Abstract
Oxygen fluxes across the sediment–water interface reflect primary production and organic matter degradation in coastal sediments and thus provide data that can be used for assessing ecosystem function, carbon cycling and the response to coastal eutrophication. In this study, the aquatic eddy covariance technique was used to measure seafloor–water column oxygen fluxes at shallow coastal sites with highly permeable sandy sediment in the northeastern Gulf of Mexico for which oxygen flux data currently are lacking. Oxygen fluxes at wave-exposed Gulf sites were compared to those at protected Bay sites over a period of 4 years and covering the four seasons. A total of 17 daytime and 14 nighttime deployments, producing 408 flux measurements (14.5 min each), were conducted. Average annual oxygen release and uptake (mean ± standard error) were 191 ± 66 and −191 ± 45 mmol m−2 day−1 for the Gulf sites and 130 ± 57 and −152 ± 64 mmol m−2 day−1 for the Bay sites. Seasonal variation in oxygen flux was observed, with high rates typically occurring during spring and lower rates during summer. The ratio of average oxygen release to uptake at both sites was close to 1 (Bay: 0.9, Gulf: 1.0). Close responses of the flux to changes in light, temperature, bottom current velocity, and wave action (significant wave height) documented tight physical–biological, benthic–pelagic coupling. The increase of the sedimentary oxygen uptake with increasing temperature corresponded to a Q10 temperature coefficient of 1.4 ± 0.3. An increase in flow velocity resulted in increased oxygen uptake (by a factor of 1–6 for a doubling in flow), which is explained by the enhanced transport of organic matter and electron acceptors into the permeable sediment. Benthic photosynthetic production and oxygen release from the sediment was modulated by light intensity at the temporal scale (minutes) of the flux measurements. The fluxes measured in this study contribute to baseline data in a region with rapid coastal development and can be used in large-scale assessments and estimates of carbon transformations.
Similar content being viewed by others
References
Aller RC (1982) The effects of macrobenthos on chemical properties of marine sediment and overlying water. In: McCall PL, Tevesz MJS (eds) Animal-sediment relations. Plenum Press, New York
Asmus RM, Bauerfeind E (1994) The microphytobenthos of konigshafen—spatial and seasonal distribution on a sandy tidal flat. Helgol Meeresunters 48:257–276. doi:10.1007/bf02367040
Attard KM, Glud RN, McGinnis DF, Rysgaard S (2014) Seasonal rates of benthic primary production in a Greenland fjord measured by aquatic eddy correlation. Limnol Oceanogr 59:1555–1569
Attard KM, Stahl H, Kamenos NA, Turner G, Burdett HL, Glud RN (2015) Benthic oxygen exchange in a live coralline algal bed and an adjacent sandy habitat: an eddy covariance study. Mar Ecol Prog Ser 535:99–115
Berg P, Huettel M (2008) Monitoring the seafloor using the noninvasive eddy correlation technique: integrated benthic exchange dynamics. Oceanography 21:164–167
Berg P, Roy H, Janssen F, Meyer V, Jorgensen BB, Huettel M, de Beer D (2003) Oxygen uptake by aquatic sediments measured with a novel non-invasive eddy-correlation technique. Mar Ecol Prog Ser 261:75–83
Berg P, Glud RN, Hume A, Stahl H, Oguri K, Meyer V, Kitazato H (2009) Eddy correlation measurements of oxygen uptake in deep ocean sediments. Limnol Oceanogr Methods 7:576–584. doi:10.4319/lom.2009.7.576
