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Loss of Large Animals Differentially Influences Nutrient Fluxes Across a Heterogeneous Marine Intertidal Soft-Sediment Ecosystem

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Abstract

Coastal marine soft-sediment ecosystems profoundly influence nutrient cycling, carbon flows and primary productivity; both the resident animal communities and environmental characteristics can drive the direction and magnitude of fluxes across the sediment–water interface. Coastal and estuarine sedimentary ecosystems are spatially heterogeneous, and many are degrading due to environmental change. How ecosystem function is affected by spatial variation in both habitats and associated animals is critical for understanding the role of specific habitats in ecosystem function and defining the consequence of the functional extinction of species and changes in habitat spatial distributions. In a multi-site field experiment, we tested the effects of spatial variation in benthic communities and environmental characteristics along natural gradients in sediment grain size. We experimentally simulated the depletion of large benthic macrofauna to assess the impact of these functionally important taxa on key ecosystem functions through ammonium and oxygen solute fluxes across the sediment–water interface. The magnitude of change in solute fluxes varied across sites and depletion treatments and was explained by changes in both sediment physico-chemical characteristics and the functional attributes of the benthic community. Quantifying variation in fluxes across multiple habitats provides insight into the trajectory of change and the consequences for ecosystem function at broad spatial scales.

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References

  • Achen CH. 1982. Interpreting and using regression. Beverley Hills and London: Sage Publications.

    Google Scholar 

  • Akaike H. 1974. A new look at the statistical model identification. IEEE Transactions on Automatic Control 19:716–23.

    Google Scholar 

  • Anderson MJ. 2008. Animal-sediment relationships re-visited: characterising species’ distributions along an environmental gradient using canonical analysis and quantile regression splines. Journal of Experimental Marine Biology and Ecology 366:16–27.

    Google Scholar 

  • Arar EJ, Collins GB. 1997. Method 445.0: In vitro determination of chlorophyll a and pheophytin a in marine and freshwater algae by fluorescence: United States Environmental Protection Agency, Office of Research and Development, National Exposure Research Laboratory.

  • Banks JL, Ross DJ, Keough MJ, Macleod CK, Eyre BD. 2012. Influence of small-scale patchiness on resilience of nutrient cycling to extended hypoxia in estuarine sediments. Marine Ecology Progress Series 453:49–62.

    CAS  Google Scholar 

  • Banks JL, Ross DJ, Keough MJ, Macleod CK, Keane J, Eyre BD. 2013. Influence of a burrowing, metal-tolerant polychaete on benthic metabolism, denitrification and nitrogen regeneration in contaminated estuarine sediments. Marine Pollution Bulletin 68:30–7.

    CAS  PubMed  Google Scholar 

  • Barbier EB, Hacker SD, Kennedy C, Koch EW, Stier AC, Silliman BR. 2011. The value of estuarine and coastal ecosystem services. Ecological Monographs 81:169–93.

    Google Scholar 

  • Bergamino L, Richoux NB. 2015. Spatial and temporal changes in estuarine food web structure: differential contributions of marsh grass detritus. Estuaries and Coasts 38:367–82.

    CAS  Google Scholar 

  • Bulmer RH, Schwendenmann L, Lohrer AM, Lundquist CJ. 2017. Sediment carbon and nutrient fluxes from cleared and intact temperate mangrove ecosystems and adjacent sandflats. Science of the Total Environment 599–600:1874–84.

    Google Scholar 

  • Byers JE, Cuddington K, Jones CG, Talley TS, Hastings A, Lambrinos JG, Crooks JA, Wilson WG. 2006. Using ecosystem engineers to restore ecological systems. Trends in Ecology & Evolution 21:493–500.

    Google Scholar 

  • Danovaro R, Gambi C, Dell’Anno A, Corinaldesi C, Fraschetti S, Vanreusel A, Vincx M, Gooday AJ. 2008. Exponential decline of deep-sea ecosystem functioning linked to benthic biodiversity loss. Current Biology 18:1–8.

    CAS  PubMed  Google Scholar 

  • Day PR. 1965. Particle fractionation and particle-size analysis. In: Black CA, Ed. Methods of Soil Analysis. Madison: American Society of Agronomy. p 545–67.

