Skip to main content

Advertisement

SpringerLink
Log in

Macrofaunal Functional Diversity Provides Resilience to Nutrient Enrichment in Coastal Sediments

  • Published:
Ecosystems Aims and scope Submit manuscript

Abstract

The degradation of ecosystems is often associated with losses of large organisms and the concomitant losses of the ecological functions they mediate. Conversely, the resilience of ecosystems to stress is strongly influenced by faunal communities and their impacts on processes. Denitrification in coastal sediments is a process that may provide ecosystem resilience to eutrophication by removing excess bioavailable nitrogen. Here, we conducted a large-scale field experiment to test the effect of macrofaunal community composition on denitrification in response to two levels of nutrient enrichment at 28 sites across a biologically heterogeneous sandflat. After 7 weeks of enrichment, we measured denitrification enzyme activity (DEA) along with benthic macrofaunal community composition and environmental variables. We normalised treatment site specific DEA values by those in ambient sediments (DEACN) to reveal the underlying response across the heterogeneous landscape. Nutrient enrichment caused reductions in DEACN as well as functional changes in the community; these were both more pronounced under the highest level of nutrient loading (on average DEACN was reduced by 34%). The degree of suppression of DEACN following moderate nitrogen loading was mitigated by a key bioturbating species, but following high nitrogen loading (which reduced the key species density) the abundance and diversity of other nutrient processing species were the most important factors alleviating negative effects. This study provides a prime example of the context-dependent role of biodiversity in maintaining ecosystem functioning, underlining that different elements of biodiversity can become important as stress levels increase. Our results emphasise that management and conservation strategies require a real-world understanding of the community attributes that facilitate nutrient processing and maintain resilience in coastal ecosystems.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Figure 1
Figure 2

Similar content being viewed by others

References

  • Anderson MJ, Cribble NA. 1998. Partitioning the variation among spatial, temporal and environmental components in a multivariate data set. Australian Journal of Ecology 23:158–67.

    Article  Google Scholar 

  • Anthonisen AC, Loehr RC, Prakasam TBS, Srinath EG. 1976. Inhibition of nitrification by ammonia and nitrous acid. Water Pollution Control Federation 48:835–52.

    CAS  Google Scholar 

  • Arar E, Collins G. 1997. In vitro determination of chlorophyll a and pheophytin a in marine and freshwater algae by fluorescence. Cincinnati: National Exposure Research Laboratory, U.S. Environmental Protection Agency.

    Google Scholar 

  • Barnes J, Owens NJP. 1998. Denitrification and nitrous oxide concentrations in the Humber estuary, UK, and adjacent coastal zones. Marine Pollution Bulletin 37:247–60.

    Article  CAS  Google Scholar 

  • Bernot MJ, Dodds WK, Gardner WS, McCarthy MJ, Sobolev D, Tank JL. 2003. Comparing denitrification estimates for a Texas estuary by using acetylene inhibition and membrane inlet mass spectrometry. Applied and Environmental Microbiology 69:5950–6.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blackburn TH, Blackburn ND, Mortimer RJG, Coleman ML, Lovley DR. 1993. Rates of microbial processes in sediments. Philosophical Transactions: Physical Sciences and Engineering 344:49–58 (and discussion).

    Article  CAS  Google Scholar 

  • Borcard D, Legendre P, Drapeau P. 1992. Partialling out the spatial component of ecological variation. Ecology 73:1045–55.

    Article  Google Scholar 

  • Bruesewitz DA, Hamilton DP, Schipper LA. 2011. Denitrification potential in lake sediment increases across a gradient of catchment agriculture. Ecosystems 14:341–52.

    Article  CAS  Google Scholar 

  • Bruesewitz DA, Tank JL, Bernot MJ, Richardson WB, Strauss EA. 2006. Seasonal effects of the zebra mussel (Dreissena polymorpha) on sediment denitrification rates in Pool 8 of the Upper Mississippi River. Canadian Journal of Fisheries and Aquatic Sciences 63:957–69.

    Article  CAS  Google Scholar 

  • Burnham KP, Anderson DR. 2002. Model selection and multimodel inference: a pratical information-theoretic approach. New York (NY): Springer.

