, Volume 17, Issue 4, pp 720–737 | Cite as

Variable Importance of Macrofaunal Functional Biodiversity for Biogeochemical Cycling in Temperate Coastal Sediments

  • U. BraeckmanEmail author
  • M. Yazdani Foshtomi
  • D. Van Gansbeke
  • F. Meysman
  • K. Soetaert
  • M. Vincx
  • J. Vanaverbeke


Coastal marine systems are currently subject to a variety of anthropogenic and climate-change-induced pressures. An important challenge is to predict how marine sediment communities and benthic biogeochemical cycling will be affected by these ongoing changes. To this end, it is of paramount importance to first better understand the natural variability in coastal benthic biogeochemical cycling and how this is influenced by local environmental conditions and faunal biodiversity. Here, we studied sedimentary biogeochemical cycling at ten coastal stations in the Southern North Sea on a monthly basis from February to October 2011. We explored the spatio-temporal variability in oxygen consumption, dissolved inorganic nitrogen and alkalinity fluxes, and estimated rates of nitrification and denitrification from a mass budget. In a next step, we statistically modeled their relation with environmental variables and structural and functional macrobenthic community characteristics. Our results show that the cohesive, muddy sediments were poor in functional macrobenthic diversity and displayed intermediate oxygen consumption rates, but the highest ammonium effluxes. These muddy sites also showed an elevated alkalinity release from the sediment, which can be explained by the elevated rate of anaerobic processes taking place. Fine sandy sediments were rich in functional macrobenthic diversity and had the maximum oxygen consumption and estimated denitrification rates. Permeable sediments were also poor in macrobenthic functional diversity and showed the lowest oxygen consumption rates and only small fluxes of ammonium and alkalinity. Macrobenthic functional biodiversity as estimated from bioturbation potential appeared a better variable than macrobenthic density in explaining oxygen consumption, ammonium and alkalinity fluxes, and estimated denitrification. However, this importance of functional biodiversity was manifested particularly in fine sandy sediments, to a lesser account in permeable sediments, but not in muddy sediments. The strong relationship between macrobenthic functional biodiversity and biogeochemical cycling in fine sandy sediments implies that a future loss of macrobenthic functional diversity will have important repercussions for benthic ecosystem functioning.


benthic ecosystem functioning macrobenthos functional biodiversity oxygen consumption nutrient fluxes alkalinity North Sea bioturbation potential 



We are very grateful to the two anonymous reviewers who considerably helped us to improve this manuscript. We are further indepted to the crew of R.V. Zeeleeuw for help with sampling at sea, to Yves Israël for the development of the experimental set-up, to Sofie Jacob, Bart Beuselinck, Niels Viaene, Liesbet Colson, Hannah Marchant, Dr. Gaute Lavik, and Jurian Brasser for help with sample processing and to Heiko Brenner, Sairah Malkin, Alexandra Rao, and attendants of the Wadden Sea Processes Mini-Workshop at Hamburg University for fruitful discussions. Kristof Van Steelandt from FIRE Statistical Consulting is acknowledged for statistical support. U.B. was financially supported by FWO Project No. G.0033.11. Additional funding was provided by the Special Research Fund of Ghent University (BOF-GOA 01GA1911W).

