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Abstract

Figures and Tables

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Introduction

The dramatically increased diversity of metazoan life through the late Ediacaran to early Cambrian transition (~585-510 Ma) coincides with a protracted transition from global ocean anoxia to widespread ocean oxygenation (Canfield et al., 2007

Canfield, D.E., Poulton, S.W., Narbonne, G.M. (2007) Late-Neoproterozoic Deep-Ocean Oxygenation and the Rise of Animal Life. Science 315, 92–95.

; Chen et al., 2015

Chen, X., Ling, H.-F., Vance, D., Shields-Zhou, G.A., Zhu, M., Poulton, S.W., Och, L.M., Jiang, S.-Y., Li, D., Cremonese, L., Archer, C. (2015) Rise to modern levels of ocean oxygenation coincided with the Cambrian radiation of animals. Nature Communications 6, 7142.

; Von Strandmann et al., 2015

Von Strandmann, P.A.P., Stüeken, E.E., Elliott, T., Poulton, S.W., Dehler, C.M., Canfield, D.E., Catling, D.C. (2015) Selenium isotope evidence for progressive oxidation of the Neoproterozoic biosphere. Nature Communications 6, 10157.

; Li et al., 2017

Li, C., Jin, C., Planavsky, N.J., Algeo, T.J., Cheng, M., Yang, X., Zhao, Y., Xie, S. (2017) Coupled oceanic oxygenation and metazoan diversification during the early–middle Cambrian? Geology 743–746.

). Throughout the Proterozoic Eon (2500 to 541 Ma), the ocean is thought to have been characterised by oxygenated surface waters overlying euxinic (anoxic and sulphidic) mid-depth waters along productive ocean margins (Poulton et al., 2010

Poulton, S.W., Fralick, P.W., Canfield, D.E. (2010) Spatial variability in oceanic redox structure 1.8 billion years ago. Nature Geoscience 3, 486–490.

), and ferruginous (anoxic, Fe-containing) deeper waters (Planavsky et al., 2011

Planavsky, N.J., McGoldrick, P., Scott, C.T., Li, C., Reinhard, C.T., Kelly, A.E., Chu, X., Bekker, A., Love, G.D., Lyons, T.W. (2011) Widespread iron-rich conditions in the mid-Proterozoic ocean. Nature 477, 448–451.

; Poulton and Canfield, 2011

Poulton, S.W., Canfield, D.E. (2011) Ferruginous Conditions: A Dominant Feature of the Ocean through Earth’s History. Elements 7, 107–112.

). Models for later Neoproterozoic oceans (635 to 541 Ma) also envisage redox stratification, with oscillations from strict anoxia to fully oxic conditions (Canfield et al., 2007

Canfield, D.E., Poulton, S.W., Narbonne, G.M. (2007) Late-Neoproterozoic Deep-Ocean Oxygenation and the Rise of Animal Life. Science 315, 92–95.

, 2008

Canfield, D.E., Poulton, S.W., Knoll, A.H., Narbonne, G.M., Ross, G., Goldberg, T., Strauss, H. (2008) Ferruginous Conditions Dominated Later Neoproterozoic Deep-Water Chemistry. Science 321, 949–952.

; Wood et al., 2015

Wood, R.A., Poulton, S.W., Prave, A.R., Hoffmann, K.-H., Clarkson, M.O., Guilbaud, R., Lyne, J.W., Tostevin, R., Bowyer, F., Penny, A.M., Curtis, A., Kasemann, S.A. (2015) Dynamic redox conditions control late Ediacaran metazoan ecosystems in the Nama Group, Namibia. Precambrian Research 261, 252–271.

). This dynamic ocean stratification is assumed to have persisted until the mid-Cambrian (Gill et al., 2011

Gill, B.C., Lyons, T.W., Young, S.A., Kump, L.R., Knoll, A.H., Saltzman, M.R. (2011) Geochemical evidence for widespread euxinia in the Later Cambrian ocean. Nature 469, 80–83.