    Google Scholar 

  • Caffrey JM, Harrington N, Solem I, Ward BB. 2003. Biogeochemical processes in a small California estuary. 2. Nitrification activity, community structure and role in nitrogen budgets. Marine Ecology Progress Series 248:27–40.

    Article  CAS  Google Scholar 

  • Chapin FS, Zavaleta ES, Eviner VT, Naylor RL, Vitousek PM, Reynolds HL, Hooper DU, Lavorel S, Sala OE, Hobbie SE, Mack MC, Diaz S. 2000. Consequences of changing biodiversity. Nature 405:234–42.

    Article  CAS  PubMed  Google Scholar 

  • Clarke KR, Gorley RN. 2015. PRIMER v7: User manual/tutorial. Plymouth, 296 pp: PRIMER-E.

  • de Juan S, Thrush SF, Hewitt JE, Halliday J, Lohrer AM. 2014. Cumulative degradation in estuaries: contribution of individual species to community recovery. Marine Ecology Progress Series 510:25–38.

    Article  Google Scholar 

  • Diaz RJ, Rosenberg R. 1995. Marine benthic hypoxia: a review of its ecological effects and the behavioural responses of benthic macrofauna. In: Ansell AD, Gibson RN, Barnes M, Eds. Oceanography and marine biology—an annual review, Vol. 33. London: UCL Press Ltd. p 245–303.

    Google Scholar 

  • Diaz RJ, Rosenberg R. 2008. Spreading dead zones and consequences for marine ecosystems. Science 321:926–9.

    Article  CAS  PubMed  Google Scholar 

  • Doak DF, Bigger D, Harding EK, Marvier MA, O’Malley RE, Thomson D. 1998. The statistical inevitability of stability–diversity relationships in community ecology. American Naturalist 151:264–76.

    CAS  PubMed  Google Scholar 

  • Dormann CF, Elith J, Bacher S, Buchmann C, Carl G, Carré G, Marquéz JRG, Gruber B, Lafourcade B, Leitão PJ, Münkemüller T, McClean C, Osborne PE, Reineking B, Schröder B, Skidmore AK, Zurell D, Lautenbach S. 2013. Collinearity: a review of methods to deal with it and a simulation study evaluating their performance. Ecography 36:27–46.

    Article  Google Scholar 

  • Douglas EJ, Pilditch CA, Hines LV, Kraan C, Thrush SF. 2016. In situ soft sediment nutrient enrichment: a unified approach to eutrophication field experiments. Marine Pollution Bulletin 111:287–94.

    Article  CAS  PubMed  Google Scholar 

  • Elmqvist T, Folke C, Nyström M, Peterson G, Bengtsson J, Walker B, Norberg J. 2003. Response diversity, ecosystem change, and resilience. Frontiers in Ecology and the Environment 1:488–94.

    Article  Google Scholar 

  • Eyre BD, Ferguson AJP. 2002. Comparison of carbon production and decomposition, benthic nutrient fluxes and denitrification in seagrass, phytoplankton, benthic microalgae- and macroalgae-dominated warm-temperate Australian lagoons. Marine Ecology Progress Series 229:43–59.

    Article  CAS  Google Scholar 

  • Eyre BD, Maher DT, Squire P. 2013. Quantity and quality of organic matter (detritus) drives N2 effluxes (net denitrification) across seasons, benthic habitats and estuaries. Global Biogeochemical Cycles 27:1083–95.

    Article  CAS  Google Scholar 

  • Fitch JE, Crowe TP. 2012. Combined effects of inorganic nutrients and organic enrichment on intertidal benthic macrofauna: an experimental approach. Marine Ecology Progress Series 461:59–70.

    Article  Google Scholar 

  • Folke C, Carpenter S, Walker B, Scheffer M, Elmqvist T, Gunderson L, Holling CS. 2004. Regime shifts, resilience, and biodiversity in ecosystem management. Annual Review of Ecology, Evolution, and Systematics 35:557–81.

    Article  Google Scholar 

  • Foster SQ, Fulweiler RW. 2014. Spatial and historical variability of benthic nitrogen cycling in an anthropogenically impacted estuary. Frontiers in Marine Science 1:56.

