The mid-Pridoli teratology event correlates with faunal turnover33 and a positive δ13C excursion34 (Fig. 5). Early Palaeozoic bioevents were generally accompanied by large, positive δ13C carb excursions. Consensus is converging that such signatures may reflect the burial and sequestration of isotopically light carbon on the deep seafloor during developing OAEs35. It is also well established that transitions to anoxic conditions in modern marine environments increase markedly the solubility of some metals in seawater36. Most significantly, suboxic conditions lead to the reductive dissolution of Fe–Mn oxyhydroxides, increasing the concentration of Fe and Mn in modern seawater by orders of magnitude. The concentration of some trace elements such as As, Mo and rare earth elements are directly controlled by absorptive scavenging and co-deposition with these oxyhydroxides; and as a consequence of reductive dissolution of oxyhydroxides, increase significantly in concentration in the seawater37,38,39. Moreover, transitions from oxic to anoxic oceanic conditions can trigger massive shifts in the cycling of Fe–Mn oxyhydroxides sequestered in sub-seafloor sediments, thereby triggering a benthic flux of Fe, Mn and associated trace elements from the sediments into the anoxic seawater37,38,40. Other elements, such as Ba, are governed by linked processes such as the reduction of sulfate in anoxic sediments41. We posit that the observed metal enrichments and teratology during this Pridoli event reflects the encroachment of metal-enriched, oxygen-depleted oceanic waters into the oxic environments of the continental shelves. As this redox front moved into shallow water, the toxic mix of elements was introduced into the shelf ecosystems teeming with Silurian life. Consequently, the metals were re-oxidized and precipitated, each at their own pace (Supplementary Dataset 1), at the redox interface between the anoxic water mass and local oxic surface waters. This scenario accounts for the accumulation of redox-sensitive metals in both the sediments and fossils and explains the teratology of organisms during the Pridoli event. This interpretation is supported by similar enrichments of redox-sensitive metals through the early Wenlock Ireviken event12, by the enrichment of rare earth elements in widespread phosphorites across Laurentia42, and by the concurrence of ironstones with Silurian C-isotope excursions in the Appalachian Basin (USA). The US sections display consistent patterns of red, green and black marine sedimentary rocks, indicative of increasingly anoxic conditions10. In this model, the harmful effects of spreading dead zones43, decreasing oxygen and increasing metal concentrations are intricately entangled. For instance, a study44 of the seasonally anoxic Chesapeake Bay links the sudden occurrence of malformed foraminifer Ammonia to the onset of anoxic conditions in the 1970s. However, it is also known that these seasonal anoxic conditions triggered the prompt release of redox-sensitive metals from the sediments into the water column40. In our Silurian data, metal-enriched malformed assemblages occur at the onset of the carbon isotope excursions, while hypoxia was starting to spread (and before it peaks later, indicated by the deposition of black shales10). This suggests that a direct toxic effect of metal enrichment contributed to the most plausible mechanism for the deformities in the organisms. Other environmental stressors that are known to cause malformation in the modern include changes in light intensity, ultraviolet radiation, predation, salinity and pH, and could have coincided with spreading anoxic waters, but there is no empirical evidence for such changes in the event interval.

Figure 5: Distribution of potential OAEs in the uppermost Ordovician and Silurian. The position of the suggested OAEs is based on δ13C stratigraphy34. Key victims of the extinction events and the events with increased occurrences of teratology are highlighted13. Metal toxicity is observed in the Pridoli (this study) and implied during the Ireviken event, where metal enrichments in carbonates and phosphates in SE Sweden indicate anoxia12. For a full list of affected fauna see Kaljo et al.33 and Calner6. Ord., Ordovician; Dev., Devonian. Full size image

The metal composition of marine sedimentary rocks is a fundamental parameter used to interpret the chemical evolution of the Earth’s atmosphere and hydrosphere. Yet, generally, uncertainty remains regarding the primary metal abundances in seawater, pathways of metal accumulation and post-depositional modification of metal abundances in sedimentary rocks. As demonstrated in modern marine environments, our results suggest that metal-induced teratology of fossil plankton may serve as an independent proxy for monitoring changes in the metal concentrations of the shallow palaeo-ocean. This new proxy enables us here to reduce these uncertainties and supports the interpretation that the sedimentary chemistry reflects changing oceanic metal compositions during OAEs. As such, this proxy has the potential to help unravel the complexities inherent to sedimentary geochemistry, and may be a tool to evaluate other instances of marine metal variation through the geological record.

The co-occurrence between mid-Pridoli teratology and the onset of extinction suggests that metal contamination may have played a direct role in the biological crisis at large. More generally, the recurring temporal match between Ordovician–Silurian teratology events and extinction events13 raises the prospect that toxic metal contamination may be a previously unrecognized contributing agent to many, if not all, of these bioevents (Fig. 5). In sections where such data exist, teratological phytoplankton precede or co-occur with the earliest phases of these major extinction events. Taken at face value, for example, Hirnantian acritarch malformation in the Lousy Cove Member (member 6) of the Ellis Bay Formation coincides with the onset of the ‘phytoplankton crisis’ on Anticosti Island (Canada) but precedes the major macrofauna extinctions in the overlying Laframboise Member (member 7) (refs 14, 45). On Gotland (Sweden), increased acritarch malformation occurs around a series of marker beds46, identifying an interval that starts below the strongest extinctions of conodonts during the early Ireviken event4. Although the patterns and exact relative timing of teratology and extinction require confirmation, the available data suggest that malformed palynomorphs could be the proverbial ‘canaries in the coal mines’, that is, the first indicators of Palaeozoic extinctions.

Metal toxicity, and its fossilized in vivo expressions, could provide the ‘missing link’ between extinction of faunas on the shelf, and widespread ocean anoxia. As part of a series of complex systemic interactions accompanying these shifts in ocean conditions, the redox cycling of metals may identify the early phase of the kill mechanisms that culminated in these catastrophic events. Although OAEs typically entail rapid climatic change, our data suggest that the proposed mechanisms of these early Palaeozoic mass extinctions were previously too simply linked to global cooling, invoking thermal stress and habitat reduction. Ultimately, metal-induced teratology might become a new forensic tool to identify original oceanic geochemical signatures and may help unravel the biologic and geochemical systematics that define these extraordinary periods of Earth history.