Supplementary material

10021_2014_9755_MOESM1_ESM.docx (1.3 mb)
Supplementary material 1 (DOCX 1292 kb)


  1. Aller R. 1988. Benthic fauna and biogeochemical processes in marine sediments: the role of burrow structures. In: Blackburn TH, Sörensen J, Eds. Nitrogen cycling in coastal marine environments. SCOPE, Vol. 33. Chichester: Wiley, Ltd. p 301–38.Google Scholar
  2. Benton TG, Solan M, Travis JMJ, Sait SM. 2007. Microcosm experiments can inform global ecological problems. Trends Ecol Evol 22:516–21.PubMedCrossRefGoogle Scholar
  3. Berg P, Røy H, Janssen F, Meyer V, Jørgensen B, 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.CrossRefGoogle Scholar
  4. Birchenough SNR, Parker RE, McManus E, Barry J. 2012. Combining bioturbation and redox metrics: potential tools for assessing seabed function. Ecol Indic 12:8–16.CrossRefGoogle Scholar
  5. Blackburn TH. 1988. Benthic mineralization and bacterial production. In: Blackburn TH, Sörensen J, Eds. Nitrogen cycling in coastal marine environments. SCOPE, Vol. 33. Chichester: Wiley, Ltd. p 175–90.Google Scholar
  6. Braeckman U, Provoost P, Gribsholt B, Van Gansbeke D, Middelburg JJ, Soetaert K, Vincx M, Vanaverbeke J. 2010. Role of macrofauna functional traits and density in biogeochemical fluxes and bioturbation. Mar Ecol Prog Ser 399:173–86.CrossRefGoogle Scholar
  7. Bulling MT, Hicks N, Murray L, Paterson DM, Raffaelli D, White PC, Solan M. 2010. Marine biodiversity–ecosystem functions under uncertain environmental futures. Philos Trans R Soc B Biol Sci 365:2107.CrossRefGoogle Scholar
  8. Cardinale BJ, Duffy JE, Gonzalez A, Hooper DU, Perrings C, Venail P, Narwani A, Mace GM, Tilman D, Wardle DA. 2012. Biodiversity loss and its impact on humanity. Nature 486:59–67.PubMedCrossRefGoogle Scholar
  9. Chen CTA. 2002. Shelf- vs. dissolution-generated alkalinity above the chemical lysocline. Deep Sea Res II 49:5365–75.CrossRefGoogle Scholar
  10. Chen CTA, Wang SL. 1999. Carbon, alkalinity and nutrient budgets on the East China Sea continental shelf. J Geophys Res 104:20675–86.CrossRefGoogle Scholar
  11. Clarke KR, Gorley RN. 2006. Primer v6: user manual/tutorial. Plymouth: PRIMER-E.Google Scholar
  12. Cornwell JC, Kemp WM, Kana TM. 1999. Denitrification in coastal ecosystems: methods, environmental controls, and ecosystem level controls, a review. Aquat Ecol 33:41–54.CrossRefGoogle Scholar
  13. Deek A, Emeis K, van Beusekom J. 2012. Nitrogen removal in coastal sediments of the German Wadden Sea. Biogeochemistry 108:1–17.CrossRefGoogle Scholar
  14. Degraer S, Verfaillie E, Willems W, Adriaens E, Vincx M, Van Lancker V. 2008. Habitat suitability modelling as a mapping tool for macrobenthic communities: an example from the Belgian part of the North Sea. Cont Shelf Res 28:369–79.CrossRefGoogle Scholar
  15. Degraer S, Braeckman U, Haelters J, Hostens K, Jacques TG, Kerckhof F, Merckx B, Rabaut M, Stienen EWM, Van Hoey G, et al. 2009. Studie betreffende het opstellen van een lijst met potentiële Habitatrichtlijngebieden in het Belgische deel van de Noordzee. Eindrapport, 93 pp.Google Scholar
  16. Deutsch B, Forster S, Wilhelm M, Dippner JW, Voss M. 2010. Denitrification in sediments as a major nitrogen sink in the Baltic Sea: an extrapolation using sediment characteristics. Biogeosciences 7:3259–71.CrossRefGoogle Scholar