    Article  Google Scholar 

  • Galloway JN, Aber JD, Erisman JW, Seitzinger SP, Howarth RW, Cowling EB, Cosby BJ. 2003. The nitrogen cascade. Bioscience 53:341–56.

    Article  Google Scholar 

  • Galloway JN, Townsend AR, Erisman JW, Bekunda M, Cai ZC, Freney JR, Martinelli LA, Seitzinger SP, Sutton MA. 2008. Transformation of the nitrogen cycle: recent trends, questions, and potential solutions. Science 320:889–92.

    Article  CAS  PubMed  Google Scholar 

  • Gilbert F, Stora G, Bonin P. 1998. Influence of bioturbation on denitrification activity in Mediterranean coastal sediments: an in situ experimental approach. Marine Ecology Progress Series 163:99–107.

    Article  CAS  Google Scholar 

  • Gladstone-Gallagher RV, Lundquist CJ, Pilditch CA. 2014. Response of temperate intertidal benthic assemblages to mangrove detrital inputs. Journal of Experimental Marine Biology and Ecology 460:80–8.

    Article  Google Scholar 

  • Gladstone-Gallagher RV, Lohrer AM, Lundquist CJ, Pilditch CA. 2016. Effects of detrital subsidies on soft-sediment ecosystem function are transient and source-dependent. PLoS ONE 11:e0154790.

    Article  PubMed  PubMed Central  Google Scholar 

  • Glud RN. 2008. Oxygen dynamics of marine sediments. Marine Biology Research 4:243–89.

    Article  Google Scholar 

  • Gray JS, Wu RSS, Ying YO. 2002. Effects of hypoxia and organic enrichment on the coastal marine environment. Marine Ecology Progress Series 238:249–79.

    Article  Google Scholar 

  • Green MO, Coco G. 2014. Review of wave-driven sediment resuspension and transport in estuaries. Reviews of Geophysics 52:77–117.

    Article  Google Scholar 

  • Greenfield BL, Kraan C, Pilditch CA, Thrush SF. 2016. Mapping functional groups can provide insight into ecosystem functioning and potential resilience of intertidal sandflats. Marine Ecology Progress Series 548:1–10.

    Article  Google Scholar 

  • Groffman PM, Altabet MA, Böhlke JK, Butterbach-Bahl K, David MB, Firestone MK, Giblin AE, Kana TM, Nielsen LP, Voytek MA. 2006. Methods for measuring denitrification: diverse approaches to a difficult problem. Ecological Applications 16:2091–122.

    Article  PubMed  Google Scholar 

  • Groffman PM, Holland EA, Myrold DD, Robertson GP. 1999. Denitrification. In: Robertson G, Bledsoe C, Coleman D, Sollins P, Eds. Standard soil methods for long term ecological research. Cary (NC): Oxford University Press. p 272–88.

    Google Scholar 

  • Henriksen K, Kemp WM. 1988. Nitrification in estuarine and coastal marine sediments. In: Blackburn TH, Sorensen J, Eds. Nitrogen cycling in coastal marine environments. New York: Wiley. p 207–49.

    Google Scholar 

  • Hewitt J, Thrush S, Lohrer A, Townsend M. 2010. A latent threat to biodiversity: consequences of small-scale heterogeneity loss. Biodiversity and Conservation 19:1315–23.

    Article  Google Scholar 

  • Hewitt JE, Legendre P, McArdle BH, Thrush SF, Bellehumeur C, Lawrie SM. 1997. Identifying relationships between adult and juvenile bivalves at different spatial scales. Journal of Experimental Marine Biology and Ecology 216:77–98.

    Article  Google Scholar 

  • Hewitt JE, Thrush SF. 2010. Empirical evidence of an approaching alternate state produced by intrinsic community dynamics, climatic variability and management actions. Marine Ecology Progress Series 413:267–76.

    Article  Google Scholar 

  • Hines AH, Whitlatch RB, Thrush SF, Hewitt JE, Cummings VJ, Dayton PK, Legendre P. 1997. Nonlinear foraging response of a large marine predator to benthic prey: eagle ray pits and bivalves in a New Zealand sandflat. Journal of Experimental marine Biology and Ecology 216:191–210.