    Google Scholar 

  • Dayton PK. 2003. The importance of the natural sciences to conservation. The American Naturalist 162:1–13.

    PubMed  Google Scholar 

  • Dean WE. 1974. Determination of carbonate and organic matter in calcareous sediments and sedimentary rocks by loss on ignition: comparison with other methods. Journal of Sedimentary Petrology 44:242–8.

    CAS  Google Scholar 

  • Dortch Q. 1990. The interaction between ammonium and nitrate uptake in phytoplankton. Marine ecology progress series. Oldendorf 61:183–201.

    CAS  Google Scholar 

  • Douglas EJ, Pilditch CA, Kraan C, Schipper LA, Lohrer AM, Thrush SF. 2017. Macrofaunal functional diversity provides resilience to nutrient enrichment in coastal sediments. Ecosystems 20:1324–36.

    CAS  Google Scholar 

  • Ellison AM, Bank MS, Clinton BD, Colburn EA, Elliott K, Ford CR, Foster DR, Kloeppel BD, Knoepp JD, Lovett GM. 2005. Loss of foundation species: consequences for the structure and dynamics of forested ecosystems. Frontiers in Ecology and the Environment 3:479–86.

    Google Scholar 

  • Eyre BD, Ferguson AJ, Webb A, Maher D, Oakes JM. 2011. Denitrification, N-fixation and nitrogen and phosphorus fluxes in different benthic habitats and their contribution to the nitrogen and phosphorus budgets of a shallow oligotrophic sub-tropical coastal system (southern Moreton Bay, Australia). Biogeochemistry 102:111–33.

    CAS  Google Scholar 

  • Findlay RH, Trexler MB, Guckert J, White DC. 1990. Laboratory study of disturbance in marine sediments: response of a microbial community. Marine Ecology Progress Series 62:121–33.

    Google Scholar 

  • Foley JA, DeFries R, Asner GP, Barford C, Bonan G, Carpenter SR, Chapin FS, Coe MT, Daily GC, Gibbs HK. 2005. Global consequences of land use. Science 309:570–4.

    CAS  PubMed  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.

    PubMed  PubMed Central  Google Scholar 

  • Gravel D, Guichard F, Loreau M, Mouquet N. 2010. Source and sink dynamics in meta-ecosystems. Ecology 91:2172–84.

    PubMed  Google Scholar 

  • Hewitt JE, Thrush SF, Dayton PD. 2008. Habitat variation, species diversity and ecological functioning in a marine system. Journal of Experimental Marine Biology and Ecology 366:116–22.

    Google Scholar 

  • Hillman JR, Lundquist CJ, Pilditch CA, Thrush SF. 2020. The role of large macrofauna in mediating sediment erodibility across sedimentary habitats. Limnology and Oceanography 65:683–93.

    Google Scholar 

  • Hoegh-Guldberg O, Bruno JF. 2010. The impact of climate change on the world’s marine ecosystems. Science 328:1523–8.

    CAS  PubMed  Google Scholar 

  • Hooper DU, Chapin F, Ewel J, Hector A, Inchausti P, Lavorel S, Lawton J, Lodge D, Loreau M, Naeem S. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecological Monographs 75:3–35.

    Google Scholar 

  • Jones CG, Lawton JH, Shachak M. 1994. Organisms as ecosystem engineers. In: Samson FB, Knopf FL, Eds. Ecosystem management: selected readings. Berlin: Springer. p 130–47.

  • Kristensen E, Delefosse M, Quintana CO, Flindt MR, Valdemarsen T. 2014. Influence of benthic macrofauna community shifts on ecosystem functioning in shallow estuaries. Frontiers in Marine Science 1:41.

    Google Scholar 

  • Levin LA, Ekau W, Gooday AJ, Jorissen F, Middelburg JJ, Naqvi SWA, Neira C, Rabalais NN, Zhang J. 2009. Effects of natural and human-induced hypoxia on coastal benthos. Biogeosciences 6:2063–98.

    CAS  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.

    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.

    Google Scholar 

  • Lohrer AM, Townsend M, Hailes SF, Rodil IF, Cartner K, Pratt DR, Hewitt JE. 2016. Influence of New Zealand cockles (Austrovenus stutchburyi) on primary productivity in sandflat-seagrass (Zostera muelleri) ecotones. Estuarine, Coastal and Shelf Science 181:238–48.