Berg P et al (2013) Eddy correlation measurements of oxygen fluxes in permeable sediments exposed to varying current flow and light. Limnol Oceanogr 58:1329–1343. doi:10.4319/lo.2013.58.4.1329
Berg P, Reimers CE, Rosman JE, Huettel M, Delgard ML, Reidenbach MA, Özkan-Haller HT (2015) Technical note: time lag correction of aquatic eddy covariance data measured in presence of waves. Biogeosciences 12:6721–6735. doi:10.5194/bg-12-6721-2015
Berg P, Koopmans DJ, Huettel M, Li H, Mori K, Wüest A (2016) A new robust oxygen–temperature sensor for aquatic eddy covariance measurements. Limnol Oceanogr Methods 14:151–167. doi:10.1002/lom3.10071
Blanchard GF, Guarini JM, Gros P, Richard P (1997) Seasonal effect on the relationship between the photosynthetic capacity of intertidal microphytobenthos and temperature. J Phycol 33:723–728. doi:10.1111/j.0022-3646.1997.00723.x
Boudreau BP et al (2001) Permeable marine sediments: overturning an old paradigm. EOS Trans Am Geophys Union 82:133–136
Businger JA (1986) Evaluation of the accuracy with which dry deposition can be measured with current micrometeorological techniques. J Clim Appl Meteorol 25:1100–1124
Cahoon LB (1999) The role of benthic microalgae in neritic ecosystems. Oceanogr Mar Biol 37:47–86
Cahoon LB, Cooke JE (1992) Benthic microalgal production in Onslow Bay, North Carolina, USA. Mar Ecol Prog Ser 84:185–196
Canfield DE, Jørgensen BB, Fossing H, Glud R, Gundersen J et al (1993) Pathways of organic carbon oxidation in three continental margin sediments. Mar Geol 113:27–40
Carpenter R, Williams S (2007) Mass transfer limitation of photosynthesis of coral reef algal turfs. Mar Biol 151:435–450
Chipman L, Podgorski D, Green S, Kostka J, Cooper W, Huettel M (2010) Decomposition of plankton-derived dissolved organic matter in permeable coastal sediments. Limnol Oceanogr 55:857–871
Chipman L, Huettel M, Berg P, Meyer V, Klimant I, Glud RN, Wenzhoefer F (2012) Oxygen optodes as fast sensors for eddy correlation measurements in aquatic systems. Limnol Oceanogr Methods 10:304–316
Cook PLM, Røy H (2006) Advective relief of CO2 limitation in highly productive sandy sediments. Limnol Oceanogr 51:1594–1601
Cook PLM, Wenzhöfer F, Glud RN, Janssen F, Huettel M (2007) Benthic solute exchange and carbon mineralization in two shallow subtidal sandy sediments: effect of advective pore-water exchange. Limnol Oceanogr 52:1943–1963
D’Andrea AF, Aller RC, Lopez GR (2002) Organic matter flux and reactivity on a South Carolina sandflat: the impacts of porewater advection and macrobiological structures. Limnol Oceanogr 47:1056–1070
de Beer D, Wenzhöefer F, Ferdelman TG, Boehme SE, Huettel M et al (2005) Transport and mineralization rates in North Sea intertidal sediments, Sylt-Rømø Basin, Wadden Sea. Limnol Oceanogr 50(1):113–127
Dean RG, Dalrymple RA (1991) Water wave mechanics for engineers and scientists. Advanced series on ocean engineering 2. World Scientific, Singapore
Donis D et al (2015) An assessment of the precision and confidence of aquatic eddy correlation measurements. J Atmos Ocean Technol 32:642–655. doi:10.1175/JTECH-D-14-00089.1
Donis D, McGinnis DF, Holtappels M, Felden J, Wenzhöefer F (2016) Assessing benthic oxygen fluxes in oligotrophic deep sea sediments (HAUSGARTEN observatory). Deep-Sea Res Part I Oceanogr Res Pap 111:1–10