    Article  Google Scholar 

  • Huettel M, Berg P, Kostka JE. 2014. Benthic exchange and biogeochemical cycling in permeable sediments. Annual Review of Marine Science 6:23–51.

    Article  PubMed  Google Scholar 

  • Jones HFE, Pilditch CA, Bruesewitz DA, Lohrer AM. 2011. Sedimentary environment influences the effect of an infaunal suspension feeding bivalve on estuarine ecosystem function. PLoS ONE 6:e27065.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jauffrais T, Drouet S, Turpin V, Mèlèder V, Jesus B, Cognie B, Raimbault P, Cosson RP, Decottignies P, Martin-Jèzèquel V. 2015. Growth and biochemical composition of a microphytobenthic diatom (Entomoneis paludosa) exposed to shorebird (Calidris alpina) droppings. Journal of Experimental Marine Biology and Ecology 469:83–92.

    Article  CAS  Google Scholar 

  • Joye SB, Hollibaugh JT. 1995. Influence of sulfide inhibition of nitrification on nitrogen regeneration in sediments. Science 270:623–5.

    Article  CAS  Google Scholar 

  • Kelly JR, Nixon S. 1984. Experimental studies of the effect of organic deposition on the metabolism of a coastal marine bottom community. Marine Ecology Progress Series 17:157–69.

    Article  CAS  Google Scholar 

  • Kohler K, Gill S. 2006. Coral point count with Excel extensions (CPCe): a Visual Basic program for the determination of coral and substrate coverage using random point count methodology. Computers and Geosciences 32:1259–69.

    Article  Google Scholar 

  • Koop-Jakobsen K, Giblin AE. 2010. The effect of increased nitrate loading on nitrate reduction via denitrification and DNRA in salt marsh sediments. Limnology and Oceanography 55:789–802.

    Article  CAS  Google Scholar 

  • Kraan C, Dormann CF, Greenfield BL, Thrush SF. 2015. Cross-scale variation in biodiversity-environment links illustrated by coastal sandflat communities. PLoS ONE 10:e0142411.

    Article  PubMed  PubMed Central  Google Scholar 

  • Kristensen E, Jensen MH, Aller RC. 1991. Direct measurement of dissolved inorganic nitrogen exchange and denitrification in individual polychaete (Nereis-virens) burrows. Journal of Marine Research 49:355–77.

    Article  CAS  Google Scholar 

  • Kristensen E, Jensen MH, Andersen TK. 1985. The impact of polychaete (Nereis virens Sars) burrows on nitrification and nitrate reduction in estuarine sediments. Journal of Experimental Marine Biology and Ecology 85:75–91.

    Article  CAS  Google Scholar 

  • Laursen AE, Seitzinger SP, Dekorsey R, Sanders JG, Breitburg DL, Osman RW. 2002. Multiple stressors in an estuarine system: effects of nutrients, trace elements, and trophic complexity on benthic photosynthesis and respiration. Estuaries 25:57–69.

    Article  CAS  Google Scholar 

  • Laverock B, Gilbert JA, Tait K, Osborn AM, Widdicombe S. 2011. Bioturbation: impact on the marine nitrogen cycle. Biochemical Society Transactions 39:315–20.

    Article  CAS  PubMed  Google Scholar 

  • Livingstone MW, Smith RV, Laughlin RJ. 2000. A spatial study of denitrification potential of sediments in Belfast and Strangford Loughs and its significance. Science of the Total Environment 251:369–80.

    Article  PubMed  Google Scholar 

  • Lohrer AM, Halliday NJ, Thrush SF, Hewitt JE, Rodil IF. 2010. Ecosystem functioning in a disturbance-recovery context: contribution of macrofauna to primary production and nutrient release on intertidal sandflats. Journal of Experimental Marine Biology and Ecology 390:6–13.

    Article  Google Scholar 

  • Lohrer AM, Hewitt JE, Hailes SF, Thrush SF, Ahrens M, Halliday J. 2011. Contamination on sandflats and the decoupling of linked ecological functions. Austral Ecology 36:378–88.

