Abstract
Fine sediment inputs can alter estuarine ecosystem structure and function. However, natural variations in the processes that regulate sediment transport make it difficult to predict their fate. In this study, sediments were sampled at different times (2011–2012) from 45 points across intertidal sandflat transects in three New Zealand estuaries (Whitford, Whangamata, and Kawhia) encompassing a wide range in mud (≤63 μm) content (0–56 %) and macrofaunal community structure. Using a core-based erosion measurement device (EROMES), we calculated three distinct measures of sediment erosion potential: erosion threshold (Ʈ c ; N m−2), erosion rate (ER; g m−2 s−1), and change in erosion rate with increasing bed shear stress (m e ; g N−1 s−1). Collectively, these measures characterized surface (Ʈ c and ER) and sub-surface (m e ) erosion. Benthic macrofauna were grouped by functional traits (size and motility) and data pooled across estuaries to determine relationships between abiotic (mud content, mean grain size) and biotic (benthic macrofauna, microbial biomass) variables and erosion measures. Results indicated that small bioturbating macrofauna (predominantly freely motile species <5 mm in size) destabilized surface sediments, explaining 23 % of the variation in Ʈ c (p ≤ 0.01) and 59 % of the variation in ER (p ≤ 0.01). Alternatively, mud content and mean grain size cumulatively explained 61 % of the variation in m e (p ≤ 0.01), where increasing mud and grain size stabilized sub-surface sediments. These results highlight that the importance of biotic and abiotic predictors vary with erosion stage and that functional group classifications are a useful way to determine the impact of benthic macrofauna on sediment erodibility across communities with different species composition.
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References
Aller, R.C. 1988. Benthic fauna and biogeochemical processes in marine sediments: the role of burrow structures. In Nitrogen cycling in coastal marine environments ed. T.H. Blackburn and J. Sørensen. John Wiley and Sons Ltd.
Amos C.L., J. Grant, G.R. Daborn, and K. Black. 1992. Sea carousel: a benthic, annular flume. Estuarine Coastal and Shelf Science 34: 557–577.
Andersen T.J., and M. Pejrup. 2002. Biological mediation of the settling velocity of bed material eroded from an intertidal mudflat, the Danish Wadden Sea. Estuarine Coastal and Shelf Science 54: 747–745.
Andersen T.J., L.C. Lund-Hansen, M. Pejrup, K.T. Jensen, and K.N. Mouritsen. 2005. Biologically induced differences in erodibility and aggregation of subtidal and intertidal sediments: a possible cause for seasonal changes in sediment deposition. Journal of Marine Systems 55: 123–138.
Andersen T.J., J. Fredsoe, and M. Pejrup. 2007. In situ estimation of erosion and deposition thresholds by acoustic Doppler velocimeter (ADV). Estuarine Coastal and Shelf Science 75: 327–336.
Andersen T.J., M. Lanuru, C. van Bernem, M. Pejrup, and R. Riethmüller. 2010. Erodibility of a mixed mudflat dominated by microphytobenthos and Cerastoderma edule, East Frisian Wadden Sea, Germany. Estuarine Coastal and Shelf Science 87: 197–206.
Anderson M.J. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecology 26: 32–46.
Anderson M.J. 2008. Animal-sediment relationships re-visited: characterizing species’ distributions along an environmental gradient using canonical analysis and quantile regression splines. Journal of Experimental Marine Biology and Ecology 366: 16–27.
Anderson M.J., R.N. Gorley, and K.R. Clarke. 2008. PERMANOVA+ for PRIMER: guide to software and statistical methods. Plymouth: Primer-E.
Arar, E. and G. Collins. 1997. Method 445.0: In vitro determination of chlorophyll a and phaeophytin a in marine and freshwater algae by fluorescence, revision 1.2. U.S. Environmental Protection Agency, Cincinnati, OH.
Austen I., T.J. Andersen, and K. Edelvang. 1999. The influence of benthic diatoms and invertebrates on the erodibility of an intertidal mudflat, the Danish Wadden Sea. Estuarine Coastal and Shelf Science 49: 99–111.
Bartzke G., K.R. Bryan, C.A. Pilditch, and K. Huhn. 2013. On the stabilizing influence of silt on sand beds. Journal of Sedimentary Research 83: 691–703.
Black K.S., T.J. Tolhurst, D.M. Paterson, and S.E. Hagerthey. 2002. Working with natural cohesive sediments. Journal of Hydraulic Engineering 128: 1–7.
