Spatially variable bioturbation and physical mixing drive the sedimentary biogeochemical seascape in the Louisiana continental shelf hypoxic zone

  • Richard DevereuxEmail author
  • John C. Lehrter
  • Giancarlo Cicchetti
  • David L. BeddickJr.
  • Diane F. Yates
  • Brandon M. Jarvis
  • Jessica Aukamp
  • Marilynn D. Hoglund


Seasonal hypoxia on the Louisiana continental shelf (LCS) has grown to over 22,000 km2 with limited information available on how low oxygen effects the benthos. Benthic macrofaunal colonization and sediment biogeochemical parameters were characterized at twelve stations in waters 10–50 m deep along four transects spanning 320 km across the LCS hypoxic zone in the early fall of 2010 when bottom waters typically return to oxic conditions. Chemical data and sediment profile imaging (SPI) support three primary mechanistic pathways of organic matter degradation on the LCS: (i) metal oxide cycling in depositional muds, (ii) infauna-driven bioturbation delivering oxygen below the sediment–water interface, and (iii) sulfate reduction in sediments where iron oxide availability is limited. The transect nearest the Mississippi River delta had the highest concentrations of porewater and solid phase Mn and Fe with SPI images of recently deposited reddish, mixed muddy sediments suggestive of metal cycling. The deepest stations had high oxidized iron concentrations and rust colored sediments with faunal colonization that suggests sediments are oxidized via bioturbation. Many nearshore and central LCS stations had more black sediments, more disturbed clay layers, lower amounts of oxidized iron, and higher sulfate reduction rates than the deepest stations. Sediment mixing coefficients, DB, determined from chlorophyll-a concentration profiles varied between 33 and 183 cm−2 year−1. DB values were highest at the deepest stations where sediments were colonized. DB were not determined at two nearshore stations where chlorophyll-a concentrations were highly variable in surficial sediments, and on the eastern shelf where sedimentation is high. This study provides a regional view of benthic faunal colonization and sediment biogeochemistry on the LCS, describes regions with potentially different pathways of organic matter degradation, and demonstrates the importance of both bioturbation and physical mixing in processing the large amounts of organic matter in river-dominated continental shelf systems.


Marine sediments Bioturbation Sediment profile imaging Infauna Gulf of Mexico Hypoxia River outflow sediments Continental shelf biogeochemistry Sulfate reduction Sediment iron cycling 



We thank Jeanne Scott, Leah Oliver, and Jan Kurtz for their help with processing samples during the cruise, and the officers and crew of the now decommissioned USEPA OSV Bold for their excellent seamanship and technical assistance. J.C. Lehrter acknowledges partial support from NSF-OE-1760747. This paper is dedicated to the memories of USEPA scientists Diane F. Yates and George Craven in recognition of their many contributions to research at the Gulf Ecology Division. The excellent comments from three anonymous reviewers are greatly appreciated. The views expressed in this paper are those of the authors and do not necessarily reflect the views or policies of the U.S. Environmental Protection Agency.