; Chen et al., 2015

Chen, X., Ling, H.-F., Vance, D., Shields-Zhou, G.A., Zhu, M., Poulton, S.W., Och, L.M., Jiang, S.-Y., Li, D., Cremonese, L., Archer, C. (2015) Rise to modern levels of ocean oxygenation coincided with the Cambrian radiation of animals. Nature Communications 6, 7142.

), by which time many key metazoan innovations had evolved.

Animals are fundamentally aerobic organisms - albeit with hugely varying oxygen demands - and their early fossil record is accordingly limited to oxygenated settings (Tostevin et al., 2016

Tostevin, R., Wood, R.A., Shields, G.A., Poulton, S.W., Guilbaud, R., Bowyer, F., Penny, A.M., He, T., Curtis, A., Hoffmann, K.H., Clarkson, M.O. (2016) Low-oxygen waters limited habitable space for early animals. Nature Communications 7, 12818.

). Most current models linking early animal evolution to redox chemistry assume a horizontally stratified ocean (Wood et al., 2015

Wood, R.A., Poulton, S.W., Prave, A.R., Hoffmann, K.-H., Clarkson, M.O., Guilbaud, R., Lyne, J.W., Tostevin, R., Bowyer, F., Penny, A.M., Curtis, A., Kasemann, S.A. (2015) Dynamic redox conditions control late Ediacaran metazoan ecosystems in the Nama Group, Namibia. Precambrian Research 261, 252–271.

; Jin et al., 2016

Jin, C., Li, C., Algeo, T.J., Planavsky, N.J., Cui, H., Yang, X., Zhao, Y., Zhang, X., Xie, S. (2016) A highly redox-heterogeneous ocean in South China during the early Cambrian (∼ 529–514 Ma): Implications for biota-environment co-evolution. Earth and Planetary Science Letters 441, 38–51.

). However, modern oceans exhibit a marked lateral redox variability, most notably where combinations of high primary productivity and metazoan activity (Bianchi et al., 2013

Bianchi, D., Galbraith, E.D., Carozza, D.A., Mislan, K.A.S., Stock, C.A. (2013) Intensification of open-ocean oxygen depletion by vertically migrating animals. Nature Geoscience 6, 545–548.

) give rise to wedge-shaped oxygen minimum zones (Sperling et al., 2015a

Sperling, E.A., Knoll, A.H., Girguis, P.R. (2015a) The Ecological Physiology of Earth’s Second Oxygen Revolution. Annual Review of Ecology, Evolution, and Systematics 46, 215–235.

). Determining which of these two models, horizontal or lateral, best characterises the structure of early Palaeozoic oceans is challenged by a dearth of spatial and temporal resolution, compounded by the removal of off-shelf signals due to subduction. Here, we exploit exceptionally well-preserved successions from the Baltic Basin to derive a high resolution redox model of early to middle Cambrian shelf seas (full details of geological setting and methods are provided as Supplementary Information).

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Stratigraphy and Depositional Environments

We examined marine sediments from eight drill cores (Finngrundet-1, Bårstad-2, Bernstorp-1, Hamnudden-1, Böda Hamn-1, File Haidar-1, Grötlingbo-1 and Kostovo-13) spanning an area of 400 by 600 km across the Baltic Basin (Fig. 1). Studied sediments encompass the Lontova, File Haidar and Borgholm formations, deposited between the early Cambrian Fortunian stage and middle Cambrian Stage 5, and the internal stratigraphy and depositional environments of these siliciclastic sediments has been studied extensively (Hagenfeldt, 1994

Hagenfeldt, S.E. (1994) The Cambrian File Haidar and Borgholm Formations in the central Baltic and south central Sweden. Stockholm Contributions in Geology 43, 69–110.

; Nielsen and Schovsbo, 2011

Nielsen, A.T., Schovsbo, N.H. (2011) The Lower Cambrian of Scandinavia: depositional environment, sequence stratigraphy and palaeogeography. Earth-Science Reviews 107, 207–310.

, 2015

Nielsen, A.T., Schovsbo, N.H. (2015) The regressive Early-Mid Cambrian ‘Hawke Bay Event’ in Baltoscandia: Epeirogenic uplift in concert with eustasy. Earth-Science Reviews 151, 288–350.

