Advertisement

Aquatic Geochemistry

, Volume 22, Issue 5–6, pp 469–504 | Cite as

The Influence of Bioturbation on Iron and Sulphur Cycling in Marine Sediments: A Model Analysis

  • Sebastiaan van de VeldeEmail author
  • Filip J. R. Meysman
Original Article

Abstract

The geochemical cycles of iron and sulphur in marine sediments are strongly intertwined and give rise to a complex network of redox and precipitation reactions. Bioturbation refers to all modes of transport of particles and solutes induced by larger organisms, and in the present-day seafloor, bioturbation is one of the most important factors controlling the biogeochemical cycling of iron and sulphur. To better understand how bioturbation controls Fe and S cycling, we developed reactive transport model of a coastal sediment impacted by faunal activity. Subsequently, we performed a model sensitivity analysis, separately investigating the two different transport modes of bioturbation, i.e. bio-mixing (solid particle transport) and bio-irrigation (enhanced solute transport). This analysis reveals that bio-mixing and bio-irrigation have distinct—and largely opposing effects on both the iron and sulphur cycles. Bio-mixing enhances transport between the oxic and suboxic zones, thus promoting the reduction of oxidised species (e.g. iron oxyhydroxides) and the oxidation of reduced species (e.g. iron sulphides). Through the re-oxidation of iron sulphides, bio-mixing strongly enhances the recycling of Fe and S between their reduced and oxidised states. Bio-irrigation on the other hand removes reduced solutes, i.e. ferrous iron and free sulphide, from the sediment pore water. These reduced species are then reoxidised in the overlying water and not recycled within the sediment column, which leads to a decrease in Fe and S recycling. Overall, our results demonstrate that the ecology of the macrofauna (inducing bio-mixing or bio-irrigation, or both) matters when assessing their impact on sediment geochemistry. This finding seems particularly relevant for sedimentary cycling across Cambrian transition, when benthic fauna started colonizing and reworking the seafloor.

Keywords

Reactive transport modelling Diagenetic cycling Iron Sulphur Bioturbation Bio-mixing Bio-irrigation 

Notes

Acknowledgments

The research leading to these results has received funding from the European Research Council under the European Union’s Seventh Framework Programme (FP/2007–2013) through ERC Grant 306933 (FJRM) and was financially supported by Research Foundation Flanders (FWO Aspirant Ph.D. Fellowship to SVDV).

Supplementary material

10498_2016_9301_MOESM1_ESM.docx (209 kb)
Supplementary material 1 (DOCX 209 kb)
10498_2016_9301_MOESM2_ESM.docx (105 kb)
Supplementary material 2 (DOCX 105 kb)