Blanchard G., J.M. Guarini, F. Orvain, and G.P. Sauriau. 2001. Dynamic behavior of benthic microalgal biomass in intertidal mudflats. Journal of Experimental Marine Biology and Ecology 264: 85–100.
Brotas V., T. Cabrita, A. Portugal, J. Serôdio, and F. Catarino. 1995. Spatio-temporal distribution of the microphytobenthic biomass in intertidal flats of Tagus Estuary (Portugal). Hydrobiologia 300/301: 93–104.
Cammen L.M. 1982. Effect of particle size on organic content and microbial abundance within four marine sediment. Marine Ecology Progress Series 9: 273–280.
Ciutat A., J. Widdows, and J.W. Readman. 2006. Influence of cockle Cerastoderma edule bioturbation and tidal-current cycles on resuspension of sediment and polycyclic aromatic hydrocarbons. Marine Ecology Progress Series 328: 51–64.
Clarke K.R., and R.N. Gorley. 2006. Primer v6: user manual/tutorial. Plymouth: PRIMER-E.
Consalvey M., B. Jesus, R.G. Perkins, V. Brotas, G.J.C. Underwood, and D.M. Paterson. 2004. Monitoring migration and measuring biomass in benthic biofilms: the effects of dark/far-red adaptation and vertical migration on fluorescence measurements. Photosynthesis Research 81: 91–101.
Cummings V.J., K. Vopel, and S.F. Thrush. 2009. Terrigenous deposits in coastal marine habitats: influences on sediment geochemistry and behavior of post-settlement bivalves. Marine Ecology Progress Series 383: 173–185.
Day P. 1965. Particle fractionation and particle-size analysis. In Methods of soil analysis, ed. C.A. Black. Madison: American Society of Agronomy.
Dean W.E. 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: 242–248.
Donadi S., J. Westra, E.J. Weerman, T. van der Heide, E.M. van der Zee, J. van de Koppel, H. Olff, T. Piersma, H.W. van der Veer, and B.K. Eriksson. 2013. Non-trophic interactions control benthic producers on intertidal flats. Ecosystems 16: 1325–1335.
Doran, P.M. 1995. Fluid flow and mixing. In Bioprocess engineering principles. Elsevier Science & Technology Books.
Dubois M., K.A. Gilles, J.K. Hamilton, P.A. Rebers, and F. Smith. 1956. Colorimetric determination of sugars and related substances. Analytical Chemistry 28: 350–356.
Eckman J.E. 1985. Flow disruption by an animal-tube mimic affects sediment bacterial colonization. Journal of Marine Research 43: 419–435.
Ellis J., V. Cummings, J.E. Hewitt, S.F. Thrush, and A. Norkko. 2002. Determining effects of suspended sediment on condition of a suspension feeding bivalve (Atrina zelandica): results of a survey, a laboratory experiment and a field transplant experiment. Journal of Experimental Marine Biology and Ecology 276: 147–174.
Fagherazzi S., L. Carniello, L. D’Alpaos, and A. Defina. 2006. Critical bifurcation of shallow microtidal landforms in tidal flats and salt marshes. Proceedings of the National Academy of Sciences 103: 8337–8341.
Fagherazzi S., C. Palermo, M.C. Rulli, L. Carniello, and A. Defina. 2007. Wind waves in shallow microtidal basins and the dynamic equilibrium of tidal flats. Journal of Geophysical Research 112: F02024. doi:10.1029/2006JF000572.
Friend P.L., P. Ciavola, S. Cappucci, and R. Santos. 2003. Bio-dependent bed parameters as a proxy tool for sediment stability in mixed habitat intertidal areas. Continental Shelf Research 23: 1899–1917.
Grabowski R.C., I.G. Droppo, and G. Wharton. 2011. Erodibility of cohesive sediment: the importance of sediment properties. Earth-Science Reviews 105: 101–120.
Green M.O., and G. Coco. 2014. Review of wave-driven sediment resuspension and transport in estuaries. Reviews of Geophysics 52: 77–117.
Heller H., and R. Keren. 2002. Anionic polyacrylamide polymers effect rheological behavior of sodium-montmorillonite suspensions. Soil Society of America Journal 66: 19–25.
Hewitt J.E., V.J. Cummings, J.I. Ellis, G. Funell, A. Norkko, T.S. Talley, and S.F. Thrush. 2003. The role of waves in the colonisation of terrestrial sediments deposited in the marine environment. Journal of Experimental Marine Biology and Ecology 290: 19–47.
Huettel M., and A. Rusch. 2000. Transport and degradation of phytoplankton in permeable sediment. Limnology and Oceanography 45: 534–549.