  17. Doney SC. 2010. The growing human footprint on coastal and open-ocean biogeochemistry. Science 328:1512–16.PubMedCrossRefGoogle Scholar
  18. Eggleston J, Rojstaczer S. 1998. Inferring spatial correlation of hydraulic conductivity from sediment cores and outcrops. Geophys Res Lett 25:2321–4.CrossRefGoogle Scholar
  19. Emmerson MC, Raffaelli DG. 2000. Detecting the effects of diversity on measures of ecosystem function: experimental design, null models and empirical observations. Oikos 91:195–203.CrossRefGoogle Scholar
  20. Eyre BD, Ferguson AJ. 2002. Comparison of carbon production and decomposition, benthic nutrient fluxes and denitrification in seagrass, phytoplankton, benthic microalgae- and macroalgae-dominated warm-temperate Australian lagoons. Mar Ecol Prog Ser 229:43–59.CrossRefGoogle Scholar
  21. Forster S, Bobertz B, Bohling B. 2003. Permeability of sands in the coastal areas of the southern Baltic Sea: mapping a grain-size related sediment property. Aquat Geochem 9:171–90.CrossRefGoogle Scholar
  22. Franco M, Vanaverbeke J, Van Oevelen D, Soetaert K, Costa MJ, Vincx M, Moens T. 2010. Respiration partitioning in contrasting subtidal sediments: seasonality and response to a spring phytoplankton deposition. Mar Ecol 31:276–90.CrossRefGoogle Scholar
  23. Gao Y, Lesven L, Gillan D, Sabbe K, Billon G, De Galan S, Elskens M, Baeyens W, Leermakers M. 2009. Geochemical behavior of trace elements in sub-tidal marine sediments of the Belgian coast. Mar Chem 117:88–96.CrossRefGoogle Scholar
  24. Gao H, Matyka M, Liu B, Khalili A, Kostka JE, Collins G, Jansen S, Holtappels M, Jensen MM, Badewien TH et al. 2012. Intensive and extensive nitrogen loss from intertidal permeable sediments of the Wadden Sea. Limnol Ocean 57:185.CrossRefGoogle Scholar
  25. Gérino M, Stora G, Francois F, Gilbert F, Poggiale JC, Mermillod-Blondin F, Desrosiers G, Vervier P. 2003. Macro-invertebrate functional groups in freshwater and marine sediments: a common mechanistic classification. Vie Milieu 53:221–32.Google Scholar
  26. Gilbertson WW, Solan M, Prosser JI. 2012. Differential effects of microorganism–invertebrate interactions on benthic nitrogen cycling. FEMS Microbiol Ecol 82:11–22.PubMedCrossRefGoogle Scholar
  27. Gillan DC, Pede A, Sabbe K, Gao Y, Leermakers M, Baeyens W, Louriño Cabana B, Billon G. 2012. Effect of bacterial mineralization of phytoplankton-derived phytodetritus on the release of arsenic, cobalt and manganese from muddy sediments in the Southern North Sea. A microcosm study. Sci Total Environ 419(2012):98–108.PubMedCrossRefGoogle Scholar
  28. Godbold J, Solan M. 2009. Relative importance of biodiversity and the abiotic environment in mediating an ecosystem process. Mar Ecol Prog Ser 396:273–82.CrossRefGoogle Scholar
  29. Godbold JA, Solan M, Killham K. 2008. Consumer and resource diversity effects on marine macroalgal decomposition. Oikos 118:77–86.CrossRefGoogle Scholar
  30. Grenz C, Cloern JE, Hager SW, Cole BE. 2000. Dynamics of nutrient cycling and related benthic nutrient and oxygen fluxes during a spring phytoplankton bloom in South San Francisco Bay (USA). Mar Ecol Prog Ser 197:67–80.CrossRefGoogle Scholar
  31. Halpern BS, Walbridge S, Selkoe KA, Kappel CV, Micheli F, D’Agrosa C, Bruno JF, Casey KS, Ebert C, Fox HE, Fujita R, Heinemann D, Lenihan HS, Madin EMP, Perry MT, Selig ER, Spalding M, Steneck R, Watson R. 2008. A global map of human impact on marine ecosystems. Science 319:948–52.PubMedCrossRefGoogle Scholar