Supplementary material

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  1. Aller RC (1994) Bioturbaton and remineralization of sedimentary organic matter: effects of redox oscillation. Chem Geol 114:331–345CrossRefGoogle Scholar
  2. Aller RC (1998) Mobile deltaic and continental shelf muds as suboxic, fluidized bed reactors. Mar Chem 61:143–155CrossRefGoogle Scholar
  3. Aller RC, Blair NE (2006) Carbon remineralization in the Amazon-Guianas tropical mobile mudbelt: a sedimentary incinerator. Cont Shelf Res 26:2241–2259CrossRefGoogle Scholar
  4. Aller RC, Madrid V, Chistoserdov A, Aller JY, Heilbrun C (2010) Unsteady diagenetic processes and sulfur biogeochemistry in tropical deltaic muds: implications for oceanic isotope cycles and the sedimentary record. Geochim Cosmochim Acta 74:4671–4692CrossRefGoogle Scholar
  5. Allison MA, Kineke GC, Gordon ES, Goñi MA (2000) Development and reworking of a seasonal flood deposit on the inner continental shelf off the Atchafalaya River. Cont Shelf Res 20:2267–2294CrossRefGoogle Scholar
  6. Allison MA, Dellapenna TM, Gordon ES, Mitra S, Petsch ST (2010) Impact of Hurricane Katrina (2005) on shelf organic carbon burial and deltaic evolution. Geophys Res Lett 37:L21605. Google Scholar
  7. Alongi DM, Robertson AI (1995) Factors regulating benthic food chains in tropical river deltas and adjacent shelf areas. Geo-Mar Lett 15:145–152CrossRefGoogle Scholar
  8. Baustian MM, Rabalais NN (2009) Seasonal composition of benthic macroinfauna exposed to hypoxia in the northern Gulf of Mexico. Estuar Coasts 32:975–983CrossRefGoogle Scholar
  9. Beckler JS, Kiriazis N, Rabouille C, Stewart FJ, Taillefert M (2016) Importance of microbial iron reduction in deep sediments of river-dominated continental margins. Mar Chem 178:22–34CrossRefGoogle Scholar
  10. Berner RA (1982) Burial of organic carbon and pyrite sulfur in the modern ocean: its geochemical and environmental significance. Am J Sci 282:451–473CrossRefGoogle Scholar
  11. Bianchi TS, Mitra S, McKee M (2002) Sources of terrestrially-derived carbon in the lower Mississippi River and Louisiana shelf: implications for differential sedimentation and transport at the coastal margin. Mar Chem 77:211–223CrossRefGoogle Scholar
  12. Bianchi TS, DiMarco SF, Cowan JH Jr, Hetland RD, Chapman R, Day JW, Allison MA (2010) The science of hypoxia in the northern Gulf of Mexico: a review. Sci Tot Environ 408:1471–1484CrossRefGoogle Scholar
  13. Briggs KB, Hartmann VA, Yeager KM, Shivarudrappa S, Diaz RJ, Ostermann LE, Reed AH (2015) Influence of hypoxia on biogenic structure in sediments on the Louisiana continental shelf. Estuar Coast Shelf Sci 164:147–160CrossRefGoogle Scholar
  14. Burdige DJ (2006) Geochemistry of marine sediments. Princeton University Press, Princeton New Jersey, p 609Google Scholar
  15. Chen N, Bianchi TS, McKee BA (2005) Early diagenesis of chloropigment biomarkers in the lower Mississippi River and Louisiana shelf: implications for carbon cycling in a river-dominated margin. Mar Chem 93:159–177CrossRefGoogle Scholar
  16. Cicchetti G, Latimer J, Rego S, Nelson W, Bergen B, Coiro L (2006) Relationships between near-bottom dissolved oxygen and sediment profile camera measures. J Mar Syst 62:124–141CrossRefGoogle Scholar
  17. Clarke KR, Gorley RN (2015) PRIMER v7: user manual/tutorial. PRIMER-E, Plymouth, p 296Google Scholar
  18. Clarke KR, Somerfield PJ, Gorley RN (2008) Testing of null hypotheses in exploratory community analyses: similarity profiles and biota-environment linkage. J Exp Mar Biol Ecol 366:56–69CrossRefGoogle Scholar