    Article  Google Scholar 

  • Lohrer AM, Thrush SF, Gibbs MM. 2004. Bioturbators enhance ecosystem function through complex biogeochemical interactions. Nature 431:1092–5.

    Article  CAS  PubMed  Google Scholar 

  • Loreau M, Naeem S, Inchausti P, Bengtsson J, Grime JP, Hector A, Hooper DU, Huston MA, Raffaelli D, Schmid B, Tilman D, Wardle DA. 2001. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294:804–8.

    Article  CAS  PubMed  Google Scholar 

  • Magalhães CM, Joye SB, Moreira RM, Wiebe WJ, Bordalo AA. 2005. Effect of salinity and inorganic nitrogen concentrations on nitrification and denitrification rates in intertidal sediments and rocky biofilms of the Douro River estuary, Portugal. Water Research 39:1783–94.

    Article  PubMed  Google Scholar 

  • Mori AS, Furukawa T, Sasaki T. 2013. Response diversity determines the resilience of ecosystems to environmental change. Biol Rev Camb Philos Soc 88:349–64.

    Article  PubMed  Google Scholar 

  • Morris L, Keough MJ. 2003. Variation in the response of intertidal infaunal invertebrates to nutrient additions: field manipulations at two sites within Port Phillip Bay, Australia. Marine Ecology Progress Series 250:35–49.

    Article  CAS  Google Scholar 

  • Naeem S, Thompson LJ, Lawler SP, Lawton JH, Woodfin RM. 1994. Declining biodiversity can alter the performance of ecosystems. Nature 368:734–7.

    Article  Google Scholar 

  • Nixon S. 1998. Enriching the sea to death. Scientific American 9:48–53.

    Google Scholar 

  • Nogaro G, Burgin AJ. 2014. Influence of bioturbation on denitrification and dissimilatory nitrate reduction to ammonium (DNRA) in freshwater sediments. Biogeochemistry 120:279–94.

    Article  CAS  Google Scholar 

  • Norkko A, Villnas A, Norkko J, Valanko S, Pilditch C. 2013. Size matters: implications of the loss of large individuals for ecosystem function. Scientific Reports 3:2646.

    Article  PubMed  Google Scholar 

  • Oakes JM, Eyre BD, Ross DJ. 2011. Short-term enhancement and long-term suppression of denitrification in estuarine sediments receiving primary- and secondary-treated paper and pulp mill discharge. Environmental Science and Technology 45:3400–6.

    Article  CAS  PubMed  Google Scholar 

  • Parker JG. 1983. A comparison of methods used for the measurement of organic matter in marine sediment. Chemistry and Ecology 1:201–9.

    Article  CAS  Google Scholar 

  • Pearson TH, Rosenberg R. 1978. Macrobenthic succession in relation to organic enrichment and pollution of the marine environment. Oceanography and Marine Biology: An Annual Review 16:229–311.

    Google Scholar 

  • Pelegri SP, Nielsen LP, Blackburn TH. 1994. Denitrification in estuarine sediment stimulated by the irrigation activity of the amphipod Corophium volutator. Marine Ecology Progress Series 105:285–90.

    Article  Google Scholar 

  • Piehler MF, Smyth AR. 2011. Habitat-specific distinctions in estuarine denitrification affect both ecosystem function and services. Ecosphere 2:art12.

    Article  Google Scholar 

  • Posey MH, Alphin TD, Cahoon L. 2006. Benthic community responses to nutrient enrichment and predator exclusion: influence of background nutrient concentrations and interactive effects. Journal of Experimental Marine Biology and Ecology 330:105–18.

    Article  CAS  Google Scholar 

  • Pratt DR, Lohrer AM, Pilditch CA, Thrush SF. 2013. Changes in ecosystem function across sedimentary gradients in estuaries. Ecosystems 17:182–94.