  32. Heiberger RM, Holland B. 2004. Statistical analysis and data display: an intermediate course with examples in S-plus, R, and SAS. Springer.Google Scholar
  33. Hooper D, Chapin F, Ewel J, Hector A, Inchausti P, Lavorel S, Lawton J, Lodge D, Loreau M, Naeem S, Schmid B, Setala H, Symstad A, Vandermeer J, Wardle D. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol Monogr 75:3–35.CrossRefGoogle Scholar
  34. Hu X, Cai WJ. 2011. An assessment of ocean margin anaerobic processes on oceanic alkalinity budget. Glob Biogeochem Cycles 25:GB3003.CrossRefGoogle Scholar
  35. Huettel M, Rusch A. 2000. Transport and degradation of phytoplankton in permeable sediment. Limnol. Oceanogr. 45:534–49.CrossRefGoogle Scholar
  36. Huettel M, Roy H, Precht E, Ehrenhauss S. 2003. Hydrodynamical impact on biogeochemical processes in aquatic sediments. Hydrobiologia 494:231–6.CrossRefGoogle Scholar
  37. Hulth S, Aller RC, Canfield DE, Dalsgaard T, Engstrom P, Gilbert F, Sundback K, Thamdrup B. 2005. Nitrogen removal in marine environments: recent findings and future research challenges. Mar Chem 94:125–45.CrossRefGoogle Scholar
  38. Ieno EN, Solan M, Batty P, Pierce GJ. 2006. How biodiversity affects ecosystem functioning: roles of infaunal species richness, identity and density in the marine benthos. Mar Ecol Prog Ser 311:263–71.CrossRefGoogle Scholar
  39. Jensen MH, Lomstein E, Sørensen J. 1990. Benthic NH4 and NO3 flux following sedimentation of a spring phytoplankton bloom in Aarhus Bight, Denmark. Mar Ecol Prog Ser 61:87–96.CrossRefGoogle Scholar
  40. Jörgensen BB. 1983. Processes at the sediment–water interface. In: Bolin B, Cook RB, Eds. Major biogeochemical cycles their interactions. New York: Wiley. p 477–515.Google Scholar
  41. Joye SB, Hollibaugh JT. 1995. Influence of sulfide inhibition of nitrification on nitrogen regeneration in sediments. Science 270:623–5.CrossRefGoogle Scholar
  42. Kana T, Darkangelo C, Hunt M, Oldham J, Bennett G, Cornwell J. 1994. Membrane inlet mass-spectrometer for rapid high-precision determination of N2, O2 and in Ar in environmental water samples. Anal Chem 66:4166–70.CrossRefGoogle Scholar
  43. Kanneworff E, Christensen H. 1986. Benthic community respiration in relation to sedimentation of phytoplankton in the Øresund. Ophelia 26:269–84.CrossRefGoogle Scholar
  44. Kristensen E, Kostka JE. 2005. Macrofaunal burrows and irrigation in marine sediment: microbiological and biogeochemical interactions. In: Kristensen E, Haese RR, Kostka JE, Eds. Interactions between macro- and microorganisms in marine sediments. Washington: American Geophysical Union. CrossRefGoogle Scholar
  45. Lancelot C, Spitz Y, Gypens N, Ruddick K, Becquevort S, Rousseau V, Lacroix G, Billen G. 2005. Modelling diatom and Phaeocystis blooms and nutrient cycles in the Southern Bight of the North Sea: the MIRO model. Mar Ecol Prog Ser 289:63–78.CrossRefGoogle Scholar
  46. Maire O, Duchene JC, Gremare A, Malyuga VS, Meysman FJR. 2007. A comparison of sediment reworking rates by the surface deposit-feeding bivalve Abra ovata during summertime and wintertime, with a comparison between two models of sediment reworking. J Exp Mar Biol Ecol 343:21–36.CrossRefGoogle Scholar
