels of herbivory pressure, and herbivory of these plants was monitored over 2 years. Throughout this study, plants with elevated Se levels suffered less herbivory and survived better than plants with low leaf Se concentrations. This study indicates that the Se in hyperaccumulator S. pinnata protects the plant in its natural habitat from herbivory by the black-tailed prairie dog. The results from this study support the hypothesis that herbivory by prairie dogs or similar small mammals has been a contributing selection pressure for the evolution of plant Se hyperaccumulation in North America. This study is the first to test the ecological significance of hyperaccumulation over a long period in a hyperaccumulator's natural habitat.

The role of selenium in protecting plants against prairie dog herbivory: implications for the evolution of selenium hyperaccumulation.

Some plants can hyperaccumulate the element selenium (Se) up to 10,000 mg Se kg(-1) dry weight. Hyperaccumulation has been hypothesized to defend against herbivory. In laboratory studies high Se levels protect plants from invertebrate herbivores and pathogens. However, field studies and mammalian herbivore studies that link Se accumulation to herbivory protection are lacking. In this study a combination of field surveys and manipulative field studies were carried out to determine whether plant Se accumulation in the field deters herbivory by black-tailed prairie dogs (Cynomys ludovicianus). The Se hyperaccumulator Astragalus bisulcatus (two-grooved milkvetch) occurs naturally on seleniferous soils in the Western USA, often on prairie dog colonies. Field surveys have shown that this Se hyperaccumulator is relatively abundant on some prairie dog colonies and suffers less herbivory than other forb species. This protection was likely owing to Se accumulation, as judged from subsequent manipulative field experiments. When given a choice between pairs of plants of the Se hyperaccumulator Stanleya pinnata (prince's plume) that were pretreated with or without Se, prairie dogs preferred to feed on the plants with low Se; the same results were obtained for the non-hyperaccumulator Brassica juncea (Indian mustard). Plants containing as little as 38 mg Se kg(-1) DW were protected from herbivory. Taken together these results shed light on the functional significance of Se hyperaccumulation and the possible selection pressures driving its evolution. They also have implications for the use of plants in Se phytoremediation, or as Se-fortified crops.

Selenium hyperaccumulation reduces plant arthropod loads in the field.

The elemental defense hypothesis proposes that some plants hyperaccumulate toxic elements as a defense mechanism. In this study the effectiveness of selenium (Se) as an arthropod deterrent was investigated under field conditions. Arthropod loads were measured over two growing seasons in Se hyperaccumulator habitats in Colorado, USA, comparing Se hyperaccumulator species (Astragalus bisulcatus and Stanleya pinnata) with nonhyperaccumulators (Camelina microcarpa, Astragalus americanus, Descurainia pinnata, Medicago sativa, and Helianthus pumilus). The Se hyperaccumulating plant species, which contained 1000-14 000 microg Se g(-1) DW, harbored significantly fewer arthropods (c. twofold) and fewer arthropod species (c. 1.5-fold) compared with nonhyperaccumulator species that contained < 30 microg Se g(-1) DW. Arthropods collected on Se-hyperaccumulating plants contained three- to 10-fold higher Se concentrations than those found on nonhyperaccumulating species, but > 10-fold lower Se concentrations than their hyperaccumulator hosts. Several arthropod species contained > 100 microg Se g(-1) DW, indicating Se tolerance and perhaps feeding specialization. These results support the elemental defense hypothesis and suggest that invertebrate herbivory may have contributed to the evolution of Se hyperaccumulation.