References

  1. Ahonen L, Tuovinen OH (1991) Temperature Effects on Bacterial leaching of Sulfide minerals in shake flask experiments. Appl Environ Microbiol 57:138–145Google Scholar
  2. Aller RC (1977) The influence of macrobenthos on chemical diagenesis of marine sediments. PhD thesis, Yale University, New Haven, Connecticut, 600 ppGoogle Scholar
  3. Aller RC (1994) The sedimentary Mn cycle in Long Island Sound: its role as intermediate oxidant and the influence of bioturbation, O2, and Corg flux on diagenetic reaction balances. J Mar Res 52:259–295. doi: 10.1357/0022240943077091 CrossRefGoogle Scholar
  4. Aller RC (2014) Sedimentary diagenesis, depositional environments, and benthic fluxes. Treatise on geochemistry, 2nd edn. Elsevier Ltd., Amsterdam, pp 293–334CrossRefGoogle Scholar
  5. Aller RC, Rude PD (1987) Complete oxidation of solid phase sulfides by manganese and bacteria in anoxic marine sediments. Geochim Cosmochim Acta 52:751–765CrossRefGoogle Scholar
  6. Aller RC, Aller JY (1998) The effect of biogenic irrigation intensity and solute exchange on diagenetic reaction rates in marine sediments. J Mar Res 56:905–936. doi: 10.1357/002224098321667413 CrossRefGoogle Scholar
  7. Aller RC, Macking JE, Cox RTJ (1986) Diagenesis of Fe and S in Amazon inner shelf muds: apparent dominance of Fe reduction and implications for the genesis of ironstones. Cont Shelf Res 6:263–289CrossRefGoogle Scholar
  8. Banta GT, Holmer M, Jensen MH, Kristensen E (1999) Effects of two polychaete worms, Nereis diversicolor and Arenicola marina, on aerobic and anaerobic decomposition in a sandy marine sediment. Aquat Microb Ecol 19:189–204. doi: 10.3354/ame019189 CrossRefGoogle Scholar
  9. Berg P, Rysgaard S, Thamdrup B (2003) Dynamic modeling of early diagenesis and nutrient cycling. A case study in an artic marine sediment. Am J Sci 303:905–955. doi: 10.2475/ajs.303.10.905 CrossRefGoogle Scholar
  10. Berner RA (1970) Sedimentary pyrite formation. Am J Sci 268:1–23. doi: 10.2475/ajs.268.1.1 CrossRefGoogle Scholar
  11. Berner RA (1981) A new geochemical classification of sedimentary Environments. J Sediment Petrol 51:359–365Google Scholar
  12. Berner RA, Westrich JT (1985) Bioturbation and the early diagenesis of carbon and sulfur. Am J Sci 285:193–206CrossRefGoogle Scholar
  13. Boudreau BP (1984) On the equivalence of nonlocal and radial-diffusion models for porewater irrigation. J Mar Res 42:731–735. doi: 10.1357/002224084788505924 CrossRefGoogle Scholar
  14. Boudreau BP (1996) The diffusive tortuosity of fine-grained unlithified sediments. Geochim Cosmochim Acta 60:3139–3142. doi: 10.1016/0016-7037(96)00158-5 CrossRefGoogle Scholar
  15. Boudreau BP (1997) Diagenetic models and their Implementation. Springer, BerlinCrossRefGoogle Scholar
  16. Boudreau BP (1998) Mean mixed depth of sediments: the wherefore and the why. Limnol Oceanogr 43:524–526CrossRefGoogle Scholar
  17. Brown PN, Byrne GD, Hindmarsh AC (1989) VODE, a variable-coefficient ODE solver. SIAM J Sci Stat Comput 10:1038–1051CrossRefGoogle Scholar
  18. Burdige DJ (1993) The biogeochemistry of manganese and iron reduction in marine sediments. Earth Sci Rev 35:249–284. doi: 10.1016/0012-8252(93)90040-E CrossRefGoogle Scholar
  19. Burdige DJ (2006) Geochemistry of marine sediments. Princeton University Press, PrincetonGoogle Scholar
  20. Cameron EM (1982) Sulphate and sulphate reduction in early Precambrian oceans. Nature 296:145–148. doi: 10.1017/CBO9781107415324.004 CrossRefGoogle Scholar
  21. Canfield DE (1989) Reactive iron in marine sediments. Geochim Cosmochim Acta 53:619–632. doi: 10.1016/0016-7037(89)90005-7 CrossRefGoogle Scholar