Forster S, Huettel M, Ziebis W (1996) Impact of boundary layer flow velocity on oxygen utilisation in coastal sediments. Mar Ecol Prog Ser 146:173–185
Forster S, Glud RN, Gundersen JK, Huettel M (1999) In situ study of bromide tracer and oxygen flux in coastal sediments. Estuar Coast Shelf Sci 49:813–827
Gattuso JP, Gentili B, Duarte CM, Kleypas JA, Middelburg JJ, Antoine D (2006) Light availability in the coastal ocean: impact on the distribution of benthic photosynthetic organisms and their contribution to primary production. Biogeosciences 3:489–513
Glud RN (2008) Oxygen dynamics of marine sediments. Mar Biol Res 4:243–289
Glud RN, Berg P, Hume A, Batty P, Blicher ME, Lennert K, Rysgaard S (2010) Benthic O2 exchange rates across hard-bottom substrates quantified by eddy correlation in a sub-Arctic fjord system. Mar Ecol Prog Ser 417:1–12
Grant J (1986) Sensitivity of benthic community respiration and primary production to changes in temperature and light. Mar Biol 90:299–306
Grasshoff K, Kremling K, Ehrhardt M (1999) Methods of seawater analysis, 3rd edn. Wiley-VCH, Weinheim
Gundersen JK, Ramsing NB, Glud RN (1998) Predicting the signal of O-2 microsensors from physical dimensions, temperature, salinity, and O-2 concentration. Limnol Oceanogr 43:1932–1937
Hallas MK, Huettel M (2013) Bar-built estuary as a buffer for riverine silicate discharge to the coastal ocean. Cont Shelf Res 55:76–85. doi:10.1016/j.csr.2013.01.011
Hancke K, Glud RN (2004) Temperature effects on respiration and photosynthesis in three diatom-dominated benthic communities. Aquat Microb Ecol 37:265–281
Hargrave BT, Prouse NJ, Phillips GA, Neame PA (1983) primary production and respiration in pelagic and benthic communities at 2 intertidal sites in the upper bay of fundy. Can J Fish Aquat Sci 40:229–243
He RY, Weisberg AH (2002) Tides on the West Florida shelf. J Phys Oceanogr 32:3455–3473
Holtappels M, Glud RN, Donis D, Liu B, Hume A, Wenzhöfer F, Kuypers M (2013) Effects of transient bottom water currents and oxygen concentrations on benthic exchange rates as assessed by eddy correlation measurements. J Geophys Res Oceans 118:1157–1169. doi:10.1002/jgrc.20112
Holtappels M, Noss Hancke K, Cathalot C, McGinnis DF, Lorke A, Glud RN (2015) Aquatic eddy correlation: quantifying the artificial flux caused by stirring-sensitive O2 sensors. PLoS ONE 10:e0116564. doi:10.1371/journal.pone.0116564
Huang WR, Spaulding M (2002) Modelling residence-time response to freshwater input in Apalachicola Bay, Florida, USA. Hydrol Process 16:3051–3064
Huettel M, Gust G (1992) Impact of bioroughness on interfacial solute exchange in permeable sediments. Mar Ecol Prog Ser 89:253–267
Huettel M, Rusch A (2000) Transport and degradation of phytoplankton in permeable sediment. Limnol Oceanogr 45:534–549
Huettel M, Webster IT (2000) Porewater flow in permeable sediment. In: Boudreau BP, Jørgensen BB (eds) The benthic boundary layer: transport processes and biogeochemistry. Oxford University Press, Oxford, pp 144–179
Huettel M, Ziebis W, Forster S, Luther GW (1998) Advective transport affecting metal and nutrient distributions and interfacial fluxes in permeable sediments. Geochim Cosmochim Acta 62:613–631
Huettel M, Røy H, Precht E, Ehrenhauss S (2003) Hydrodynamical impact on biogeochemical processes in aquatic sediments. Hydrobiologia 494:231–236
Huettel M, Berg P, Kostka JE (2014) Benthic exchange and biogeochemical cycling in permeable sediments. Annu Rev Mar Sci 6(6):23–51. doi:10.1146/annurev-marine-051413-012706