    CAS  Google Scholar 

  • Loreau M, Mouquet N, Holt RD. 2003. Meta-ecosystems: a theoretical framework for a spatial ecosystem ecology. Ecology Letters 6:673–9.

    Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Lorenzen CJ. 1967. Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnology and Oceanography 12:343–6.

    CAS  Google Scholar 

  • Millenium Ecosystem Assessment. 2005. Millennium Ecosystem Assessment: Living Beyond Our Means—Natural Assets and Human Well-Being. Washington, DC: World Resources Institute.

    Google Scholar 

  • Mitchener H, Torfs H. 1996. Erosion of mud/sand mixtures. Coastal Engineering 29:1–25.

    Google Scholar 

  • Mouquet N, Miller ET, Daufresne T, Kneitel MJ. 2006. Consequences of varying regional heterogeneity in source–sink metacommunities. Oikos 113:481–8.

    Google Scholar 

  • Needham HR, Pilditch CA, Lohrer AM, Thrush SF. 2010. Habitat dependence in the functional traits of Austrohelice crassa, a key bioturbating species. Marine Ecology Progress Series 414:179–93.

    Google Scholar 

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

    PubMed  PubMed Central  Google Scholar 

  • Norkko J, Gammal J, Hewitt JE, Josefson AB, Carstensen J, Norkko A. 2015. Seafloor ecosystem function relationships: in situ patterns of change across gradients of increasing hypoxic stress. Ecosystems 18:1424–39.

    CAS  Google Scholar 

  • Norling K, Rosenberg R, Hulth S, Grémare A, Bonsdorff E. 2007. Importance of functional biodiversity and species-specific traits of benthic fauna for ecosystem functions in marine sediment. Marine Ecology Progress Series 332:11–23.

    CAS  Google Scholar 

  • O’Meara TA, Hillman JR, Thrush SF. 2017. Rising tides, cumulative impacts and cascading changes to estuarine ecosystem functions. Scientific Reports 7:10218.

    PubMed  PubMed Central  Google Scholar 

  • Pearson T, 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 

  • Pratt DR, Pilditch CA, Lohrer AM, Thrush SF. 2013. The effects of short-term increases in turbidity on sandflat microphytobenthic productivity and nutrient fluxes. Journal of Sea Research 92:170–7.

    Google Scholar 

  • R Core Team. 2017. R: A language and environment for statistical computing. Vienna: R Foundation for Statistical Computing.

    Google Scholar 

  • Reid W, Mooney H, Cropper A, Capistrano D, Carpenter S, Chopra K, Dasgupta P, Dietz T, Duraiappah A, Hassan R, Kasperson R, Leemans R, May R, McMichael T, Pingali P, Samper C, Scholes R, Watson R, Zakri A, Shidong Z, Ash N, Bennett E, Kumar P, Lee M, Raudsepp-Hearne C, Simons H, Thonell J, Zurek M. 2005. Millennium Ecosystem Assessment synthesis report. Washington, DC: Millenium Assessment and World Resources Institute.

    Google Scholar 

  • Reise K. 1985. Predator control in marine tidal sediments. In: Gibbs P, editor. Proceedings of the 19th European Marine Biology Symposium Plymouth. Cambridge: Cambridge University Press, pp 311–322.

  • Snelgrove PVR, Thrush SF, Wall DH, Norkko A. 2014. Real world biodiversity–ecosystem functioning: a seafloor perspective. Trends in Ecology & Evolution 29:398–405.

    Google Scholar 

  • Solan M, Cardinale BJ, Downing AL, Engelhardt KA, Ruesink JL, Srivastava DS. 2004. Extinction and ecosystem function in the marine benthos. Science 306:1177–80.

    CAS  PubMed  Google Scholar 

  • Thrush SF, Cummings VJ, Dayton PK, Ford R, Grant J, Hewitt JE, Hines AH, Lawrie SM, Pridmore RD, Legendre P. 1997. Matching the outcome of small-scale density manipulation experiments with larger scale patterns: an example of bivalve adult/juvenile interactions. Journal of Experimental Marine Biology and Ecology 216:153–69.