  22. Canfield DE, Farquhar J (2009) Animal evolution, bioturbation, and the sulfate concentration of the oceans. Proc Natl Acad Sci 106:8123–8127CrossRefGoogle Scholar
  23. Canfield DE, Thamdrup B (2009) Towards a consistent classification scheme for geochemical environments, or, why we wish the term ‘suboxic’ would go away. Geobiology 7:385–392. doi: 10.1111/j.1472-4669.2009.00214
  24. Canfield DE, Jorgensen BB, Fossing H et al (1993) Pathways of organic carbon oxidation in three continental margin sediments. Mar Geol 113:27–40. doi: 10.1016/0025-3227(93)90147-N CrossRefGoogle Scholar
  25. Canfield DE, Habicht KS, Thamdrup B (2000) The Archean sulfur cycle and the early history of atmospheric oxygen. Science 288:658–661. doi: 10.1126/science.288.5466.658 CrossRefGoogle Scholar
  26. Canfield DE, Poulton SW, Narbonne GM (2007) Late-neoproterozoic deep-ocean oxygenation and the rise of animal life. Science 315:92–95. doi: 10.1126/science.1135013 CrossRefGoogle Scholar
  27. Canfield DE, Ngombi-pemba L, Hammarlund EU et al (2013) Oxygen dynamics in the aftermath of the Great Oxidation of Earth’ s atmosphere. Proc Natl Acad Sci 110:16736–16741. doi: 10.1073/pnas.1315570110 CrossRefGoogle Scholar
  28. Chen X, Ling H-F, Vance D et al (2015) Rise to modern levels of ocean oxygenation coincided with the Cambrian radiation of animals. Nat Commun 6:7142. doi: 10.1038/ncomms8142 CrossRefGoogle Scholar
  29. Dale AW, Nickelsen L, Scholz F et al (2015) A revised global estimate of dissolved iron fluxes from marine sediments. Global Biogeochem Cycles 29:1–17. doi: 10.1002/2013GB004679.Received CrossRefGoogle Scholar
  30. Fick A (1855) Uber Diffusion. Ann Phys (N Y) 94:59–86CrossRefGoogle Scholar
  31. Fossing H, Berg P, Thamdrup B, Rysgaard S, Sørensen HM, Nielsen K (2004) A model set-up for an oxygen and nutrient flux model for Aarhus Bay (Denmark). NERI Technical Report No. 483, National Environmental Research Institute, Denmark, 65 ppGoogle Scholar
  32. François F, Gerino M, Stora G et al (2002) Functional approach to sediment reworking by gallery-forming macrobenthic organisms: modeling and application with the polychaete Nereis diversicolor. Mar Ecol Prog Ser 229:127–136. doi: 10.3354/meps229127 CrossRefGoogle Scholar
  33. Gilbert F, Hulth S, Grossi V et al (2007) Sediment reworking by marine benthic species from the Gullmar Fjord (Western Sweden): importance of faunal biovolume. J Exp Mar Biol Ecol 348:133–144. doi: 10.1016/j.jembe.2007.04.015 CrossRefGoogle Scholar
  34. Goldhaber M, Kaplan I (1974) The sulfur cycle. In: Goldberg E (ed) The sea, 5th edn. Wiley-Interscience, New YorkGoogle Scholar
  35. Guilbaud R, Poulton SW, Butterfield NJ et al (2015) A global transition to ferruginous conditions in the early Neoproterozoic oceans. Nat Geosci. doi: 10.1038/NGEO2434 Google Scholar
  36. Hines ME, Jones GE (1985) Microbial biogeochemistry and bioturbation in the sediments of Great Bay, New Hampshire. Estuar Coast Shelf Sci 20:729–742CrossRefGoogle Scholar
  37. Hofmann AF, Meysman FJR, Soetaert K, Middelburg JJ (2008) A step-by-step procedure for pH model construction in aquatic systems. Biogeosciences 5:227–251. doi: 10.5194/bgd-4-3723-2007 CrossRefGoogle Scholar
  38. Jørgensen BB (1982) Mineralization of organic matter in the sea bed—the role of sulphate reduction. Nature 296:643–645CrossRefGoogle Scholar
  39. Jørgensen BB, Gallardo VA (1999) Thioploca spp.: filamentous sulfur bacteria with nitrate vacuoles. FEMS Microbiol Ecol 28:301–313CrossRefGoogle Scholar
