Metal transfer in a tri-trophic terrestrial system of naturally metal enriched soils

Abstract

Potentially toxic metal(loid)s (PTMs) are elements that are toxic to plants and animals at elevated concentrations. In addition to anthropogenically altered environments, PTMs occur naturally in soil derived from ultramafic rocks, often referred to as ultramafic soil. Although some ultramafic ecosystems are well studied, those within South Africa still demand attention, including the ultramafic komatiite outcrops of the Vredefort Dome. There are few reports of ultramafic soil from the dome, and even less on the trophic transfer of PTMs. Therefore, the aim of this study was to assess the transfer of PTMs to three trophic levels within a naturally PTM rich terrestrial ecosystem model, using wild and crop plants as producers. First, a review was conducted on the topic, identifying knowledge gaps and necessary focal points for research. The search engine used was ScienceDirect®. Any article investigating PTM accumulation or trophic transfer within terrestrial ecosystems with a minimum of one living organism was included. Results indicated that most literature (62%) originated from developed regions (USA and Europe), while research from Africa and South America only contributed 2.6% and 6.8%, respectively. Furthermore, only 3.2% of the studies focused on PTMs from natural sources. Therefore, the present study investigated the transfer of PTMs in a tri-trophic food chain using ultramafic (komatiite) and control soil as substrates. The wild plant Berkheya radula and the crop plant Brassica oleracea var. acephala (kale) were selected as primary producers, while the house cricket Acheta domesticus and the African twig mantis Popa spurca were the primary and secondary consumers, respectively. The concentrations of PTMs in each trophic level were evaluated, as well as the bioaccumulation factors between each link. The effect of PTMs on the development of the African twig mantis was evaluated through the duration of each instar and entire life cycle. Additionally, the effect of PTMs on house cricket feeding behaviour was assessed through olfaction and gustation tests. Although the concentrations of PTMs in the komatiite soil were twice as high as that of the control, the trophic levels did not reflect the PTM contents within the soil. For example, both control and komatiite Berkheya bioaccumulated Ba and Sr, while excluding As, Co, Cu, Mo, Se, Pb, and V. Similarly, both control and komatiite kale bioaccumulated Sr, while excluding As, Co, Cu, Mn, Pb, Se, and V. All above mentioned PTMs were higher in komatiite than control soil. Furthermore, crickets in the Berkheya trial bioaccumulated the same PTMs regardless of food treatments (i.e. komatiite or control Berkheya), and control crickets in the kale trial from komatiite excluded Mo and Rb, which were bioaccumulated by control kale plants. Still, the PTMs that were bioaccumulated by crickets fed on komatiite kale were excluded from these plants. Lastly, mantids in the Berkheya trial bioaccumulated Cu, Mo, Ni, Sr, and V regardless of the food treatment (i.e. crickets fed on komatiite or control Berkheya), and mantids in the kale trial did the same with As, Cu, and Se. Although some differences were observed regarding mantid developmental duration in both trials, the non-significant differences of PTM concentrations suggested that other factors besides PTM levels contributed to the results. Olfaction and gustation tests revealed that PTM levels within plant leaves were not discriminated by house crickets overall, even though female house crickets showed preference towards Berkheya leaves grown in PTM soils during the olfaction test. Ultimately, the concentrations of PTMs in wild plant and crop plant ecosystem models did not reflect soil total PTM concentrations. Thus, PTM bioaccumulation and subsequently availability of PTMs to the next trophic level seems to be a function of the plant species rather than of soil content. The insights gained by this study advanced our understanding of naturally PTM rich ecosystems, especially in the Vredefort Dome, and how organisms within these ecosystems adapted to these conditions. Furthermore, this study adds to the research record from Africa, which is currently underrepresented when compared to the global context.