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Animal evolution, bioturbation, and the 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 on a 40 massive scale, aiding in the decomposition of 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 . 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 ͉ ͉ 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 cycle. (Top) nism (1). It leaves the ocean as either (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 (NaCl) and record. Through the Phanerozoic, the data has been binned from individual GEOLOGY becomes an important evaporite component when the 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 (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 (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 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 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. 2): matter encountered with depth will likely not equal the amount oxidized near the surface at the lower sulfate levels. Therefore, ϭ Fluxin Fluxout [2] sulfate reduction rates will likely increase by factor of Ͻ2in response to a doubling of sulfate concentration. In the modeling Sulfur leaves the oceans either as minerals in below, we will explore values of y ranging from 0.3 to 0.75; the evaporite deposits, or as pyrite buried in sediments. The amount value of y ϭ 0.3 most closely fits with the results of a previous of pyrite buried is related to the amount of sulfide produced by modeling study that explored the relationship between sulfate sulfate reducers by a stoichiometric factor called x. When x ϭ 0.1, concentration and sulfate reduction rate in nonbioturbated for example, 10% of the sulfide produced by sulfate reduction is sediments (9). buried in sediments and 90% is reoxidized. Overall: Model Results and Discussion ϭ ϩ Fluxout xSR evap [3] The model is run assuming modern S input rates of 3.3 ϫ 1012 ⅐ Ϫ1 ϫ 12 where SR is sulfate reduction rate and evap is the rate of sulfur mol year , which include a contribution of 2.6 10 ⅐ Ϫ1 ϫ 12 ⅐ Ϫ1 removed in evaporites. Sulfate reduction rate will depend on mol year from rivers (21, 30), 0.5 10 mol year from mid ϫ 12 ⅐ Ϫ1 both the availability of reactive organic carbon (22) and sulfate ocean ridge hydrothermal sources (31) and 0.2 10 mol year concentration (9, 23). The relationship between these variables from subaerial volcanics (1). The model results do not greatly and sulfate reduction rate is expressed in Eq. 4, where a is a depend on the value of this input flux; the main effect of altering constant of proportionality, y is an exponential factor and OC this value will be to change the response time of the system to expresses the concentration of reactive organic carbon available changes in the initial input parameters. Thus, higher input rates for sulfate reduction. will reduce the response time of the system and lower input rates will increase the response time, with little influence on the ϭ ͓ ͔y magnitude of the response in sulfate concentration. Also, be- SR aOC SO4 [4] cause this model is designed to predict the transition from late Combining equations 2, 3 and 4 yields a simple expression for Precambrian nonbioturbated conditions to early Phanerozoic, steady state sulfate concentration in the oceans: we must consider whether or not probable reduced late Pre- cambrian atmospheric oxygen levels would have influenced the ͓ Ϫ ͔ 1/y fluxin evap weathering flux of sulfides. In other words, is there a hidden ͓SO ͔ ϭ ͫ ͬ [5] 4 axOC oxygen sensitivity in the model? We do not believe so, because the oxygen requirement for efficient sulfide weathering (Ͻ0.5% We believe it most likely that x has varied much more than OC present levels) (20) is very low compared with estimates for late availability from the Precambrian into the Phanerozoic, and we Precambrian atmospheric oxygen (Ϸ10% present levels) (27). therefore ignore OC in Eq. 5. Holding fluxin constant and The model assumes an isotope fractionation of 35 ‰ between ignoring (for the moment) the formation of evaporites, x and y seawater sulfate and the sulfide buried in sediments, a starting are the most important factors controlling marine sulfate sulfate concentration of 1 mM, and it starts with no gypsum concentrations. burial. We then chose a value of y within the range of 0.3 to 0.75 Presently, most of the sulfide produced by sulfate-reducing as discussed above. With a given value of y, a value of a was then is reoxidized (x is close to 0; see below) (24). Reoxida- calculated from Eq. 4, using the modern sulfate level (28 mM) tion is promoted by animals that mix and stir the sediment while and modern rates of sulfate reduction. This value of a was foraging for food and building shelters. This bioturbation com- assumed to apply to all sulfate levels, and with it, sulfate

8124 ͉ www.pnas.org͞cgi͞doi͞10.1073͞pnas.0902037106 Canfield and Farquhar Downloaded by guest on September 29, 2021 Table 1. Model input parameters 80 y=0.75

Parameter Magnitude 70 SEE COMMENTARY Sulfur input rate 3.3 ϫ 1012 mol⅐yearϪ1 Sulfate 60 δ34S ϫ 12 ⅐ Ϫ1 Modern sulfate reduction rate 40 10 mol year SRR Modern pyrite burial rate 1.2 ϫ 1012 mol⅐yearϪ1 50 Ϫ Cenozoic sulfate burial rate 2.1 ϫ 1012 mol⅐year 1 40 Modern value for x 0.033 Prebioturbation sulfate level 1 mM 30 Modern sulfate level 28 mM 20 Modern sulfate reservoir 3.8 ϫ 1019 mol 10