  40. Jørgenson BB, Nelson DC (2004) Sulfide oxidation in marine sediments: geochemistry meets microbiology. In: Amend JP, Edwards KJ, Lyons TW (eds) Sulfur biogeochemistry past and present. The Geological Society of America, Inc., Bouldor, Colorado, pp 63–82Google Scholar
  41. Jørgensen BB, Glud RN, Holby O (2005) Oxygen distribution and bioirrigation in Arctic fjord sediments (Svalbard, Barents Sea). Mar Ecol Prog Ser 292:85–95CrossRefGoogle Scholar
  42. Kristensen E, Kostka JE (2005) Macrofaunal burrows and irrigation in marine sediment: microbiological and biogeochemical interactions. Interact Between Macro Microorg Mar Sediments. doi: 10.1029/CE060p0125 CrossRefGoogle Scholar
  43. Katsev S, Sundby B, Mucci A (2006) Modeling vertical excursions of the redox boundary in sediments: Application to deep basins of the Arctic Ocean. Limnol and Oceanogr 51(4):1581–1593CrossRefGoogle Scholar
  44. Kristensen E, Ahmed SI, Devol AH (1995) Aerobic and anaerobic decomposition of organic matter in marine sediment: which is fastest? Limnol Oceanogr 40:1430–1437CrossRefGoogle Scholar
  45. Kristensen E, Penha-Lopes G, Delefosse M et al (2012) What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Mar Ecol Prog Ser 446:285–302. doi: 10.3354/meps09506 CrossRefGoogle Scholar
  46. Lenton TM, Boyle RA, Poulton SW et al (2014) Co-evolution of eukaryotes and ocean oxygenation in the Neoproterozoic era. Nat Geosci 7:257–265. doi: 10.1038/NGEO2108 CrossRefGoogle Scholar
  47. Lovley DR (1991) Dissimilatory Fe(III) and Mn(IV) reduction. Microbiol Rev 55:259–287Google Scholar
  48. Lyons TW, Severmann S (2006) A critical look at iron paleoredox proxies: new insights from modern euxinic marine basins. Geochim Cosmochim Acta 70:5698–5722. doi: 10.1016/j.gca.2006.08.021 CrossRefGoogle Scholar
  49. Meile C, Berg P, Van Cappellen P, Tuncay K (2005) Solute-specific pore water irrigation: implications for chemical cycling in early diagenesis. J Mar Res 63:601–621. doi: 10.1357/0022240054307885 CrossRefGoogle Scholar
  50. Meysman FJR, Middelburg JJ, Herman PMJ, Heip CHR (2003) Reactive transport in surface sediments. II. Media: an object-oriented problem-solving environment for early diagenesis. Comput Geosci 29:301–318. doi: 10.1016/S0098-3004(03)00007-4 CrossRefGoogle Scholar
  51. Meysman FJR, Boudreau BP, Middelburg JJ (2005) Modeling reactive transport in sediments subject to bioturbation and compaction. Geochim Cosmochim Acta 69:3601–3617. doi: 10.1016/j.gca.2005.01.004 CrossRefGoogle Scholar
  52. Meysman FJR, Galaktionov OS, Gribsholt B, Middelburg JJ (2006a) Bio-irrigation in permeable sediments: an assessment of model complexity. J Mar Res 64:589–627. doi: 10.1357/002224006778715757 CrossRefGoogle Scholar
  53. Meysman FJR, Middelburg JJ, Heip CHR (2006b) Bioturbation: a fresh look at Darwin’s last idea. Trends Ecol Evol 21:688–695. doi: 10.1016/j.tree.2006.08.002 CrossRefGoogle Scholar
  54. Meysman FJR, Boudreau BP, Middelburg JJ (2010) When and why does bioturbation lead to diffusive mixing? J Mar Res 68:881–920CrossRefGoogle Scholar
  55. Meysman FJR, Risgaard-Petersen N, Malkin SY, Nielsen LP (2015) The geochemical fingerprint of microbial long-distance electron transport in the seafloor. Geochim Cosmochim Acta 152:122–142. doi: 10.1016/j.gca.2014.12.014 CrossRefGoogle Scholar
  56. Middelburg JJ, Levin LA (2009) Coastal hypoxia and sediment biogeochemistry. Biogeosciences 6:1273–1293CrossRefGoogle Scholar
  57. Millero FJ, Hubinger S, Fernandez M, Garnett S (1987a) Oxidation of H2S in Seawater as a function of temperature, pH, and ionic strength. Environ Sci Technol 21:439–443. doi: 10.1021/es00159a003 CrossRefGoogle Scholar