). The studied area records a partial, yet substantial archive of contiguous sequences, organised into two supersequences for the lower Cambrian, ‘LC1’ and ‘LC2’, and one supersequence for the lower middle Cambrian, ‘MC3’ (Fig. 1). Nielsen and Schovsbo (2011

Nielsen, A.T., Schovsbo, N.H. (2011) The Lower Cambrian of Scandinavia: depositional environment, sequence stratigraphy and palaeogeography. Earth-Science Reviews 107, 207–310.

, 2015

Nielsen, A.T., Schovsbo, N.H. (2015) The regressive Early-Mid Cambrian ‘Hawke Bay Event’ in Baltoscandia: Epeirogenic uplift in concert with eustasy. Earth-Science Reviews 151, 288–350.

) reconstructed the depositional environment of stratigraphic successions, reporting a gradient from proximal inner-shelf to mid-shelf and outer-shelf deposition below storm wave base. Inner-shelf deposition is recognised in all cores by abundant cross-bedding features within siltstones and generally coarser lithologies accompanying falling stage system tracts (FSSTs). Mid-shelf deposition is expressed as green silts and black shales with common glauconitic horizons and silty distal storm beds. Outer-shelf deposition is recognised by the presence of laminated mudstones and bioturbated siltstones in the absence of current features.

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Results

Dominant water column redox conditions were determined via iron (Fe) speciation and trace metal systematics on mudstones and silts. Fe speciation relies on the quantification of highly reactive Fe (Fe_HR) relative to total Fe (Fe_T). Anoxic settings promote the formation of authigenic Fe minerals in the water column, resulting in Fe_HR enrichments in underlying sediments, with typically Fe_HR/Fe_T ≥ 0.38 (Poulton and Canfield, 2011

Poulton, S.W., Canfield, D.E. (2011) Ferruginous Conditions: A Dominant Feature of the Ocean through Earth’s History. Elements 7, 107–112.

). By contrast, sediments deposited under oxic water columns lack Fe_HR enrichments, with Fe_HR/Fe_T < 0.22. Ratios between 0.22-0.38 are equivocal, and may represent either anoxic or oxic conditions, due to partial transformation of Fe_HR to sheet silicates during burial. We used Fe_T/Al enrichments (≥0.6) to evaluate this mechanism in instances of equivocal Fe_HR/Fe_T, since the ratio remains unaffected by diagenesis (Lyons and Severmann, 2006

Lyons, T.W., Severmann, S. (2006) A critical look at iron paleoredox proxies: new insights from modern euxinic marine basins. Geochimica et Cosmochimica Acta 70, 5698–5722.

). For anoxic samples, ferruginous conditions are distinguished from euxinic settings by quantifying the extent of sulphidation of Fe_HR, whereby Fe_P/Fe_HR ≥ 0.7 is characteristic of euxinic deposition and Fe_P/Fe_HR < 0.7 indicates ferruginous conditions (Poulton and Canfield, 2011

Poulton, S.W., Canfield, D.E. (2011) Ferruginous Conditions: A Dominant Feature of the Ocean through Earth’s History. Elements 7, 107–112.

).

Of the eight cores analysed, seven show marked stratigraphic shifts between oxic and anoxic deposition (Fig. 2). High concentrations of total organic carbon (TOC, up to ~20 %) are associated with anoxic conditions, reflecting enhanced organic carbon preservation and supply, with the latter exerting a primary control on the development of anoxia. LC1 records dominantly anoxic conditions at the base of Kostovo-13, whereas oxic conditions prevail in the upper part of the core. Through LC2 and MC3, water column conditions are characterised predominately by ferruginous anoxia, with some euxinic horizons towards the top of Bårstad-2 and Bernstorp-1. Within these latter strata, oxic conditions prevail at the base of Grötlingbo-1 and throughout all FSSTs (Figs. 1 and 2).