Hume T.M., and C.E. Herdendorf. 1988. A geomorphic classification of estuaries and its application to coastal resource management—a New Zealand example. Ocean and Shoreline Management 11: 249–274.
Hunt S., K.R. Bryan, and J.C. Mullarney. 2015. The influence of wind and waves on the existence of stable intertidal morphology in meso-tidal estuaries. Geomorphology 228: 158–174.
Jacobs W., P. Le Hir, W. Van Kesteren, and P. Cann. 2011. Erosion threshold of sand-mud mixtures. Continental Shelf Research 31: 1–18.
Jesus B., V. Brotas, L. Ribeiro, C.R. Mendes, P. Cartaxana, and D.M. Paterson. 2009. Adaptations of microphytobenthos assemblages to sediment type and tidal position. Continental Shelf Research 29: 1624–1634.
Jones H.F.E., C.A. Pilditch, D.A. Bruesewitz, and A.M. Lohrer. 2011. Sedimentary environment influences the effect of an infaunal suspension feeding bivalve on estuarine ecosystem function. PloS One 6: e27065.
Jumars P.A., and A.R.M. Nowell. 1984. Fluid and sediment dynamic effects on marine benthic community structure. American Zoologist 24: 45–55.
Kristensen E., J.M. Neto, M. Lundkvist, L. Frederiksen, M.A. Pardal, T. Valdemarsen, and M.R. Flindt. 2013. Influence of benthic macroinvertebrates on the erodibility of estuarine cohesive sediments: density- and biomass-specific responses. Estuarine Coastal and Shelf Science 134: 80–87.
Lanuru M., R. Riethmüller, C. van Bernem, and K. Heymann. 2007. The effect of bed forms (crest and trough systems) on sediment erodibility on a back-barrier tidal flat of the East Frisian Wadden Sea, Germany. Estuarine Coastal and Shelf Science 72: 603–614.
Le Hir P., W. Roberts, O. Cazaillet, M. Chrisstie, P. Bassoullet, and C. Bacher. 2000. Characterization of intertidal flat hydrodynamics. Continental Shelf Research 20: 1433–1459.
Le Hir P., Y. Monbet, and F. Orvain. 2007. Sediment erodibility in sediment transport modeling: can we account for biota effects?. Continental Shelf Research 27: 1116–1142.
Lelieveld S.D., C.A. Pilditch, and M.O. Green. 2003. Variation in sediment stability and relation to indicators of microbial abundance in the Okura Estuary, New Zealand. Estuarine Coastal and Shelf Science 57: 123–136.
Lelieveld S.D., C.A. Pilditch, and M.O. Green. 2004. Effects of deposit-feeding bivalve (Macomona liliana) density on intertidal sediment stability. New Zealand Journal of Marine and Freshwater Research 38: 115–128.
Levin S.A. 1992. The problem of pattern and scale in ecology: the Robert H MacArthur Award lecture. Ecology 73: 1974–1967.
Lumborg U., T.J. Andersen, and M. Pejrup. 2006. The effects of Hydrobia ulvae and microphytobenthos on cohesive sediment dynamics on an intertidal mudflat described by means of numerical modelling. Estuarine Coastal and Shelf Science 68: 208–220.
Miller M.C., I.N. McMace, and P.D. Komar. 1977. Threshold of sediment motion under unidirectional currents. Sedimentology 24: 507–527.
Mitchener H.J., and H. Torfs. 1996. Erosion of mud/sand mixtures. Coastal Engineering 29: 1–25.
Norkko A., S.F. Thrush, J.E. Hewitt, V.J. Cummings, J. Norkko, J.I. Ellis, G.A. Funnell, D. Schultz, and I. MacDonald. 2002. Smothering of estuarine sandflats by terrigenous clay: the role of wind-wave disturbance and bioturbation in site-dependent macrofaunal recovery. Marine Ecology Progress Series 234: 23–41.
Norkko A., R. Rosenberg, S.F. Thrush, and R.B. Whitlatch. 2006. Scale- and intensity-dependent disturbance determines the magnitude of opportunistic response. Journal of Experimental Marine Biology and Ecology 330: 195–120.
Orvain F. 2005. A model of sediment transport under the influence of surface bioturbation: generalisation to the facultative suspension-feeder Scrobicularia plana. Marine Ecology Progress Series 286: 43–56.
Orvain F., P. Le Hir, and P.G. Sauriau. 2003. A model of fluff layer erosion and subsequent bed erosion in the presence of the bioturbator Hydrobia ulvae. Journal of Marine Research 31: 823–851.