0 y=0.5 reduction rates could be calculated for our initial starting sulfate ) 70 concentration. With an estimate of sulfate reduction rates, initial -1 values of x are obtained from Eq. 3 so that rates of pyrite burial 60 mol y S (per mil)

matched the sulfur input rate. Therefore, initial values of x are 12 34 50 not independent, but depend on choices for y and the initial δ sulfate concentration. However, in all cases explored, x values 40 were much higher than present-day values and in line with the 30 idea that they would have been higher in the absence of bioturbation. Model input parameters are in Tables 1 and 2, and 20 model results are in Fig. 2. 10 Model runs are initialized and then bioturbation is turned on, 0 which is accomplished by reducing x to 0.033 (the modern value). y=0.3 This reduces pyrite burial, and as a result, sulfate concentration 70 increases. Increasing sulfate concentration acts to increase rates EVOLUTION Sulfate Reduction Rate (x 10 60 of sulfate reduction, which, in turn, increase rates of pyrite burial. Sulfate Concentration (mM), bioturbation on With the functionalities between sulfate reduction rate in sulfate 50 gypsum on bioturbation off gypsum off concentration we use, sulfate concentrations will continue to 40 increase to 100 mM or more before they stabilize. However, in our model, as in the real world, sulfate depositing as gypsum 30 becomes a significant sulfate removal pathway at elevated sulfate 20

concentrations. In our model, we switch on evaporite deposition GEOLOGY when sulfate exceeds 20 mM, to yield an f value of 0.36 (see Eq. 10 1), comparable to the modern value (Fig. 1). Clearly, some 0 gypsum deposited in the Precambrain under lower sulfate con- 01020304050607080 centrations than this, but as mentioned above, gypsum deposi- Time (Ma) tion was only a minor sulfate removal pathway until the Pha- Fig. 2. Model calculations showing the influence of bioturbation on the nerozoic (Fig. 1). In line with the above discussion and consistent sulfate concentration of the oceans with different values of y as used in with the results in Fig. 1, gypsum deposition more likely acts as equations 4 and 5. In all cases, an increase in bioturbation leads to an increase a cap keeping sulfate from becoming too high rather than a in sulfate concentrations, an increase in sulfate reduction rate, and a decrease means of keeping sulfate concentration low. in the isotopic composition of sulfate in seawater. The initiation of gypsum In the present model, sulfate deposition at higher sulfate evaporite formation to modern proportions of sulfur removal from the oceans stabilizes the system. If bioturbation ceases, sulfate levels and sulfate reduc- concentration stabilizes the system to approximately modern tion rates drop, with a transient increase in the isotopic composition of sulfate levels and sulfate isotopic composition. The model runs seawater sulfate. In modeling this event, the increase in sulfide burial associ- are then perturbed a second time to explore how the system ated with the stop in bioturbation was not allowed to exceed 7.46 ϫ 1012 recovers. The value of x is restored to its prebiotubation values, mol⅐yearϪ1, which is the amount of sulfide yielding a 1.36 wt% S concentration and gypsum deposition is stopped. Lowering x increases rates of in sediments, the maximum pyrite S content assuming a reactive Fe concen- Ϫ pyrite burial, and the sulfate concentration falls to the starting tration of 1 wt% and a sediment input rate of 1.8 ϫ 1016 g⅐year 1 (26, 48). value. An interesting consequence of the high initial sulfur burial rate is a transient increase in the isotopic composition of sulfate. This exercise illustrates how oceanic sulfate would respond to This pattern is a reservoir effect that is reproduced under all an increase in sulfur oxidation rate brought about by bioturba- model scenarios. The most important difference between the tion. Changes in the magnitude of sulfide reoxidation, as ex- models is that at lower values of y, the system is less responsive pressed here by the value x, have a strong influence on seawater to perturbations and rates of sulfate reduction vary less in sulfate concentrations, a point also made in reference (1). If the response to changing sulfate concentrations. onset (evolution) of bioturbation drove a reduction of x, which we contend is likely, it seems almost inescapable that sulfate levels would have increased. We maintain here that such a rise Table 2. Initial model parameters for different values of y in sulfate levels promoted the substantial deposition of sulfate Initial sulfate reduction evaporites, which the isotope record indicates is largely a Pha- yx a rate, mol⅐yearϪ1 nerozoic phenomenon. Neoproterozoic values for x are difficult to constrain. The minor sulfur isotopic composition of Neopro- 0.75 1.0 3.18 ϫ 1012 3.18 ϫ 1012 terozoic records the influence of sulfide oxidation in the 0.50 0.44 7.56 ϫ 1012 7.56 ϫ 1012 marine through sulfur disproportionation reactions 0.30 0.22 14.7 ϫ 1012 14.7 ϫ 1012 (32), but the value of x is difficult to extract from this data. We