Hume AC, Berg P, McGlathery KJ (2011) Dissolved oxygen fluxes and ecosystem metabolism in an eelgrass (Zostera marina) meadow measured with the eddy correlation technique. Limnol Oceanogr 56:86–96. doi:10.4319/lo.2011.56.1.0086
Jahnke RA, Marinelli RL, Eckmann JE, Nelson JR (1996) Pore water nutrient distributions in non-accumulating, sandy sediments of the South Atlantic Bight continental shelf. EOS 76:202
Jahnke RA, Nelson JR, Marinelli RL, Eckman JE (2000) Benthic flux of biogenic elements on the Southeastern US continental shelf: influence of pore water advective transport and benthic microalgae. Cont Shelf Res 20:109–127
Jahnke R, Richards M, Nelson J, Robertson C, Rao A, Jahnke D (2005) Organic matter remineralization and porewater exchange rates in permeable South Atlantic Bight continental shelf sediments. Cont Shelf Res 25:1433–1452. doi:10.1016/j.csr.2005.04.002
Jahnke RA, Nelson JR, Richards ME, Robertson CY, Rao AMF, Jahnke DB (2008) Benthic primary productivity on the Georgia midcontinental shelf: benthic flux measurements and high-resolution, continuous in situ PAR records. J Geophys Res 113:C08022. doi:10.1029/2008JC004745
Janssen F, Huettel M, Witte U (2005) Pore-water advection and solute fluxes in permeable marine sediments (II): benthic respiration at three sandy sites with different permeabilities (German Bight, North Sea). Limnol Oceanogr 50:779–792
Jasby AD, Platt T (1976) Mathematical formulation of the relationship between photosynthesis and light for phytoplankton. Limnol Oceanogr 21:540–547
Krause-Jensen D, Markager S, Dalsgaard T (2012) Benthic and pelagic primary production in different nutrient regimes. Estuar Coasts 35:527–545. doi:10.1007/s12237-011-9443-1
Kristensen E, Aller RC, Aller JY (1991) Oxic and anoxic decomposition of tubes from the burrowing sea anemone Ceriantheopsis americanus—implications for bulk sediment carbon and nitrogen balance. J Mar Res 49:589–617
Kristensen E, Jensen MH, Jensen KM (1997) Temporal variations in microbenthic metabolism and inorganic nitrogen fluxes in sandy and muddy sediments of a tidally dominated bay in the northern Wadden Sea. Helgol Meeresunters 51:295–320. doi:10.1007/bf02908717
Kuwae T, Kamio K, Inoue T, Miyoshi E, Uchiyama Y (2006) Oxygen exchange flux between sediment and water in an intertidal sandflat, measured in situ by the eddy-correlation method. Mar Ecol Prog Ser 307:59–68
Lee X, Massman W, Law B (2004) Handbook of micro-meteorology: a guide for surface flux measurement and analysis. Kluwer Academic Publishers, Dordrecht
Long MH, Berg P, de Beer D, Zieman JC (2013) In situ coral reef oxygen metabolism: an eddy correlation study. PLoS ONE. doi:10.1371/journal.pone.0058581
Long MH, Berg P, McGlathery K, Zieman JC (2015) Sub-tropical seagrass ecosystem metabolism measured by eddy covariance. Mar Ecol Prog Ser 529:75–90. doi:10.3354/meps11314
Lorke A, McGinnis DF, Maeck A (2013) Eddy-correlation measurements of benthic fluxes under complex flow conditions: effects of coordinate transformations and averaging time scales. Limnol Oceanogr Methods 11:425–437. doi:10.4319/lom.2013.11.425
Lorrai C, McGinnis DF, Brand A, Wüest A (2010) Application of oxygen eddy correlation in aquatic systems. J Atmos Ocean Technol 27:1533–1546. doi:10.1175/2010JTECHO723.1