  19. Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oeanogr 14:454–458CrossRefGoogle Scholar
  20. Cochrane JD, Kelly FJ (1986) Low-frequency circulation on the Texas-Louisiana continental shelf. J Geophys Res 91:10645–10659CrossRefGoogle Scholar
  21. Devereux R, Lehrter JC, Beddick DL Jr, Yates DF, Jarvis BM (2015) Manganese, iron, and sulfur cycling in Louisiana continental shelf sediments. Cont Shelf Res 99:46–56CrossRefGoogle Scholar
  22. Diaz RJ, Rosenberg R (1995) Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. Oceangr Mar Biol Ann Rev 33:245–303Google Scholar
  23. Diaz RJ, Trefy JH (2006) Comparison of sediment profile image data with profiles of oxygen and Eh from sediment cores. J Mar Syst 62:164–172CrossRefGoogle Scholar
  24. FGDC; Federal Geographic Data Committee (2012) Coastal and Marine Ecological Classification Standard (CMECS) version IV. FGDC-STD-018-2012. Accessed 7 Dec 2017
  25. Fossing H, Jørgensen BB (1989) Measurement of bacterial sulfate reduction in sediments: evaluation of a single-step chromium reduction method. Biogeochem 8:205–222CrossRefGoogle Scholar
  26. Germano JD, Rhoads DC, Valente RM, Carey DA, Solan M (2011) The use of sediment profile imaging (SPI) for environmental impact assessments and monitoring studies: lessons learned from the past four decades. Oceanogr Mar Biol 49:235–298Google Scholar
  27. Goñi MA, Gordon ES, Monacci NM, Clinton R, Gisewhite R, Allison MA, Kineke G (2006) The effect of Hurricane Lili on the distribution of organic matter along the inner Louisiana shelf (Gulf of Mexico, USA). Cont Shelf Res 26:2260–2280CrossRefGoogle Scholar
  28. Gordon ES, Goñi MA (2004) Controls on the distribution and accumulation of terrigenous organic matter in sediments from the Mississippi and Atchafalaya river margin. Mar Chem 92:331–352CrossRefGoogle Scholar
  29. Green MA, Aller RC, Cochran JK, Lee C, Aller JY (2002) Bioturbation in shelf/slope sediments off Cape Hatteras, North Carolina: the use of 234Th, Chl-a, and Br to evaluate rates of particle and solute transport. Deep Sea Res Part II 49:4627–4644CrossRefGoogle Scholar
  30. Grizzle RE, Penniman CA (1991) Effects of organic enrichment on estuarine macrofaunal benthos: a comparison of sediment profile imaging and traditional methods. Mar Ecol Progr Ser 74:249–262CrossRefGoogle Scholar
  31. Hall POJ, Aller RC (1992) Rapid, small-volume flow injection analysis for ΣCO2 and NH4 + in marine and fresh waters. Limnol Oceaogr 37:1113–1119CrossRefGoogle Scholar
  32. Hedges JI, Keil R (1995) Sedimentary organic matter preservation; an assessment and speculative synthesis. Mar Chem 49:81–115CrossRefGoogle Scholar
  33. Holm S (1979) A simple sequentially rejective multiple test procedure. Scand J Stat 6:65–70Google Scholar
  34. Hulth S, Aller RC, Canfield DE, Dalsgaard T, Engström P, Gilbert F, Sundbäck Thamdrup B (2005) Nitrogen removal in marine environments: recent findings and future research challenges. Mar Chem 94:125–145CrossRefGoogle Scholar
  35. Hyun J-H, Kim S-H, Mok J-S, Cho H, Lee T, Vandieken V, Thamdrup B (2017) Manganese and iron reduction dominate organic carbon oxidation in surface sediments of the deep Ulleung Basin, East Sea. Biogeosci 14:941–958CrossRefGoogle Scholar
  36. Jensen MM, Thamdrup B, Rysgaard S, Holmer M, Fossing H (2003) Rates and regulation of microbial iron reduction in sediments of the Baltic-North Sea transition. Biogeochem 65:295–317CrossRefGoogle Scholar
  37. Kristensen E (2000) Organic matter diagenesis at the oxic/anoxic interface in coastal marine sediments, with emphasis on the role of burrowing animals. Hydrobiol 426:1–24CrossRefGoogle Scholar