    Article  Google Scholar 

  • Pratt DR, Lohrer AM, Thrush SF, Hewitt JE, Townsend M, Cartner K, Pilditch CA, Harris RJ, van Colen C, Rodil IF. 2015. Detecting subtle shifts in ecosystem functioning in a dynamic estuarine environment. PLoS ONE 10:e0133914.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rothschild BJ, Ault JS, Goulletquer P, Héral M. 1994. Decline of the Chesapeake Bay oyster population: a century of habitat destruction and overfishing. Marine Ecology Progress Series 111:29–39.

    Article  Google Scholar 

  • Sandwell DR, Pilditch CA, Lohrer AM. 2009. Density dependent effects of an infaunal suspension-feeding bivalve (Austrovenus stutchburyi) on sandflat nutrient fluxes and microphytobenthic productivity. Journal of Experimental Marine Biology and Ecology 373:16–25.

    Article  Google Scholar 

  • Seitzinger S, Harrison JA, Böhlke JK, Bouwman AF, Lowrance R, Peterson B, Tobias C, Van Drecht G. 2006. Denitrification across landscapes and waterscapes: a synthesis. Ecological Applications 16:2064–90.

    Article  CAS  PubMed  Google Scholar 

  • Singer JK, Anderson JB, Ledbetter MT, McCave IN, Jones KPN, Wright R. 1988. An assessment of analytical techniques for the size analysis of fine-grained sediments. Journal of Sedimentary Research 58:534–43.

    Google Scholar 

  • Sloth NP, Blackburn H, Hansen LS, Risgaard-Pedersen N, Lomstein BA. 1995. Nitrogen cycling in sediments with different organic loading. Marine Ecology Progress Series 116:163–70.

    Article  CAS  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • StatSoft Inc. 2012. STATISTICA (data analysis software system), version 11. www.statsoft.com.

  • Stief P. 2013. Stimulation of microbial nitrogen cycling in aquatic ecosystems by benthic macrofauna: mechanisms and environmental implications. Biogeosciences Discussions 10:11785–824.

    Article  Google Scholar 

  • Teixeira C, Magalhães C, Boaventura RAR, Bordalo AA. 2010. Potential rates and environmental controls of denitrification and nitrous oxide production in a temperate urbanized estuary. Marine Environmental Research 70:336–42.

    Article  CAS  PubMed  Google Scholar 

  • Thrush S, Hewitt J, Parkes S, Lohrer A, Pilditch C, Woodin SA, Wethey D, Chiantore M, Asnaghi V, De Juan S, Kraan C, Rodil I, Savage C, Van Colen C. 2014. Experimenting with ecosystem interaction networks in search of threshold potentials in real world marine ecosystems. Ecology 95:1451–7.

    Article  PubMed  Google Scholar 

  • Thrush SF, Coco G, Hewitt JE. 2008. Complex positive connections between functional groups are revealed by neural network analysis of ecological time series. American Naturalist 171:669–77.

    Article  PubMed  Google Scholar 

  • Thrush SF, Dayton PK. 2002. Disturbance to marine benthic habitats by trawling and dredging: implications for marine biodiversity. Annual Review of Ecology and Systematics 33:449–73.

    Article  Google Scholar 

  • Thrush SF, Hewitt JE, Gibbs M, Lundquist C, Norkko A. 2006. Functional role of large organisms in intertidal communities: community effects and ecosystem function. Ecosystems 9:1029–40.

    Article  Google Scholar 

  • Thrush SF, Prridmore RD, Hewitt JE, Cummings VJ. 1994. The improtance of predators on a sandflat: interplay between seasonal change sin prey densities and predator effects. Marine Ecology Progress Series 107:211–22.

    Article  Google Scholar 

  • Tiedje JM, Simkins S, Groffman PM. 1989. Perspectives on measurement of denitrification in the field including recommended protocols for acetylene based methods. Plant and Soil 115:261–84.

    Article  Google Scholar 

  • Vieillard AM, Fulweiler RW. 2012. Impacts of long-term fertilization on salt marsh tidal creek benthic nutrient and N2 gas fluxes. Marine Ecology Progress Series 471:11–22.

    Article  CAS  Google Scholar 

  • Villnäs A, Norkko J, Hietanen S, Josefson AB, Lukkari K, Norkko A. 2013. The role of recurrent disturbances for ecosystem multifunctionality. Ecology 94:2275–87.

