Mercury concentrations in terrestrial fossil vertebrates from the Bauru Group (Upper Cretaceous), Brazil and implications for vertebrate paleontology
Introduction
Recent studies have reported the presence of mercury (Hg) in sedimentary rocks as evidence of mass mortality events (MMEs) in different geological periods (e.g. Sial et al., 2013; Font et al., 2016; Ernst and Youbi, 2017; Gong et al., 2017; Jones et al., 2017; Percival et al., 2017). Mercury is a globally distributed toxic metal that exists as metallic (Hg0), inorganic (Hg2+), and organic (e.g. MeHg) forms (Fitzgerald et al., 1998; Morel et al., 1998; Liu et al., 2012). Mercury mobility and bioaccumulation are directly related to its chemical speciation, which occurs in cyclic processes of oxidation and reduction in the environment (Fitzgerald et al., 1998).
The elemental mercury (Hg0), produced by geological processes, is primarily volatilized to the atmosphere by geological activities (e.g. volcanism), and secondarily by volatilization from water bodies and from soil (Morel et al., 1998; Selin, 2009), corresponding to approximately 95% of the total mercury available in the atmosphere (Morel et al., 1998), which can be oxidized into Hg2+, an inorganic species that is precipitated and deposited in terrestrial and aquatic systems (Amyot et al., 1997; Fitzgerald et al., 1998; Morel et al., 1998; Selin, 2009). In aquatic systems and sediments (and soil), part of Hg2+ can be methylated by sulfate-reducing microorganisms in the form of bioavailable methylmercury (MeHg) (Compeau and Bartha, 1985; Ullrich et al., 2001), an organic compound that can be bioaccumulated in organisms (WHO, 1992; Clarkson, 1997; Morel et al., 1998; Watras et al., 1998).
Recently, Percival et al. (2017) suggested a close association between the end-Triassic (∼201.5 Ma) mass extinction event and the presence of elevated Hg concentrations in sediments related to large-scale volcanic activities that took place at that time. They examined the concentration of Hg and total organic carbon (TOC) in end-Triassic sediments of six geographically distinct records of basaltic units of the Central Atlantic Magmatic Province (CAMP). The results suggest that Hg peaks in end-Triassic sedimentary rocks are associated with the volatilization of Hg0 released by a great volcanic episode, which led to the global environmental disturbance during a long-time interval, with harmful effects on the biota and its recovery capacity (Percival et al., 2017).
Although other studies have also suggested the relationship between the increase of Hg concentration in sediments and mass extinctions events (e.g. Sial et al., 2013; Font et al., 2016; Thibodeau et al., 2016; Gong et al., 2017; Grasby et al., 2017), none, as far as we know, have yet performed measurements of Hg in fossils vertebrates, which could provide additional and more effective evidence of the influence of Hg in past terrestrial ecosystems.
Previous studies reported the presence of Hg in mineralized tissues (hydroxyapatite/calcite/aragonite) in archaeological/fossil remains. Outridge et al. (2002), for example, compared THg concentrations in modern and preindustrial teeth of belugas from Canada. Although in this study the THg may include both the hydroxyapatite and the collagen, they found that the Hg concentrations increased at least four times in modern teeth. Xu et al. (2011) also noted an increase in THg concentrations in a 700-year record of avian eggshells from China. Rasmussen et al. (2013) analyzed the THg in medieval skeletons, using bone tissues and surrounding sediments, to investigate the cause of death of those individuals and concluded that the Hg, besides accumulating in the organism, has the capacity to remain stored for a long time in bones and other biomineralized materials. Murray et al. (2015) studied the variations in Holocene THg concentration in fish bone from Alaska and suggested that the increase in THg concentrations was the result of coastal flooding that could have led to increased methylation of Hg in the studied area. Meyer et al. (2017) reported the presence of THg anomalies in shell of marine mollusks and suggested they could be related to the volcanic activities that formed the Deccan Traps.
In this work, we analyze the presence of Hg in Upper Cretaceous crocodylomorphs from Brazil and the natural uptake of mercury in these organisms as sourced from their paleoenvironment. The fossils used in this study include bone, tooth, osteoderm, and eggshells of various Baurusuchidae specimens, a relatively common crocodylomorph found in Bauru Group deposits.
Although not conclusive, the realization that fossil vertebrate materials (e. g. tooth, bones, and eggshells) may contain Hg that has been incorporated by the organism from the environment during its life furnishes an additional information on the study of mass mortality events caused by volcanic activities. In this case, a connection among coeval large igneous provinces, sedimentary deposits, and associated fossils can be made by the identification of synchronic positive Hg anomalies in them. Moreover, the presence of Hg in fossil vertebrates could provide additional support for studies regarding ontogenetic development and, in some specific cases (e. g. egg-laying vertebrates with osteoderms, such as crocodylomorphs) the identification of female individuals.
Section snippets
Geological setting
The samples were collected from rocks of the Adamantina Formation (Bauru Group), Upper Cretaceous, in the cities of Fernandópolis and Jales, São Paulo State, Brazil (Fig. 1). The Bauru Group corresponds to a continental depositional system formed by the accumulation of a ∼300 m thick sedimentary sequence that overlies a large basaltic province (Serra Geral Formation) in the center of the South American Plate, which mainly developed during the Upper Cretaceous (e.g., Fulfaro and Perinotto, 1996;
Results
The results show higher values for THg concentration in biomineralized tissues in comparison to their surrounding sediments (Table 1), with a range of values from approximately 5.0 to 77.0 (ng.g−1) for the fossil samples and a range of 2.6–3.4 (ng.g−1) for the surrounding sediment/host rock (sandstones). The standard deviation, considering the triplicates analyzed is not higher than 0.7 ng.g−1, except for the eggshell and basalt samples, where it can reach up 5.9 ng.g−1. The analysis was not
Discussion
Recent studies have related volcanism to mass extinctions events by determining the THg in sedimentary rocks associated with large igneous provinces (LIPs; Thibodeau et al., 2016; Ernst and Youbi, 2017; Jones et al., 2017; Percival et al., 2017). One of the reasons for this type of analysis not being carried out in fossils so far is concerned to the absence of fossil remains in large igneous provinces (Bergquist, 2017). To date, only Meyer et al. (2017) evaluated the concentration of THg in
Conclusions
The presence of Hg in fossil Crocodyliformes (Baurusuchidae) from the Adamantina Formation seems to be linked to a natural presence of this element in their Cretaceous paleoenvironment furnished by the weathering of the underlaying basaltic rocks of the Serra Geral Formation. This is the first and earliest record of natural Hg contamination in vertebrate fossils, where the presence of Hg in different biomineralized tissues (teeth, bones, dermal scutes, and eggs) is interpreted as a record of
Acknowledgements
We are in debt to Lourdes Morais (IBRAM), Geraldo Martins (CAESB), João Victor (TQB), and Jurandir Souza (IQ, UnB) for their help during the preparation of the material and analytical procedures. Douglas Galante (LNLS) is thanked for his help with the RAMAN analysis and Luiz Mancini (IG/UnB) is thanked for the S isotopic analysis. We are also in debt to two anonymous reviewers whose comments improved an earlier draft of this manuscript. RMS also thanks the Conselho Nacional de Desenvolvimento
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