Macintyre HL, Geider RJ, Miller DC (1996) Microphytobenthos: the ecological role of the “secret garden” of unvegetated, shallow-water marine habitats. 1. Distribution, abundance and primary production. Estuaries 19:186–201
Mass T, Genin A, Shavit U, Grinstein M, Tchernov D (2010) Flow enhances photosynthesis in marine benthic autotrophs by increasing the efflux of oxygen from the organism to the water. PNAS 107(6):2527–2531
McCann-Grosvenor K, Reimers CE, Sanders RD (2014) Dynamics of the benthic boundary layer and seafloor contributions to oxygen depletion on the Oregon inner shelf. Cont Shelf Res 84:93–106. doi:10.1016/j.csr.2014.05.010
McGinnis DF, Berg P, Brand A, Lorrai C, Edmonds TJ, Wuest A (2008) Measurements of eddy correlation oxygen fluxes in shallow freshwaters: towards routine applications and analysis. Geophys Res Lett. doi:10.1029/2007gl032747
McGinnis DF, Sommer S, Lorke A, Glud RN, Linke P (2014) Quantifying tidally driven benthic oxygen exchange across permeable sediments: an aquatic eddy correlation study. J Geophys Res 119:6918–6932
Mermillod-Blondin F, Francois-Carcaillet F, Rosenberg R (2005) Biodiversity of benthic invertebrates and organic matter processing in shallow marine sediments: an experimental study. J Exp Mar Biol Ecol 315:187–209
Meyercordt J, Gerbersdorf S, Meyer-Reil LA (1999) Significance of pelagic and benthic primary production in two shallow coastal lagoons of different degrees of eutrophication in the southern Baltic Sea. Aquat Microb Ecol 20:273–284. doi:10.3354/ame020273
Morey SL, Dukhovskoy DS, Bourassa MA (2009) Connectivity of the Apalachicola River flow variability and the physical and bio-optical oceanic properties of the northern West Florida Shelf. Cont Shelf Res 29:1264–1275. doi:10.1016/j.csr.2009.02.003
Mortazavi B, Iverson RL, Huang WR, Lewis FG, Caffrey JM (2000a) Nitrogen budget of Apalachicola Bay, a bar-built estuary in the northeastern Gulf of Mexico. Mar Ecol Prog Ser 195:1–14
Mortazavi B, Iverson RL, Landing WM, Huang WR (2000b) Phosphorus budget of Apalachicola Bay: a river-dominated estuary in the northeastern Gulf of Mexico. Mar Ecol Prog Ser 198:33–42
Precht E, Franke U, Polerecky L, Huettel M (2004) Oxygen dynamics in permeable sediments with wave-driven pore water exchange. Limnol Oceanogr 49:693–705. doi:10.4319/lo.2004.49.3.0693
Reimers CE, Özkan-Haller T, Berg P, Devol A, McCann-Grosvenor K, Sanders RD (2012) Benthic oxygen consumption rates during hypoxic conditions on the Oregon continental shelf: evaluation of the eddy correlation method. J Geophys Res 117:1–18. doi:10.1029/2011JC007564
Reimers CE, Ozkan-Haller T, Albright A, Berg P (2016) Microelectrode velocity effects and aquatic eddy covariance measurements under waves. J Atmos Ocean Technol 33:263–282
Revsbech NP (1989) An oxygen microsensor with a guard cathode. Limnol Oceanogr 34:474–478
Rheuban JE, Berg P, McGlathery KJ (2014a) Ecosystem metabolism along a colonization gradient of eelgrass (Zostera marina) measured by eddy correlation. Limnol Oceanogr 59:1376–1387. doi:10.4319/lo.2014.59.4.1376
Rheuban JE, Berg P, McGlathery KJ (2014b) Multiple timescale processes drive ecosystem metabolism in eelgrass (Zostera marina) meadows. Mar Ecol Prog Ser 507:1–13. doi:10.3354/meps10843
Riedl R, Huang N, Machan R (1972) The subtidal pump: a mechanism of interstitial water exchange by wave action. Mar Biol 13:210–221