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Redox variations between sequences are likely to reflect temporal changes. Furthermore, the core availability did not permit us to track each sequence in their full lateral expression. Therefore, in order to integrate water column redox data into a palaeo-environmental framework, we used the reconstructions of shelf environments in the Baltic Basin (Nielsen and Schovsbo 2011

Nielsen, A.T., Schovsbo, N.H. (2011) The Lower Cambrian of Scandinavia: depositional environment, sequence stratigraphy and palaeogeography. Earth-Science Reviews 107, 207–310.

, 2015

Nielsen, A.T., Schovsbo, N.H. (2015) The regressive Early-Mid Cambrian ‘Hawke Bay Event’ in Baltoscandia: Epeirogenic uplift in concert with eustasy. Earth-Science Reviews 151, 288–350.

) as binning discriminants (Fig. 3a). This statistical approach allows us to build a time-independent model for the redox architecture of the basin. Throughout the deposition of all successions, we observe statistically significant differences in the redox chemistry of inner-, mid- and outer-shelf environments (Table S-2). Oxic conditions systematically dominate throughout FSSTs, inner- and outer-shelf settings. Anoxic conditions, by contrast, tend to prevail in mid-shelf environments. Such distribution strongly suggests that the shelf was largely oxygenated at this time, with an expansion of anoxia limited to mid-shelves (Fig. 4). Trace metal (U and V) variations support Fe_T/Al and Fe speciation data, with pronounced sedimentary enrichments under euxinic water column conditions (Fig. 2). We note that for some instances of apparent oxic deposition based on Fe speciation (e.g., at the basal and uppermost parts of the Grötlingbo-1 core), U enrichments are coeval with muted V enrichments, indicating low-oxygen conditions (Zhang et al., 2016

Zhang, S., Wang, X., Wang, H., Bjerrum, C.J., Hammarlund, E.U., Costa, M.M., Connelly, J.N., Zhang, B., Su, J., Canfield, D.E. (2016) Sufficient oxygen for animal respiration 1,400 million years ago. Proceedings of the National Academy of Sciences 113, 1731–1736.

), comparable to that seen in modern OMZs (see Supplementary Information for details).

We complemented the inorganic redox proxies with biomarker indicators selected from mid-shelf sediments (Finngrundet-1, Bårstad-2, Bernstorp-1). The ratio of pristane to phytane (Pr/Ph) is low (0.46-0.79), supporting a dominantly anoxic mid-depth water column (Schwark and Frimmel, 2004

Schwark, L., Frimmel, A. (2004) Chemostratigraphy of the Posidonia Black Shale, SW-Germany: II. Assessment of extent and persistence of photic-zone anoxia using aryl isoprenoid distributions. Chemical Geology 206, 231–248.

). In these anoxic environments, 2,3,6-trimethyl aryl isoprenoids (AI) likely derived from anaerobic phototrophic green sulphur bacteria (GSB), and their detection indicates that the water column was temporarily anoxic up to the photic zone (Brocks et al., 2005

Brocks, J.J., Love, G.D., Summons, R.E., Knoll, A.H., Logan, G.A., Bowden, S.A. (2005) Biomarker evidence for green and purple sulphur bacteria in a stratified Palaeoproterozoic sea. Nature 437, 866–870.

). The ratio between shorter- (C₁₃ to C₁₇) and longer-chain (C₁₈ to C₂₂) AI (the AI ratio, AIR) is used as a measure of oxidative degradation during deposition (Schwark and Frimmel, 2004

Schwark, L., Frimmel, A. (2004) Chemostratigraphy of the Posidonia Black Shale, SW-Germany: II. Assessment of extent and persistence of photic-zone anoxia using aryl isoprenoid distributions. Chemical Geology 206, 231–248.

). Despite AI production in anoxic settings, the range and magnitude of AIR values (1.3 to 5.8) provide independent support for transient oxygenated conditions beneath the anoxic zone (Fig. 3b). Together with our Fe speciation data, this suggests that anoxic mid-depth waters overlaid oxygenated waters, enhancing oxidative degradation of AI during deposition.