  47. Malkin SY, Rao AMF, Seitaj D, Vasquez-Cardenas D, Zetsche EM, Hidalgo-Martinez S, Boschker HTS, Meysman FJR. Accepted. Natural occurrence of microbial sulphur oxidation by long-range electron transport in the seafloor. ISME J.Google Scholar
  48. Marcus NH, Boero F. 1998. Minireview: the importance of benthic–pelagic coupling and the forgotten role of life cycles in coastal aquatic systems. Limnol Ocean 43:763–8.CrossRefGoogle Scholar
  49. Mermillod-Blondin F, Rosenberg R, Francois-Carcaillet F, Norling K, Mauclaire L. 2004. Influence of bioturbation by three benthic infaunal species on microbial communities and biogeochemical processes in marine sediment. Aquat Microb Ecol 36:271–84.CrossRefGoogle Scholar
  50. Mermillod-Blondin F, François-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.CrossRefGoogle Scholar
  51. Meysman FJ, Middelburg JJ, Heip CH. 2006. Bioturbation: a fresh look at Darwin’s last idea. Trends Ecol Evol 21:688–95.PubMedCrossRefGoogle Scholar
  52. Michaud E, Desrosiers G, Mermillod-Blondin F, Sundby B, Stora G. 2005. The functional group approach to bioturbation: the effects of biodiffusers and gallery-diffusers of the Macoma balthica community on sediment oxygen uptake. J Exp Mar Biol Ecol 326:77–88.CrossRefGoogle Scholar
  53. Na T, Gribsholt B, Galaktionov OS, Lee T, Meysman FJR. 2008. Influence of advective bio-irrigation on carbon and nitrogen cycling in sandy sediments. J Mar Res 66:691–722.CrossRefGoogle Scholar
  54. Nielsen LP, Risgaard-Petersen N, Fossing H, Christensen PB, Sayama M. 2010. Electric currents couple spatially separated biogeochemical processes in marine sediment. Nature 463:1071–4.PubMedCrossRefGoogle Scholar
  55. Norling K, Rosenberg R, Hulth S, Gremare A, Bonsdorff E. 2007. Importance of functional biodiversity and species-specific traits of benthic fauna for ecosystem functions in marine sediment. Mar Ecol Prog Ser 332:11–23.CrossRefGoogle Scholar
  56. Parsons TR, Maita Y, Lalli CM. 1984. A manual of chemical and biological methods for seawater analysis. New York: Pergamon Press.Google Scholar
  57. Pede A. 2012. Diversity and dynamics of protist communities in subtidal North Sea sediments in relation to metal pollution and algal bloom deposition.Google Scholar
  58. Pelegri SP, Nielsen LP, Blackburn TH. 1994. Denitrification in estuarine sediment stimulated by the irrigation activity of the amphipod Corophium volutator. Mar Ecol Prog Ser 105:285–90.CrossRefGoogle Scholar
  59. Pinheiro JC, Bates D. 2009. Mixed-effects models in S and S-PLUS. New York: Springer.Google Scholar
  60. Provoost P, Braeckman U, Vanaverbeke J, Middelburg JJ, Soetaert K. 2013. Benthic oxygen consumption and benthic–pelagic coupling at a shallow station in the Southern North Sea. Estuar Coast Shelf Sci 120:1–11.CrossRefGoogle Scholar
  61. Queirós AM, Birchenough SNR, Bremner J, Godbold JA, Parker RE, Romero-Ramirez A, Reiss H, Solan M, Somerfield PJ, Van Colen C, Van Hoey G, Widdicombe S. 2013. A bioturbation classification of European marine infaunal invertebrates. Ecol Evol 3:3958–85.PubMedCentralPubMedCrossRefGoogle Scholar
  62. Raffaelli DG. 2006. Biodiversity and ecosystem functioning: issues of scale and trophic complexity. Mar Ecol Prog Ser 311:285–94.CrossRefGoogle Scholar
  63. Rasheed M, Badran MI, Huettel M. 2003. Influence of sediment permeability and mineral composition on organic matter degradation in three sediments from the Gulf of Aqaba, Red Sea. Estuar Coast Shelf Sci 57:369–84.CrossRefGoogle Scholar
