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Animal Evolution, Bioturbation, and the Sulfate Concentration of the Oceans

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Animal Evolution, Bioturbation, and the Sulfate Concentration of the Oceans Animal evolution, bioturbation, and the sulfate SEE COMMENTARY concentration of the oceans Donald E. Canfielda,1 and James Farquhara,b aNordic Center for Earth Evolution, and Institute of Biology, University of Southern Denmark, Campusvej 55, 5230 Odense M, Denmark; and bEarth System Science Interdisciplinary Center and Department of Geology, University of Maryland, College Park, MD 20742 Contributed by Donald E. Canfield, March 3, 2009 (sent for review December 17, 2008) As recognized already by Charles Darwin, animals are geobiologi- 60 cal agents. Darwin observed that worms aerate and mix soils on a 40 massive scale, aiding in the decomposition of soil organic matter. 20 δ34S 0 A similar statement can be made about marine benthic animals. -20 This mixing, also known as bioturbation, not only aides in the -40 decomposition of sedimentary organic material, but as contended 1.5 here, it has also significantly influenced the chemistry of seawater. In particular, it is proposed that sediment mixing by bioturbating f-ratio 1.0 organisms resulted in a severalfold increase in seawater sulfate 0.5 concentration. For this reason, the evolution of bioturbation is linked to the significant deposition of sulfate evaporate minerals, 0 which is largely a phenomena of the Phanerozoic, the last 542 Sulfate 10 million years and the time over which animals rose to prominence. (mM) 1.0 Phanerozoic ͉ evaporite ͉ gypsum ͉ sulfate reduction 0.1 EVOLUTION ith a current concentration of 28 mM, sulfate is the second 0 0.5 1.0 1.5 2.0 2.5 3.0 3.5 4.0 Time (Ga) Wmost abundant anion in seawater. Sulfate enters the ocean mostly from river runoff, with minor contributions from volca- Fig. 1. Graph showing key aspects of the history of the sulfur cycle. (Top) nism (1). It leaves the ocean as either pyrite (FeS2) buried in Isotopic composition of sedimentary sulfides (diamonds) and sulfate (indi- sediments, formed as a product of microbial sulfate reduction, or cated by the 2 red parallel lines) through time. A complete list of data can be as sulfate minerals, mostly gypsum (CaSO ⅐5H O), in evaporite found in the Dataset S1.(Middle) The proportion of total sulfur buried as 4 2 pyrite through time. This is calculated using Eq. 1, using data from the isotope deposits (2). Gypsum precipitates before halite (NaCl) and record. Through the Phanerozoic, the data has been binned from individual GEOLOGY becomes an important evaporite component when the ion Periods, and in the Precambrian, the data were binned in the time intervals: 2ϩ 2- product (IPCaSO4) between Ca and SO4 in unevaporated 542–580 Ma, 580–636 Ma, 636–660 Ma, 660–700 Ma, 750–805 Ma, 805 to 2 2. seawater exceeds 23 mM (3); presently IPCaSO4 is 280 mM The 1000 Ma, and into 300 Ma bins hereafter. Note that between 636 and 700 Ma concentration of Ca2ϩ has varied between 10 and 40 mM over the (between the Sturtian and Marinoan glaciations) the f ratios are off scale (2.9 last 550 million years (4), and if this range applies through Earth and 9.3 in the 2 time bins in this interval) for reasons that are not well 2 2- understood (1). (Bottom) A diagram representing our best estimate for the history, IPCaSO4 would exceed 23 mM with relatively low SO4 levels of 0.5 to 2 mM. If sulfate concentrations fall below this history of seawater sulfate concentrations. See text for details. The vertical Ͻ 2 dotted line at 2.4 Ga represents the ‘‘Great Oxidation Event’’ (15) and the level or if IPCaSO4 becomes 23 mM , the chances for gypsum initial rise in the concentration of atmospheric oxygen (see text for details). supersaturation during evaporation of seawater is reduced. The The line at 0.542 Ga represents the Cambrian–Precambrian boundary. total amount of gypsum deposition from any given parcel of seawater is also limited by sulfate concentration. Previous studies have documented little evidence for gypsum We have used this approach to illustrate to a first order (Fig. 1), 34 deposition before the Mesoproterozoic (1.6 to 1.0 billion years the long term history of gypsum deposition, assuming that ␦ Sin ago) suggesting reduced seawater sulfate concentrations before has been a constant 5 per mil, the most likely value for the recent this time (5). This analysis is predicated on the assumption that Phanerozoic (7). We point out that this value may have varied observations of gypsum abundance faithfully represent the orig- through time (1, 8), but note that within the range of reasonable inal magnitude of gypsum deposition. However, it is known that values (Ϸ4toϷ12 ‰), our conclusions are not changed. gypsum is easily dissolved during weathering (6), and alternative The record of fsulfide (Fig. 1) straddles a value of 1 through all approaches have been developed to evaluate the history of of the Precambrian, implying that