    Article  PubMed  Google Scholar 

  • Vitousek PM, Aber JD, Howarth RW, Likens GE, Matson PA, Schindler DW, Schlesinger WH, Tilman D. 1997. Human alteration of the global nitrogen cycle: sources and consequences. Ecological Applications 7:737–50.

    Google Scholar 

  • Volkenborn N, Meile C, Polerecky L, Pilditch CA, Norkko A, Norkko J, Hewitt JE, Thrush SF, Wethey DS, Woodin SA. 2012. Intermittent bioirrigation and oxygen dynamics in permeable sediments: an experimental and modeling study of three tellinid bivalves. Journal of Marine Research 70:794–823.

    Article  CAS  Google Scholar 

  • Volkenborn N, Polerecky L, Wethey DS, Woodin SA. 2010. Oscillatory porewater bioadvection in marine sediments induced by hydraulic activities. Limnology and Oceanography 55:1231–47.

    Article  CAS  Google Scholar 

  • Wall LG, Tank JL, Royer TV, Bernot MJ. 2005. Spatial and temporal variability in sediment denitrification within an agriculturally influenced reservoir. Biogeochemistry 76:85–111.

    Article  CAS  Google Scholar 

  • Webb AP, Eyre BD. 2004. The effect of natural populations of the burrowing and grazing soldier crab (Mictyris longicarpus) on sediment irrigation, benthic metabolism and nitrogen fluxes. Journal of Experimental Marine Biology and Ecology 309:1–19.

    Article  Google Scholar 

  • Yazdani Foshtomi M, Braeckman U, Derycke S, Sapp M, Van Gansbeke D, Sabbe K, Willems A, Vincx M, Vanaverbeke J. 2015. The link between microbial diversity and nitrogen cycling in marine sediments is modulated by macrofaunal bioturbation. PLoS ONE 10:e0130116.

    Article  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank all those involved in field sampling and laboratory work, especially Barry Greenfield, Sarah Hailes, Lisa McCartain, Katie Cartner, Kelly Carter, Rosalie Carter, Carsten Dormann, Chris Eager, Laura Hines and Rebecca Gladstone-Gallagher. Special thanks to Judi Hewitt for advice with statistical analysis and two anonymous reviewers whose constructive comments improved the manuscript. This work was funded by the Marsden Fund, Royal Society of New Zealand (NIW1102) to SFT, a Marie-Curie International Outgoing Fellowship (FP7-PEOPLE-2011-IOF) to CK and CO1x1515 4.2.1 to SFT and CAP. EJD was funded by a University of Waikato Doctoral Scholarship. These funders had no role in the study design, interpretation or writing of this manuscript.

Author information

Author notes

  1. Casper Kraan

    Present address: Department of Functional Ecology, Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research, Am Handelshafen 12, 27570, Bremerhaven, Germany

Authors and Affiliations

  1. School of Science, University of Waikato, Private Bag 3105, Hamilton, 3240, New Zealand

    Emily J. Douglas, Conrad A. Pilditch & Louis A. Schipper

  2. National Institute of Water and Atmospheric Research, P.O. Box 11-115, Hamilton, 3251, New Zealand

    Casper Kraan & Andrew M. Lohrer

  3. Institute of Marine Science, University of Auckland, Private Bag 92019, Auckland, 1142, New Zealand

    Simon F. Thrush

Authors
  1. Emily J. Douglas
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Conrad A. Pilditch
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Casper Kraan
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Louis A. Schipper
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrew M. Lohrer
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Simon F. Thrush
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Conrad A. Pilditch.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Authors contributions

EJD, CAP, SFT, CK and AML designed the study and performed field research. EJD performed laboratory analyses with input from LAS. EJD and CAP analysed data, EJD wrote the manuscript with assistance from CAP and input from SFT, CK, AML and LAS.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 54 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Douglas, E.J., Pilditch, C.A., Kraan, C. et al. Macrofaunal Functional Diversity Provides Resilience to Nutrient Enrichment in Coastal Sediments. Ecosystems 20, 1324–1336 (2017). https://doi.org/10.1007/s10021-017-0113-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10021-017-0113-4

Keywords

Search

Navigation