  64. 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.CrossRefGoogle Scholar
  65. Rousseau V, Leynaert A, Daoud N, Lancelot C. 2002. Diatom succession, silicification and silicic acid availability in Belgian coastal waters (Southern North Sea). Mar Ecol Prog Ser 236:61–73.CrossRefGoogle Scholar
  66. Rudnick DT. 1989. Time lags between the deposition and meiobenthic assimilation of phytodetritus. Mar Ecol Prog Ser 50:231–40.CrossRefGoogle Scholar
  67. Rusch A, Forster S, Huettel M. 2001. Bacteria, diatoms and detritus in an intertidal sandflat subject to advective transport across the water-sediment interface. Biogeochemistry 55:1–27.CrossRefGoogle Scholar
  68. Rysgaard S, Christensen PB, Nielsen LP. 1995. Seasonal variation in nitrification and denitrification in estuarine sediment colonized by benthic microalgae and bioturbating infauna. Mar Ecol Prog Ser 126:111–21.CrossRefGoogle Scholar
  69. Seitzinger SP. 1988. Denitrification in freshwater and coastal marine ecosystems: ecological and geochemical significance. Limnol Ocean Methods 33:702–24.CrossRefGoogle Scholar
  70. Smith SV, Hollibaugh JT. 1993. Coastal metabolism and the oceanic organic carbon balance. Rev Geophys 31:75–89.CrossRefGoogle Scholar
  71. Soetaert K, Middelburg JJ. 2009. Modeling eutrophication and oligotrophication of shallow-water marine systems: the importance of sediments under stratified and well-mixed conditions. Eutrophication Coast Ecosyst 207:239–54.CrossRefGoogle Scholar
  72. Soetaert K, Herman PMJ, Middelburg JJ, Heip C, Smith CL, Tett P, Wild-Allen K. 2001. Numerical modelling of the shelf break ecosystem: reproducing benthic and pelagic measurements. Deep Sea Res II 48:3141–77.CrossRefGoogle Scholar
  73. Soetaert K, Van den Meersche K, van Oevelen D. 2009. LimSolve: solving linear inverse models. R Package Version 1. Accessed 03 July 2013.
  74. Solan M, Cardinale BJ, Downing AL, Engelhardt KAM, Ruesink JL, Srivastava DS. 2004. Extinction and ecosystem function in the marine benthos. Science 306:1177–80.PubMedCrossRefGoogle Scholar
  75. Solan M, Scott F, Dulvy NK, Godbold JA, Parker R. 2012. Incorporating extinction risk and realistic biodiversity futures: implementation of trait-based extinction scenarios. Marine biodiversity and ecosystem functioning: frameworks, methodologies, and integration. Oxford: Oxford University Press. pp 127–48.Google Scholar
  76. Teal LR, Parker ER, Solan M. 2010. Sediment mixed layer as a proxy for benthic ecosystem process and function. Mar Ecol Prog Ser 414:27–40.CrossRefGoogle Scholar
  77. Teal LR, Parker ER, Solan M. 2013. Coupling bioturbation activity to metal (Fe and Mn) profiles in situ. Biogeosciences 10:2365–78.CrossRefGoogle Scholar
  78. Thomas H, Schiettecatte LS, Suykens K, Koné YJM, Shadwick EH, Prowe F, Bozec Y, de Baar HJW, Borges AV. 2009. Enhanced ocean carbon storage from anaerobic alkalinity generation in coastal sediments. Biogeosciences 6:267–74.CrossRefGoogle Scholar
  79. Underwood AJ. 1997. Experiments in ecology: their logical design and interpretation using analysis of variance. Cambridge: Cambridge University Press.Google Scholar
  80. Van Colen C, Rossi F, Montserrat F, Andersson M, Gribsholt B, Herman P, Degraer S, Vincx M, Ysebaert T, Middelburg J. 2012. Organism–sediment interactions govern post-hypoxia recovery of ecosystem functioning. PLoS ONE 7(11):e49795.PubMedCentralPubMedCrossRefGoogle Scholar