Orvain F., S. Lefebvre, J. Montepini, M. Sébire, A. Gangnery, and B. Sylvand. 2012. Spatial and temporal interaction between sediment and microphytobenthos in a temperate estuarine macro-intertidal bay. Marine Ecology Progress Series 458: 53–68.
Orvain F., K. Guizien, S. Lefebvre, M. Bréret, and C. Dupuy. 2014. Relevance of macrozoobenthic grazers to understand the dynamic behavior of sediment erodibility and microphytobenthos resuspension in sunny summer conditions. Journal of Sea Research 92: 46–55.
Panagiotopoulos I., G. Voulgaris, and M.B. Collins. 1997. The influence of clay on the threshold of movement of fine sandy beds. Coastal Engineering 32: 19–43.
Passarelli C., F. Olivier, D.M. Paterson, and C. Hubas. 2012. Impacts of biogenic structures on benthic assemblages: microbes, meiofauna, macrofauna and related ecosystem functions. Marine Ecology Progress Series 465: 85–97.
Perkins R.G., G.J.C. Underwood, V. Brotas, G. Snow, B. Jesus, and L. Ribeiro. 2001. In situ microphytobenthic primary production during low tide emersion in the Tagus Estuary, Portugal: production rates, carbon partitioning and vertical migration. Marine Ecology Progress Series 223: 101–112.
Pilditch C.A., J. Widdows, N.J. Kuhn, N.D. Pope, and M.D. Brinsley. 2008. Effects of low tide rainfall on the erodibility of intertidal cohesive sediments. Continental Shelf Research 28: 1854–1865.
Pratt D.R., C.A. Pilditch, A.M. Lohrer, and S.F. Thrush. 2013. The effects of short-term increases in turbidity on sandflat microphytobenthic productivity and nutrient fluxes. Journal of Sea Research 92: 170–177.
Pratt D.R., A.M. Lohrer, C.A. Pilditch, and S.F. Thrush. 2014. Changes in ecosystem function across sedimentary gradients in estuaries. Ecosystems 17: 182–194.
Rhoads D.C., and D.G. Young. 1970. The influence of deposit-feeding organisms on sediment stability and community trophic structure. Journal of Marine Research 28: 150–178.
Rodil I.F., A.M. Lohrer, L.D. Chiaroni, J.E. Hewitt, and S.F. Thrush. 2011. Disturbance by thin terrigenous sediment deposits: consequences for primary production and nutrient cycling. Ecological Applications 21: 416–426.
Rodil I.F., A.M. Lohrer, J.E. Hewitt, M. Townsend, S.F. Thrush, and M. Carbines. 2013. Tracking environmental stress gradients using three biotic integrity indices: advantages of a locally-developed traits-based approach. Ecological Indicators 34: 560–570.
Sandwell D.R., C.A. Pilditch, and A.M. Lohrer. 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.
Schünemann, M. and H. Kühl. 1991. A device for erosion-measurements on naturally formed, muddy sediments: the EROMES system. Report of GKSS Research Centre GKSS 91/E/18. p 28.
Soares C., and P. Sobral. 2009. Bioturbation and erodibility of sediments from the Tagus Estuary. Journal of Coastal Research SI 56: 1429–1433.
Solan M., B.J. Cardinale, A.L. Downing, A.M. Engelhardt, J.L. Ruesink, and D.S. Srivastava. 2004. Extinction and ecosystem function in the marine benthos. Science 306: 177–1180.
Sutherland T.F., P.M. Lane, C.L. Amos, and J. Downing. 2000. The calibration of optical backscatter sensors for suspended sediment of varying darkness levels. Marine Geology 162: 587–597.
Thrush S.F., R.B. Whitlatch, R.D. Pridmore, J.E. Hewitt, V.J. Cummings, and M.R. Wilkinson. 1996. Scale-dependent recolonization: the role of sediment stability in a dynamic sandflat habitat. Ecology 77: 2472–2487.
Thrush S.F., D.C. Schneider, P. Legendre, R.B. Whitlach, P.K. Dayton, J.E. Hewitt, A.H. Hines, V.J. Cummings, S.M. Lawrie, J. Grant, R.D. Pridmore, S.J. Turner, and B.H. McArdle. 1997. Scaling-up from experiments to complex ecological systems: where to next?. Journal of Experimental Marine Biology and Ecology 216: 243–254.