Rusch A, Huettel M, Wild C, Reimers CE (2006) Benthic oxygen consumption and organic matter turnover in organic-poor, permeable shelf sands. Aquat Geochem 12:1–19
Santema M, Clarke AJ, Speer K, Huettel M (2015) Water column oxygen dynamics within the coastal gradient in the northeastern Gulf of Mexico inner shelf. Cont Shelf Res 104:104–119. doi:10.1016/j.csr.2015.05.006
Santos IR, Glud RN, Maher D, Erler D, Eyre BD (2011) Diel coral reef acidification driven by porewater advection in permeable carbonate sands, Heron Island, Great Barrier Reef. Geophys Res Lett 38:L03604
Snyder RA et al (2014a) Polycyclic aromatic hydrocarbon concentrations across the Florida Panhandle continental shelf and slope after the BP MC 252 well failure. Mar Pollut Bull 89:201–208. doi:10.1016/j.marpolbul.2014.09.057
Snyder RA, Vestal A, Welch C, Barnes G, Pelot R, Ederington-Hagy M, Hileman F (2014b) PAH concentrations in Coquina (Donax spp.) on a sandy beach shoreline impacted by a marine oil spill. Mar Pollut Bull 83:87–91. doi:10.1016/j.marpolbul.2014.04.016
Thamdrup B, Hansen JW, Jorgensen BB (1998) Temperature dependence of aerobic respiration in a coastal sediment. FEMS Microbiol Ecol 25:189–200. doi:10.1016/s0168-6496(97)00095-0
Wenzhofer F, Glud RN (2004) Small-scale spatial and temporal variability in coastal benthic O-2 dynamics: effects of fauna activity. Limnol Oceanogr 49:1471–1481
Westrich JT, Berner RA (1984) The role of sedimentary organic matter in bacterial sulfate reduction: the G model tested. Limnol Oceanogr 29:236–249
Wild C, Rasheed M, Jantzen C, Cook P, Struck U, Huettel M, Boetius A (2005) Benthic metabolism and degradation of natural particulate organic matter in carbonate and silicate reef sands of the northern Red Sea. Mar Ecol Prog Ser 298:69–78
Wild C, Naumann MS, Haas A, Struck U, Mayer FW, Rasheed MY, Huettel M (2009) Coral sand O-2 uptake and pelagic-benthic coupling in a subtropical fringing reef, Aqaba, Red Sea. Aquatic Biology 6:133–142
Wolfstein K, Stal LJ (2002) Production of extracellular polymeric substances (EPS) by benthic diatoms: effect of irradiance and temperature. Mar Ecol Prog Ser 236:13–22
Zavala-Hidalgo J, Romero-Centeno R, Mateos-Jasso A, Morey SL, Martinez-Lopez B (2014) The response of the Gulf of Mexico to wind and heat flux forcing: what has been learned in recent years? Atmosfera 27:317–334
Ziebis W, Forster S, Huettel M, Jorgensen BB (1996a) Complex burrows of the mud shrimp Callianassa truncata and their geochemical impact in the sea bed (vol 382, pg 619, 1996). Nature 383:457
Ziebis W, Huettel M, Forster S (1996b) Impact of biogenic sediment topography on oxygen fluxes in permeable seabeds. Mar Ecol Prog Ser 140:227–237
Acknowledgments
We thank Pascal Brignole, Natalie Geyer, Chiu Cheng, Andrew Hume, John Kaba, Matt Long, Cedric Magen, Lee Russell, Mike Santema, and Brian Wells for help with the fieldwork and laboratory analyses. We also would like to thank all the volunteers that helped with instrument deployments and sample collection. This research was supported by funding from NSF Projects OCE-424967, OCE-536431, OCE-0758446, OCE-1061110 and OCE-1334117.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chipman, L., Berg, P. & Huettel, M. Benthic Oxygen Fluxes Measured by Eddy Covariance in Permeable Gulf of Mexico Shallow-Water Sands. Aquat Geochem 22, 529–554 (2016). https://doi.org/10.1007/s10498-016-9305-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10498-016-9305-3