  81. Van Hoey G, Degraer S, Vincx M. 2004. Macrobenthic community structure of soft-bottom sediments at the Belgian Continental Shelf. Estuar Coast Shelf Sci 59:599–613.CrossRefGoogle Scholar
  82. Van Hoey G, Pecceu E, Vanaverbeke J, Hostens K, Vincx M. 2009. Macrobenthos monitoring on the Belgian Part of the North Sea in the framework of the OSPAR eutrophication assessment (EUTROF). Ilvo Report, p 50.Google Scholar
  83. Verfaillie E, Van Lancker V, Van Meirvenne M. 2006. Multivariate geostatistics for the predictive modelling of the surficial sand distribution in shelf seas. Cont Shelf Res 26:2454–68.CrossRefGoogle Scholar
  84. Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman DG. 1997. Human alteration of the global nitrogen cycle: sources and consequences. Ecol Appl 7:737–50.Google Scholar
  85. Waldbusser GG, Marinelli RL, Whitlatch RB, Visscher PT. 2004. The effects of infaunal biodiversity on biogeochemistry of coastal marine sediments. Limnol Ocean 49:1482–92.Google Scholar
  86. Wentworth CK. 1922. A scale of grade and class terms for clastic sediments. J Geol 30:377–92.CrossRefGoogle Scholar
  87. Wenzhöfer F, Glud RN. 2002. Benthic carbon mineralization in the Atlantic: a synthesis based on in situ data from the last decade. Deep Sea Res I 49:1255–79.CrossRefGoogle Scholar
  88. West B, Welch KB, Galecki AT. 2006. Linear mixed models: a practical guide using statistical software. Boca Raton: Taylor & Francis.Google Scholar
  89. Wilson AM, Huettel M, Klein S. 2008. Grain size and depositional environment as predictors of permeability in coastal marine sands. Estuar Coast Shelf Sci 80(1):193–9.CrossRefGoogle Scholar
  90. Wollast R. 1998. Evaluation and comparison of the global carbon cycle in the coastal zone and in the open ocean. The Sea 10:213–52.Google Scholar
  91. Wright SW, Jeffrey SW. 1997. High-resolution HPLC system for chlorophylls and carotenoids of marine phytoplankton. In: Jeffrey SW, Mantoura RFC, Wright SW, Eds. Phytoplankton pigments in oceanography: guidelines to modern methods. Paris: UNESCO. p 327–41.Google Scholar
  92. Yingst JY, Rhoads DC. 1980. The role of bioturbation in the enhancement of bacterial growth rates in marine sediments. In: Tenore, K.R. et al. Ed. Marine Benthic Dynamics: 11th Belle W. Baruch symposium in marine science, Georgetown (SC) April 1979. The Belle W. Baruch Library in Marine Science, pp 407–21.Google Scholar
  93. Zuur A, Ieno EN, Walker N. 2009. Mixed effects models and extensions in ecology with R. New York: Springer.CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2014

Authors and Affiliations

  • U. Braeckman
    • 1
    Email author
  • M. Yazdani Foshtomi
    • 1
    • 2
  • D. Van Gansbeke
    • 1
  • F. Meysman
    • 3
    • 4
  • K. Soetaert
    • 3
  • M. Vincx
    • 1
  • J. Vanaverbeke
    • 1
  1. 1.Marine Biology Research Group, Department of BiologyGhent UniversityGhentBelgium
  2. 2.Iranian National Institute for OceanographyTehranIran
  3. 3.Department of Ecosystem StudiesNetherlands Institute for Sea ResearchYersekeThe Netherlands
  4. 4.Department of Analytical and Environmental ChemistryVrije Universiteit Brussel (VUB)BrusselsBelgium

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