Mercury accumulation and mutagenesis in ferns surviving mass-extinction

Mutated pteridophyte spores occur abundantly in conjunction with the end-Triassic mass-extinction (ETME), ~201.6 million years ago, one of the ‘Big Five’ mass-extinction events of the past 500 million years. Based on high concentrations of sedimentary mercury (Hg) in beds that contain abundant mutated fern spore fossils, it has been hypothesized that volcanogenic Hg-emission from large-scale volcanism in the Central Atlantic Magmatic Province exerted stress on standing and pioneering vegetation, causing malfunctions in meiosis and the production of malformed pteridophyte spores. Here, we provide the first clear in vivo evidence for anomalously high Hg among the plants that survived and proliferated through the ETME using synchrotron X-ray fluorescence (XRF). Our analysis reveals highly enriched values of Hg within the fronds of the earliest Jurassic fern Phlebopteris angustiloba from southern Germany. Intriguingly, P. angustiloba, a member of the Matoniaceae, is recognized as the parent plant which produced malformed spores within the Deltoidospora-Concavisporites complex that are common in the same beds that contain the fossil fern leaves. Using XRF and X-ray absorption near edge structure (XANES) analyses, we made comparisons between the fossil fern leaves and those of extant ferns growing in high-mercury environments in Slovenia, Slovakia, and the Czech Republic. These comparisons suggest that ferns can tolerate elevated Hg-levels and bind it in their placentas with sulfurous compounds. Our combined analysis of extant and extinct ferns suggests that these traits may have evolved in response to past environments with high concentrations of toxic metals—like those caused by magmatically-triggered mass extinctions—during which metal-tolerant strategies would have greatly enhanced survivorship.