  38. Kristensen E, Blackburn TH (1987) The fate of organic carbon and nitrogen in experimental marine sediment systems: influence of bioturbation and anoxia. J Mar Res 45:231–257CrossRefGoogle Scholar
  39. LDWF; Louisiana Department of Wildlife and Fisheries (2018) Shrimp Season. 7 Dec 2018
  40. Lehrter JC, Beddick DL Jr, Devereux R, Yates DF, Murrell MC (2012) Sediment-water fluxes of dissolved inorganic carbon, O2, nutrients, and N2 from the hypoxic region of the Louisiana continental shelf. Biogeochem 109:233–252CrossRefGoogle Scholar
  41. McKee BA, Aller RC, Allison MA, Bianchi TS, Kineke GC (2004) Transport and transformation of dissolved and particulate materials on continental margins influenced by major rivers: benthic boundary layer and seabed processes. Cont Shelf Res 24:899–926CrossRefGoogle Scholar
  42. Middelburg JJ, Levin LA (2009) Coastal hypoxia and sediment biogeochemistry. Biogeosciences 6:1273–1293CrossRefGoogle Scholar
  43. Morse JW, Lin S (1991) Sulfate reduction and iron sulfide mineral formation in Gulf of Mexico anoxic sediments. Am J Sci 291:55–89CrossRefGoogle Scholar
  44. Morys C, Forster S, Graf G (2016) Variability of bioturbation in various sediment types and on different spatial scales in the southwestern Baltic Sea. Mar Ecol Prog Ser 557:31–49CrossRefGoogle Scholar
  45. National Hurricane Center (2018a) 2010 Atlantic hurricane season. Accessed 14 Dec 2018
  46. National Hurricane Center (2018b) 2009 Atlantic hurricane season. Accessed 14 Dec 2018
  47. Nilsson HC, Rosenberg R (1997) Benthic habitat quality assessment of an oxygen-stressed fjord by surface and sediment profile images. J Mar Syst 11:249–264CrossRefGoogle Scholar
  48. Nilsson HC, Rosenberg R (2000) Succession in marine benthic habitats and fauna in response to oxygen deficiency: analysed by sediment profile imaging and by grab samples. Mar Ecol Progr Ser 197:139–149CrossRefGoogle Scholar
  49. NOAA (2017) Gulf of Mexico ‘dead zone’ is the largest ever measured. National Oceanic and Atmospheric Administration. Accessed 16 April 2018
  50. Pearson TH, Rosenberg R (1978) Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanogr Mar Biol 16:229–311Google Scholar
  51. Rabalais NN, Turner RE, Wiseman WJ Jr (2002) Gulf of Mexico hypoxia, A.K.A. “The Dead Zone”. Ann Rev Ecol Syst 33:235–263CrossRefGoogle Scholar
  52. Raiswell R, Canfield DE, Berner RA (1994) A comparison of iron extraction methods for the determination of degree of pyritisation and the recognition of iron-limited pyrite formation. Chem Geol 111:101–110CrossRefGoogle Scholar
  53. Reese BK, Mills HJ, Dowd SE, Morse JW (2012) Linking molecular microbial ecology to geochemistry on a coastal hypoxic zone. Geomicrobiol J 302:160–172Google Scholar
  54. Rhoads DC, Cande S (1971) Sediment profile camera for in situ study of organism-sediment relations. Limnol Oceanogr 16:110–114CrossRefGoogle Scholar
  55. Rhoads DC, Germano JD (1982) Characterization of organism–sediment relationships using sediment profile imaging: an efficient method of Remote Ecological Monitoring of the Seafloor (REMOTS® System). Mar Ecol Progr Ser 8:115–128CrossRefGoogle Scholar
  56. Rosenberg R, Nilsson HC, Diaz RJ (2001) Response of benthic fauna and changing sediment redox profiles over a hypoxic gradient. Estuar Coast Shelf Sci 53:343–350CrossRefGoogle Scholar
  57. Rossner M, Yamada KM (2004) What’s in a picture? The temptation of image manipulation. J Cell Biol 166:11–15CrossRefGoogle Scholar
