From bioaccumulation to biodecumulation: Nickel movement from Odontarrhena lesbiaca (Brassicaceae) individuals into consumers

Abstract

Hyperaccumulation describes plants' ability to take up high amounts of soil metals such as Ni and allocate them to aboveground tissues. Little is known, however, about the rate at which Ni is allocated to different plant parts, or about the consumers related to these parts, including their pollinator mutualists. In this study, we examine the interface between the serpentine endemic Ni-hyperaccumulator Odontarrhena lesbiaca and its consumers of different plant parts: leaves (consumers), floral parts (consumers and primitive pollinators), and floral rewards (true pollinators). The study was conducted at two serpentine areas on Lesvos, Greece. Over 13 rounds of sampling during the flowering period of O. lesbiaca in both areas we collected plant stems with flowers, consumers of different plant parts, and flower visitors. Collected animals were mainly insects and some spiders. Chemical analyses showed negligible Ni-concentration differences between the two areas. Among all plant parts, the lowest Ni concentration was found in pollen and the highest in leaves. Regarding animal dietary habits, folivores accumulated the highest Ni concentrations, therefore characterized as "high-Ni insects", while floral-reward consumers, both primary (bees) and secondary (Eristalis tenax, Pygopleurus spp., and wasps), bore low Ni loads. Ni-body load of predators that fed on animals that were passing by was also low. Among floral-reward consumers, short-range fliers (bees of the genera Andrena and Lasioglossum) accumulated higher Ni loads than long-range fliers (Apis mellifera, Bombus terrestris, Eristalis tenax). Solitary Andrena bees accumulated higher Ni concentration than eusocial honeybees (Apis mellifera) and bumblebees (Bombus terrestris); a group of Lasioglossum specimens encompassing both solitary and eusocial bees lay in between. Our results show that diet, foraging distance, and sociality are important factors for Ni transferred into consumers and mutualists, mostly insects that are directly associated with different plant parts of O. lesbiaca.

Keywords: Arthropod; Diet habit; Foraging distance; Nickel hyperaccumulation; Pollen; Ultramafic soils.