Further evidence for distinct redox conditions across the shelf comes from the record of ‘small carbonaceous fossils’ (SCFs) (Butterfield and Harvey, 2012

Butterfield, N., Harvey, T. (2012) Small carbonaceous fossils (SCFs): a new measure of early Paleozoic paleobiology. Geology 40, 71–74.

), found in oxic inner- and outer-shelf settings and ferruginous mid-shelf environments (Fig. 1). All recognisable SCFs are the remains of benthic aerobic animals, including Wiwaxia, stem-annelids, priapulids and palaeoscolecid worms (Fig. 3c). In contrast to sparsely fossiliferous mid-shelves, inner- and outer-shelf facies preserved most diverse SCFs assemblages, along with conspicuous burrows and bioturbation fabrics (Slater et al., 2017

Slater, B.J., Harvey, T.H.P., Guilbaud, R., Butterfield, N.J. (2017) A cryptic record of Burgess Shale-type diversity from the early Cambrian of Baltica. Palaeontology 60, 117–140.

). These palaeontological data corroborate the geochemical signatures for oxygenated inner- and outer-shelf environments (Fig. 3c). Fossilisation is of course a combination of both organismal ecology and taphonomic opportunity. Transient ferruginous conditions represent the dynamic interface between the oxic conditions where most metazoans live, and the anoxic conditions necessary to preserve non-biomineralising forms. Therefore, the apparently paradoxical persistence of SCFs in ferruginous settings may imply an iron shuttle from the core to the edges of the OMZ, enhancing the Fe_HR flux to oxygenated settings, or more likely dynamic oscillations between oxic and ferruginous water column conditions – in contrast to more permanently anoxic mid-shelves which were devoid of benthic metazoans and prone to euxinia.

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Implications

Our data provide evidence for a lateral expression of redox variation, which resembles the structure of modern OMZs (Fig. 4), although oxygen depletion was likely more pronounced and at shallower depths than in modern counterparts. Gentle topographical slope and reduced circulation in the relatively shallow Baltic Basin may have further exacerbated the role of benthic oxygen uptake, analogous to shallow OMZs (Brandt et al., 2015

Brandt, P., Bange, H.W., Banyte, D., Dengler, M., Didwischus, S.-H., Fischer, T., Greatbatch, R.J., Hahn, J., Kanzow, T., Karstensen, J., Körtzinger, A., Krahmann, G., Schmidtko, S., Stramma, L., Tanhua, T., Visbeck, M. (2015) On the role of circulation and mixing in the ventilation of oxygen minimum zones with a focus on the eastern tropical North Atlantic. Biogeosciences (BG) 12, 489–512.

). The discovery of OMZ denitrification in early Cambrian successions of China (Hammarlund et al., 2017

Hammarlund, E.U., Gaines, R.R., Prokopenko, M.G., Qi, C., Hou, X.-G., Canfield, D.E. (2017) Early Cambrian oxygen minimum zone-like conditions at Chengjiang. Earth and Planetary Science Letters 475, 160–168.

) suggests that our model may have been a common feature of contemporaneous margins. The record of ancient marine sedimentary rocks is certainly biased towards continental margins, which promotes the sampling of environments prone to host OMZs. Thus, in the absence of detailed spatial and temporal resolution, apparent horizontal stratification may often capture the upper boundary of OMZs, over-estimating global deep-water anoxia. By contrast, the recognition of such structure would explain the large discrepancies reported through the Neoproterozoic-Cambrian transition (e.g., Sperling et al., 2015b

Sperling, E.A., Wolock, C.J., Morgan, A.S., Gill, B.C., Kunzmann, M., Halverson, G.P., Macdonald, F.A., Knoll, A.H., Johnston, D.T. (2015b) Statistical analysis of iron geochemical data suggests limited late Proterozoic oxygenation. Nature 523, 451–454.

). Our data augments emerging views of early Cambrian expanded marine oxygenated conditions (Chen et al., 2015

Chen, X., Ling, H.-F., Vance, D., Shields-Zhou, G.A., Zhu, M., Poulton, S.W., Och, L.M., Jiang, S.-Y., Li, D., Cremonese, L., Archer, C. (2015) Rise to modern levels of ocean oxygenation coincided with the Cambrian radiation of animals. Nature Communications 6, 7142.