  58. Millero FJ, Sotolongo S, Izaguirre M (1987b) The oxidation kinetics of Fe(II) in seawater. Geochim Cosmochim Acta 51:793–801. doi: 10.1016/0016-7037(87)90093-7 CrossRefGoogle Scholar
  59. Mouret A, Anschutz P, Lecroart P et al (2009) Benthic geochemistry of manganese in the Bay of Biscay, and sediment mass accumulation rate. Geo Mar Lett 29:133–149. doi: 10.1007/s00367-008-0130-6 CrossRefGoogle Scholar
  60. Nielsen LP, Risgaard-Petersen N, Fossing H et al (2010) Electric currents couple spatially separated biogeochemical processes in marine sediment. Nature 463:1071–1074. doi: 10.1038/nature08790 CrossRefGoogle Scholar
  61. Pfeffer C, Larsen S, Song J et al (2012) Filamentous bacteria transport electrons over centimetre distances. Nature 491:218–221. doi: 10.1038/nature11586 CrossRefGoogle Scholar
  62. Postma D, Jakobsen R (1996) Redox zonation: equilibrium constraints on the Fe(III)/SO4-reduction interface. Geochim Cosmochim Acta 60:3169–3175. doi: 10.1016/0016-7037(96)00156-1 CrossRefGoogle Scholar
  63. Poulton SW, Canfield DE (2005) Development of a sequential extraction procedure for iron: implications for iron partitioning in continentally derived particulates. Chem Geol 214:209–221. doi: 10.1016/j.chemgeo.2004.09.003 CrossRefGoogle Scholar
  64. Poulton SW, Fralick PW, Canfield DE (2004a) The transition to a sulphidic ocean ~1.84 billion years ago. Nature 431:173–177. doi: 10.1038/nature02863.1 CrossRefGoogle Scholar
  65. Poulton SW, Krom MD, Raiswell R (2004b) A revised scheme for the reactivity of iron (oxyhydr)oxide minerals towards dissolved sulfide. Geochim Cosmochim Acta 68:3703–3715. doi: 10.1016/j.gca.2004.03.012 CrossRefGoogle Scholar
  66. Raiswell R, Canfield DE (2012) The iron biogeochemical cycle past and present. Geochem Perspect 1:1–232CrossRefGoogle Scholar
  67. Reed DC, Gustafsson BG, Slomp CP (2015) Shelf-to-basin iron shuttling enhances vivianite formation in deep Baltic Sea sediments. Earth Planet Sci Lett 1:1–11. doi: 10.1016/j.epsl.2015.11.033 Google Scholar
  68. Reimers CE, Suess E (1983) The partitioning of organic carbon fluxes and sedimentary organic matter decomposition rates in the ocean. Mar Chem 13:141–168CrossRefGoogle Scholar
  69. Renz JR, Forster S (2014) Effects of bioirrigation by the three sibling species of Marenzelleria spp. on solute fluxes and porewater nutrient profiles. Mar Ecol Prog Ser 505:145–159. doi: 10.3354/meps10756 CrossRefGoogle Scholar
  70. Rickard D (1995) Kinetics of FeS precipitation: part 1. Competing reaction mechanisms. Geochim Cosmochim Acta 59:4367–4379. doi: 10.1016/0016-7037(95)00251-T CrossRefGoogle Scholar
  71. Rickard D (2006) The solubility of FeS. Geochim Cosmochim Acta 70:5779–5789CrossRefGoogle Scholar
  72. Rickard D, Luther GW (2007) Chemistry of Iron Sulfides. Chem Rev 107(2):514–562. doi: 10.1021/cr0503658 CrossRefGoogle Scholar
  73. Risgaard-Petersen N, Revil A, Meister P, Nielsen LP (2012) Sulfur, iron-, and calcium cycling associated with natural electric currents running through marine sediment. Geochim Cosmochim Acta 92:1–13. doi: 10.1016/j.gca.2012.05.036 CrossRefGoogle Scholar
  74. Sayama M, Risgaard-petersen N, Nielsen LP et al (2005) Impact of bacterial NO3—transport on sediment biogeochemistry. Appl Environ Microbiol 71:7575–7577. doi: 10.1128/AEM.71.11.7575 CrossRefGoogle Scholar
  75. Schippers A, Jørgensen BB (2002) Biogeochemistry of pyrite and iron sulfide oxidation in marine sediments. Geochim Cosmochim Acta 66:85–92. doi: 10.1016/S0016-7037(01)00745-1 CrossRefGoogle Scholar
  76. Scholz F, Severmann S, Mcmanus J, Hensen C (2014) Beyond the Black Sea paradigm: the sedimentary fingerprint of an open-marine iron shuttle. Geochim Cosmochim Acta 127:368–380. doi: 10.1016/j.gca.2013.11.041 CrossRefGoogle Scholar