  58. Rowe GT, Cruz Kaegi MA, Morse JW, Boland GS, Escobar Briones EG (2002) Sediment community metabolism associated with continental shelf hypoxia, northern Gulf of Mexico. Estuaries 25:1097–1106CrossRefGoogle Scholar
  59. Simone M, Grant J (2017) Visual assessment of redoxcline compared to electron potential in coastal marine sediments. Estuar Coast Shelf Sci 188:156–162CrossRefGoogle Scholar
  60. Statham PJ, Homoky, Parker ER, Klar JK, Silburn B, Poulton SW, Kröger S, Pearce RB, Harris EL (2017) Extending the applications of sediment profile imaging to geochemical interpretations using colour. Cont Shelf Res.
  61. Stookey LL (1970) Ferrozine—a new spectrophotometric reagent for iron. Anal Chem 42:779–781CrossRefGoogle Scholar
  62. Sun M, Aller RC, Lee C (1991) Early diagenesis of chlorophyll-a in Long Island Sound sediments: a measure of carbon flux and particle reworking. J Mar Res 49:379–401CrossRefGoogle Scholar
  63. Teal LR, Parker R, Fones G, Solana M (2009) Simultaneous determination of in situ vertical transitions of color, pore-water metals, and visualization of infaunal activity in marine sediments. Limnol Oceanogr 54:1801–1810CrossRefGoogle Scholar
  64. Thamdrup B, Canfield DE (1996) Pathways of carbon oxidation in continental margin sediments off central Chile. Limnol Oceanogr 41:1629–1650CrossRefGoogle Scholar
  65. Thamdrup B, Dalsgaard T (2000) The fate of ammonium in anoxic manganese oxide-rich marine sediment. Geochim Cosmochim Acta 64:4157–4164CrossRefGoogle Scholar
  66. Thamdrup B, Fossing H, Jørgensen B (1994) Manganese, iron, and sulfur cycling in a coastal marine sediment, Aarhus Bay, Denmark. Geochim Cosmochim Acta 58:5115–5129CrossRefGoogle Scholar
  67. Turner RE, Rabalais NN, Justic D (2012) Predicting summer hypoxia in the northern Gulf of Mexico: redux. Mar Poll Bull 64:319–324CrossRefGoogle Scholar
  68. Valente RM, Evans NC, Whiteside PGD (1996) Environmental monitoring in Hong Kong using the REMOTS seabed camera. Coast Manag Trop Asia 6:26–29Google Scholar
  69. van de Velde S, Meysman FJR (2016) The influence of bioturbation on iron and Sulphur cycling in marine sediments: a model analysis. Aquat Geochem 22:469–504CrossRefGoogle Scholar
  70. Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985–1992CrossRefGoogle Scholar
  71. Wiseman WJ, Rabablais NN, Turner RE, Dinnel SP, Mac-Naughton A (1997) Seasonal and interannual variability within the Louisiana coastal current: stratification and hypoxia. J Mar Syst 12:237–248CrossRefGoogle Scholar
  72. Xu K, Harris CK, Hetland RD, Kaihatu JM (2011) Dispersal of Mississippi and Atchafalaya sediment on the Texas—Louisiana shelf: model estimates for the Year 1993. Cont Shelf Res 31:1558–1575CrossRefGoogle Scholar
  73. Xu K, Corbett DR, Walsh JP, Young D, Briggs KB, Cartwright GM, Friedrichs CT, Harris CK, Mickey RC, Mitra S (2014) Seabed erodibility variations on the Louisiana continental shelf before and after the 2011 Mississippi River flood. Estuar Coast Shelf Sci 149:283–293CrossRefGoogle Scholar

Copyright information

© This is a U.S. government work and not under copyright protection in the U.S.; foreign copyright protection may apply 2019

Authors and Affiliations

  1. 1.National Health and Environmental Effects Research Laboratory, Gulf Ecology DivisionUnited States Environmental Protection AgencyGulf BreezeUSA
  2. 2.Department of Marine SciencesUniversity of South AlabamaDauphin IslandUSA
  3. 3.National Health and Environmental Effects Research Laboratory, Atlantic Ecology DivisionUnited States Environmental Protection AgencyNarragansettUSA

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