Canfield and Farquhar PNAS ͉ May 19, 2009 ͉ vol. 106 ͉ no. 20 ͉ 8125 Downloaded by guest on September 29, 2021 suggest that values were likely well Ͻ1, and perhaps as low as correct; that the evolution of bioturbation and its influence on 0.22. This lower value for x arises from calibration of our model sulfide oxidation in sediments generated a severalfold increase with a y value of 0.3, as discussed above (Table 2). in seawater sulfate concentration, and that this led to the The geologic record shows that the earliest evidence for substantial deposition of sulfate evaporites in the Phanerozoic. animal foraging and feeding on the sediment surface is found at Finally, the model also holds a testable prediction. As shown least 10–15 million years before the Cambrian–Precambrian in Fig. 2, a cessation of bioturbation results in a drop in sulfate boundary (33, 34). The first evidence for deeper 3-dimensional concentration and a transient increase in the ␦34S of sulfate. The sediment burrowing occurs near, but still below the boundary end Permian mass extinction provides a potential test of this (35). Bioturbation intensity increased substantially into the early model prediction. Here, perhaps as many as 95% of marine Cambrian (28) but did not reach full intensity until the Upper animal species went extinct (43), manifest in a dramatic reduc- Ordovician (445–460 Ma) as evidenced by the intensity of tion in bioturbation and a near collapse of marine benthic animal disturbance of sedimentary fabric (36) and the expansion of ecosystems (43). The recovery was slow, taking some 4 million bioturbators into offshore sediments (37). This record of bio- years (44). Sulfate concentrations are not constrained through turbation intensity is approximately congruent with the history this time interval, but the isotope record of seawater sulfate ␦34 Ϸ of sulfate burial (Fig. 1) where sulfate removal from the oceans shows a rapid increase from low S values of 17 permil at the as evaporites becomes important after the Ordovician. Permian-Triassic boundary to up to 38 per mil in the Spathian There is, however, one apparent incongruity with model some 3–4 million years later (45). Full biotic recovery occurred ␦34 Ϸ predictions. As mentioned above, the earliest evidence for high in the early-middle Triassic where S values returned to 18 sulfate concentrations comes from fluid inclusions within the per mil (46). This pattern has been explained by mixing of latest Neoproterozoic and earliest Cambrian Ara evaporites isotopically enriched sulfate from an anoxic-sulfidic deep ocean onto the shelf, where it is then captured in evaporites and as a from Oman. These high sulfate levels appear contemporane- structural component of carbonate minerals (so-called ‘‘CAS’’; ously with the evolution of 3D sediment burrowing, so it is CAS itself should be a minor sink for sulfate) (45, 47). The model tempting to relate the two. However, bioturbation intensity in here provides an alternative explanation. We argue that the the late Neoproterozoic was most probably low with an uncertain collapse of benthic marine animal ecosystems and their associ- x influence on (28, 34). This incongruity could indicate that ated bioturbating activities caused a transient increase in the ␦34S factors other than bioturbation also influenced seawater sulfate of seawater sulfate consistent with the modeling in Fig. 2. concentration. These factors would include organic matter as it In summary, the evolution of bioturbating organisms had a influences rates of sulfate reduction (see Eq. 5), sedimentation profound impact on the concentrations of sulfate in the oceans. rate as it influences rates of pyrite burial (38) and sealevel Indeed, we propose that the oxidation of sedimentary sulfides change as it influences a number of things including the recycling associated with sediment stirring by benthic animals has resulted of recently exposed sediment, the availability of land area for in a severalfold increase in seawater sulfate concentrations, weathering, and shelf area where the highest rates of sulfate initiating the widespread deposition of gypsum evaporites. The reduction are encountered. Indeed, the latest Neoproterozoic cessation of bioturbation associated with major extinctions and earliest Cambrian was a time of geological and geochemical would have also influenced sulfate concentrations and left an turmoil as indicated by a rapid fall in sealevel (39), and large imprint in the isotopic composition of seawater sulfate. carbon, sulfur isotope and Sr isotope anomolies (40–42), the generation of which are still not well understood. Therefore, it ACKNOWLEDGMENTS. We thank Bo Thamdrup, Andy Knoll, Minik Rosing, is possible the high sulfate concentrations as inferred during Tim Lowenstein, Chris Honeycutt, and Doug Erwin for valuable comments and deposition of the Ara evaporites was a transient event and a input and to Andy Knoll and Simon Poulton for illuminating comments on the manuscript. This work was supported by the Danish National Research Foun- product of this turmoil, although exact causes are not clear. We dation (Danmarks Grundforskningsfond). J.F. acknowledges support from the maintain, however, that the broad picture outlined here is Guggenheim Foundation and NASA ExB.

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