gypsum deposition was not a gypsum deposition. One of these derives the history of gypsum major sulfur removal pathway from the oceans until the Pha- deposition from the isotope record of sulfate and sulfide (Fig. 1) nerozoic (last 542 million years) (see also ref 1). This, in turn, (1), with the fraction of the total sulfur leaving the oceans as would imply that sulfate concentrations remained too low to pyrite given by the equation: promote substantial gypsum deposition throughout most of the Precambrian, consistent with independent evidence for the ͓␦34S Ϫ ␦34S ͔ ϭ in sulfate fsulfide ͓␦34 Ϫ ␦34 ͔ [1] Ssulfide Ssulfate Author contributions: D.E.C. designed research; D.E.C. and J.F. performed research; D.E.C. 34 In this equation, ␦ Sx represents either the isotopic composition and J.F. analyzed data; and D.E.C. and J.F. wrote the paper. of sulfur input to the oceans (in), or output from the oceans as The authors declare no conflict of interest. sulfate minerals (sulfate) or sulfide minerals (sulfide), and fsulfide See Commentary on page 8081. is the fraction of the total sulfur removed from the oceans as 1To whom correspondence should be addressed. E-mail: [email protected]. sulfide. The sulfur not deposited as sulfide precipitates as This article contains supporting information online at www.pnas.org/cgi/content/full/ gypsum, so fsulfide Ͻ 1 provides evidence for gypsum deposition. 0902037106/DCSupplemental. www.pnas.org͞cgi͞doi͞10.1073͞pnas.0902037106 PNAS ͉ May 19, 2009 ͉ vol. 106 ͉ no. 20 ͉ 8123–8127 Downloaded by guest on September 29, 2021 history of seawater sulfate concentrations. The keys points in this bines Fe sulfides formed deeper in the sediment with oxidized history include evidence for very low sulfate concentrations of species near the surface, promoting the oxidation of the sulfide. 200 ␮M or less before 2.4 billion years ago (Ga) (9). After this, The global value of x is Ϸ0.033, which is calculated by combining concentrations rose to values probably not exceeding 1 to 2 mM present-day sulfate reduction rate estimates (40 ϫ 1012 over the next 1.6 billion years or so (1, 10–13). The increase at mol⅐yearϪ1) (25) with the burial rate of pyrite (1.2 ϫ 1012 2.4 Ga is coincident with an increase in atmospheric oxygen mol⅐yearϪ1) (26). levels (14–17) promoting the efficient oxidative weathering of In the Precambrian, values for x would have been higher. sulfide minerals on land and increasing the sulfate input to the Geochemical analysis of hundreds of Neoproterozoic sedimen- oceans (18). The first evidence for elevated sulfate concentra- tary rocks shows that these rocks typically contain iron minerals tions (Ϸ16 mM) comes from fluid inclusions in halite deposits such as iron oxides and iron carbonates that are highly reactive collected from the latest Precambrian and earliest Cambrian Ara toward sulfide (27). Because these minerals are in excess, they Group in Oman (19). Other fluid inclusion studies support would have reacted with all sulfide produced by sulfate reduc- seawater sulfate concentrations of 5 to 28 mM through the tion, minimizing sulfide loss from the sediment. Some sulfide Phanerozoic (4). This history is presented in Fig. 1. oxidation may have been promoted by wave and tide-induced Whereas the increase in sulfate concentrations at 2.4 Ga sediment mixing in near shore regions, but except for perhaps in represented the efficient oxidative weathering of sulfides in the latest Neoproterozoic (28), there was no sediment distur- response to increased atmospheric oxygen (e.g., refs. 18 and 20), bance by animals, and mechanisms for reoxidation of sulfide that it is unclear what factor or factors caused the further Phanero- would reduce x to present-day values were lacking. zoic increase in sulfate concentrations. It has been suggested that Sulfate concentration influences both the metabolic activity of the reoxidation of sulfides formed in marine sediments has an sulfate reducers (23) and the depth of sulfate penetration into important influence on seawater sulfate concentrations (21). sediments, which controls the availability of sulfate for sulfate This idea is further developed here, where sulfide oxidation by reduction and values for y. In a previous study of the global bioturbating animals is linked to the Phanerozoic increase in carbon and sulfur cycles, sulfate reduction was assumed to seawater sulfate concentrations. respond linearly to sulfate concentration, the equivalent of y ϭ 1inEq.4 (29). In our view, this value for y is too high because Model the reactive carbon available for sulfate reduction is concen- The link between bioturbation and sulfate concentrations is trated at the sediment surface. This means that although dou- developed in the following equations. First, steady state is bling sulfate concentration, for example, will increase the depth assumed, where the flux of sulfur into the oceans is assumed to of sulfate penetration, the amount of ‘‘extra’’ reactive organic equal the flux out (Eq.
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