    Google Scholar 

  • Thrush SF, Dayton PK. 2010. What can ecology contribute to ecosystem-based management? Annual Review of Marine Science 2:419–41.

    PubMed  Google Scholar 

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

    Google Scholar 

  • Thrush SF, Hewitt JE, Kraan C, Lohrer AM, Pilditch CA, Douglas E. 2017. Changes in the location of biodiversity–ecosystem function hot spots across the seafloor landscape with increasing sediment nutrient loading. Proceedings of the Royal Society B 284:20162861.

    PubMed  Google Scholar 

  • Thrush SF, Hewitt JE, Lohrer AM. 2012. Interaction networks in coastal soft-sediments highlight the potential for change in ecological resilience. Ecological Applications 22:1213–23.

    CAS  PubMed  Google Scholar 

  • Thrush SF, Hewitt JE, Parkes S, Lohrer AM, Pilditch C, Woodin SA, Wethey DS, Chiantore M, Asnaghi V, De Juan S. 2014. Experimenting with ecosystem interaction networks in search of threshold potentials in real-world marine ecosystems. Ecology 95:1451–7.

    PubMed  Google Scholar 

  • Thrush SF, Townsend M, Hewitt JE, Davies K, Lohrer AM, Lundquist CJ, Cartner K. 2013. The many uses and values of estuarine ecosystems. In: Dymond JR, Ed. Ecosystem services in New Zealand. Manaaki Whenua Press: Lincoln. p 226–37.

    Google Scholar 

  • Volkenborn N, Reise K. 2006. Lugworm exclusion experiment: responses by deposit feeding worms to biogenic habitat transformations. Journal of Experimental Marine Biology and Ecology 330:169–79.

    Google Scholar 

  • Volkenborn N, Robertson DM, Reise K. 2009. Sediment destabilizing and stabilizing bio-engineers on tidal flats: cascading effects of experimental exclusion. Helgoland Marine Research 63:27–35.

    Google Scholar 

  • Woodin SA, Marinelli RL, Lindsay SM. 1998. Process-specific cues for recruitment in sedimentary environments: geochemical signals? Journal of Marine Research 56:535–58.

    CAS  Google Scholar 

  • Woodin SA, Volkenborn N, Pilditch CA, Lohrer AM, Wethey DS, Hewitt JE, Thrush SF. 2016. Same pattern, different mechanism: locking onto the role of key species in seafloor ecosystem process. Scientific Reports 6:26678.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Zuur A, Ieno EN, Walker N, Saveliev AA, Smith GM. 2009. Mixed effects models and extensions in ecology with R. Switzerland: Springer.

    Google Scholar 

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Acknowledgements

We thank the many field assistants, and J. Hewitt, A. Vieillard, and two anonymous reviewers for comments on the manuscript. Funding to J. R. Hillman was provided by the New Zealand Ministry of Business, Innovation and Employment (National Institute of Water and Atmospheric Research Coasts & Oceans Research Programme, SSIF Project COME1903), and the Royal Society of New Zealand Hutton Fund 2015.

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Authors and Affiliations

  1. Institute of Marine Science, University of Auckland, Auckland, 1142, New Zealand

    Jenny R. Hillman, Carolyn J. Lundquist & Simon F. Thrush

  2. National Institute of Water and Atmospheric Research, Hamilton, 3251, New Zealand

    Carolyn J. Lundquist

  3. Smithsonian Environmental Research Center, 647 Contees Wharf Rd, Edgewater, MD, 21037, USA

    Theresa A. O’Meara

Authors
  1. Jenny R. Hillman
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  2. Carolyn J. Lundquist
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  3. Theresa A. O’Meara
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  4. Simon F. Thrush
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Correspondence to Jenny R. Hillman.

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Author Contributions

JRH designed and conducted the experiment, analysed the data, and wrote the manuscript. TAO contributed field labour, laboratory, and data analysis. CJL and SFT contributed during study design and development, field labour, editing, and funding.

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Hillman, J.R., Lundquist, C.J., O’Meara, T.A. et al. Loss of Large Animals Differentially Influences Nutrient Fluxes Across a Heterogeneous Marine Intertidal Soft-Sediment Ecosystem. Ecosystems 24, 272–283 (2021). https://doi.org/10.1007/s10021-020-00517-4

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