  77. Schulz HN, Jørgensen BB (2001) Big bacteria. Annu Rev Microbiol 55:105–137CrossRefGoogle Scholar
  78. Seitaj D, Schauer R, Sulu-gambari F et al (2015) Cable bacteria generate a firewall against euxinia in seasonally hypoxic basins. Proc Natl Acad Sci 112:13278–13283. doi: 10.1073/pnas.1510152112 CrossRefGoogle Scholar
  79. Soetaert K, Meysman F (2012) Reactive transport in aquatic ecosystems: rapid model prototyping in the open source software R. Environ Model Softw 32:49–60. doi: 10.1016/j.envsoft.2011.08.011 CrossRefGoogle Scholar
  80. Soetaert K, Herman PMJ, Middelburg JJ (1996) A model of early diagenetic processes from the shelf To abyssal depths. Geochim Cosmochim Acta 60:1019–1040CrossRefGoogle Scholar
  81. Soetaert K, Petzoldt T, Meysman FJR (2010a) marelac: Tools for Aquatic Sciences R package version 2.1Google Scholar
  82. Soetaert K, Petzoldt T, Setzer RW (2010b) Package deSolve: solving initial value differential equations in R. J Stat Softw 33:1–25Google Scholar
  83. Sperling EA, Halverson GP, Knoll AH et al (2013) A basin redox transect at the dawn of animal life. Earth Planet Sci Lett 371–372:143–155. doi: 10.1016/j.epsl.2013.04.003 CrossRefGoogle Scholar
  84. Taylor AM, Goldring R (1993) Description and analysis of bioturbation and ichnofabric. J Geol Soc London 150:141–148CrossRefGoogle Scholar
  85. Thamdrup B (2000) Bacterial manganese and iron reduction in aquatic sediments. In: Schink B (ed) Advances in microbial ecology, 16th edn. Luwer Academic/Plenum Publishers, New York, pp 41–84CrossRefGoogle Scholar
  86. Thamdrup B, Fossing H, Jorgensen BB (1994) Manganese, iron, and sulfur cycling in a coastal marine sediment, Aarhus Bay, Denmark. Geochim Cosmochim Acta 58:5115–5129CrossRefGoogle Scholar
  87. Turchyn AV, Schrag DP (2004) Oxygen isotope constraints on the sulfur cycle over the past 10 million years. Science 303:2004–2007. doi: 10.1126/science.1092296 CrossRefGoogle Scholar
  88. Van Cappellen P, Wang Y (1996) Cycling of iron and manganese in surface sediments: a general theory for the coupled transport and reaction of carbon, oxygen, nitrogen, sulfur, iron, and manganese. Am J Sci 296:197–243CrossRefGoogle Scholar
  89. Volkenborn N, Polerecky L, Wethey DS, Woodin SA (2010) Oscillatory porewater bioadvection in marine sediments induced by hydraulic activities of Arenicola marina. Limnol Oceanogr 55:1231–1247. doi: 10.4319/lo.2010.55.3.1231 CrossRefGoogle Scholar
  90. Westrich JT, Berner RA (1984) The role of sedimentary organic matter in bacterial sulfate reduction: the G model tested. Limnol Oceanogr 29:236–249. doi: 10.4319/lo.1984.29.2.0236 CrossRefGoogle Scholar
  91. Wijsman JWM, Middelburg JJ, Heip CHR (2001) Reactive iron in Black Sea Sediments: implications for iron recycling. Mar Geol 172:167–180. doi: 10.1016/S0025-3227(00)00122-5 CrossRefGoogle Scholar
  92. van de Velde S, Lesven L, Burdorf LDW et al. The impact of electrogenic sulfur oxidation on the biogeochemistry of coastal sediments: a field study. (accepted)Google Scholar
  93. Zobell C, Rittenberg S (1948) Sulfate-reducing bacteria in marine sediments. J Mar Res 7:602–617Google Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Sebastiaan van de Velde
    • 1
    Email author
  • Filip J. R. Meysman
    • 1
    • 2
  1. 1.Department of Analytical, Environmental and Geo-ChemistryVrije Universiteit Brussel (VUB)BrusselsBelgium
  2. 2.Department of Ecosystem StudiesThe Royal Netherlands Institute of Sea Research (NIOZ)YersekeThe Netherlands

Personalised recommendations