; Li et al., 2017

Li, C., Jin, C., Planavsky, N.J., Algeo, T.J., Cheng, M., Yang, X., Zhao, Y., Xie, S. (2017) Coupled oceanic oxygenation and metazoan diversification during the early–middle Cambrian? Geology 743–746.

), supporting the establishment of a modern-like ocean architecture during the ‘explosion’ of metazoan diversity (Butterfield, 2018

Butterfield, N.J. (2018) Oxygen, animals and aquatic bioturbation: An updated account. Geobiology 16, 3–16.

).

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Conclusion

Identification of dynamic wedge-shaped OMZs along the margins of the early Cambrian Baltic Basin raises the question of the antiquity of such structures. The evolutionary switch from a prokaryote- to eukaryote-dominated biological pump is thought to have played an essential role in the ventilation of the deep ocean (Butterfield, 2009

Butterfield, N.J. (2009) Oxygen, animals and oceanic ventilation: an alternative view. Geobiology 7, 1–7.

, 2018

Butterfield, N.J. (2018) Oxygen, animals and aquatic bioturbation: An updated account. Geobiology 16, 3–16.

; Lenton et al., 2014

Lenton, T.M., Boyle, R.A., Poulton, S.W., Shields-Zhou, G.A., Butterfield, N.J. (2014) Co-evolution of eukaryotes and ocean oxygenation in the Neoproterozoic era. Nature Geoscience 7, 257–265.

). The subsequent establishment of modern-type OMZs, as identified in the early Cambrian ocean, may have developed as a consequence of contemporaneous metazoan expansion, whereby animal activity maintains high levels of oxygen depletion in OMZs (Bianchi et al., 2013

Bianchi, D., Galbraith, E.D., Carozza, D.A., Mislan, K.A.S., Stock, C.A. (2013) Intensification of open-ocean oxygen depletion by vertically migrating animals. Nature Geoscience 6, 545–548.

). However, OMZ structures may track back to older, Mesoproterozoic oceans (Zhang et al., 2016

Zhang, S., Wang, X., Wang, H., Bjerrum, C.J., Hammarlund, E.U., Costa, M.M., Connelly, J.N., Zhang, B., Su, J., Canfield, D.E. (2016) Sufficient oxygen for animal respiration 1,400 million years ago. Proceedings of the National Academy of Sciences 113, 1731–1736.

). Although fundamental differences in pre-metazoan biological pump may have given terminal Proterozoic OMZs a distinct expression (presumably thicker and shallower), this overall geometry may have been a prevalent feature of late Precambrian oceans.

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Acknowledgements

We are thankful to Linda Wickström (Geological Survey of Sweden), Ursula Toom, Olle Hints and Heikki Bauert (Tallinn University of Technology), and Tõnis Saadre (Estonian Geological Survey) for sampling support, and James Rolfe, Jason Day and Janet Hope for analytical technical support. The authors are thankful to the constructive comments of T. Lyons, C. Scott and an anonymous reviewer. This work was funded by NERC (NE/K005251/1). SWP acknowledges support from a Royal Society Wolfson Research Merit Award.

Editor: Liane G. Benning

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Author Contributions

RG, BJS, THPH and NJB collected samples. RG extracted and interpreted geochemical data with significant contributions from BJN, JJB and SWP. BJS extracted and interpreted palaeontological data with significant contributions from THPH and NJB. RG and BJS wrote the manuscript, with significant contributions from all co-authors.

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References

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Supplementary Information

The Supplementary Information includes:

• Geological Descriptions
• Methods
• Trace Metal Geochemistry
• Biomarker Maturity and Redox Indicators
• Distribution of Redox Data through Depositional Environments
• Distribution of SCFs and Diversity
• Tables S-1 (Excel Download) and S-2
• Figures S-1 to S-4
• Supplementary Information References

Download the Supplementary Information (PDF).
Download Table S-1 (Excel file).