Thrush S.F., J.E. Hewitt, A. Norkko, P.E. Nicholls, G.A. Funnell, and J. Ellis. 2003. Habitat change in estuaries: predicting broad-scale responses of intertidal macrofauna to sediment mud content. Marine Ecology Progress Series 263: 101–112.
Thrush S.F., J.E. Hewitt, V.J. Cummings, J. Ellis, C. Hatton, A. Lohrer, and A. Norkko. 2004. Muddy waters: elevating sediment input to coastal and estuarine habitats. Frontiers in Ecology and the Environment 2: 299–306.
Ubertini M., S. Lefebvre, C. Rakotomalala, and F. Orvain. 2015. Impact of sediment grain-size and biofilm age on epipelic microphytobenthos resuspension. Journal of Experimental Marine Biology and Ecology 467: 52–64.
Underwood G.J.C., and J. Kromkamp. 1999. Primary production by phytoplankton and microphytobenthos in estuaries. Advances in Ecological Research 23: 93–153.
Underwood G.J.C., D.M. Paterson, and R.J. Parkes. 1995. The measurement of microbial carbohydrate exopolymers from intertidal sediments. Limnology and Oceanography 40: 1243–1253.
Underwood G.J.C., R.G. Perkins, M.C. Consalvey, A.R.M. Hanlon, K. Oxborough, N.R. Baker, and D.M. Paterson. 2005. Patterns in microphytobenthic primary productivity: species-specific variations in migratory rhythms and photosynthetic efficiency in mixed-species biofilms. Limnology and Oceanography 50: 755–767.
Valiela I., M. Bartholomew, A. Giblin, J. Tucker, C. Harris, P. Martinetto, M. Otter, L. Camilli, and T. Stone. 2014. Watershed deforestation and down-estuary transformations alter sources, transport, and export of suspended particles in Panamanian mangrove forests. Ecosystems 17: 96–111.
Van Colen C., S.F. Thrush, M. Vincx, and T. Ysebaert. 2013. Conditional responses of benthic communities to interference from an intertidal bivalve. PloS One 8: e65861.
van de Koppel J., P.M.J. Herman, P. Thoolen, and C.H.R. Heip. 2001. Do alternate stable states occur in natural ecosystems? Evidence form a tidal flat. Ecology 82: 3449–34461.
Verney R., J.C. Brun-Cottan, R. Lafite, J. Deloffre, and J.A. Taylor. 2006. Tidally-induced shear stress variability above intertidal mudflats. Case of the macrotidal Seine Estuary. Estuaries and Coasts 29: 653–664.
Weerman E.J., P.M.J. Herman, and J. van de Koppel. 2011. Top-down control inhibits spatial self-organization of a patterned landscape. Ecology 92: 487–495.
Weerman E.J., J. Van Belzen, M. Rietkerk, S. Temmerman, S. Kèfi, P.M.J. Herman, and J. van de Koppel. 2012. Changes in diatom patch-size distribution and degradation in a spatially self-organized intertidal mudflat ecosystem. Ecology 93: 608–618.
Widdows J., and M. Brinsley. 2002. Impact of biotic and abiotic processes on sediment dynamics and the consequences to the structure and functioning of the intertidal zone. Journal of Sea Research 48: 143–156.
Widdows J., M.D. Brinsley, P.N. Salkeld, and C.H. Lucas. 2000. Influence of biota on spatial and temporal variation in sediment erodibility and material flux on a tidal flat (Westerschelde, The Netherlands). Marine Ecology Progress Series 194: 23–37.
Widdows J., A. Blauw, C.H.R. Heip, P.M.J. Herman, C.H. Lucas, J.J. Middelburg, S. Schmidt, M.D. Brinsley, F. Twisk, and H. Verbeek. 2004. Role of physical and biological processes in sediment dynamics of a tidal flat in Westerschelde Estuary, SW Netherlands. Marine Ecology Progress Series 274: 41–56.
Widdows J., P.L. Friend, A.J. Bale, M.D. Brinslet, N.D. Pope, and C.E.L. Thompson. 2007. Inter-comparison between five devices for determining erodibility of intertidal sediments. Continental Shelf Research 27: 1174–1189.
Woodin S.A., D.S. Wethey, J.E. Hewitt, and S.F. Thrush. 2012. Small scale terrestrial clay deposits on intertidal sandflats: behavioural changes and productivity reduction. Journal of Experimental Marine Biology and Ecology 413: 184–191.
Wright L.D., L.C. Schaffner, and J.P.Y. Maa. 1997. Biological mediation of bottom boundary layer processes and sediment suspension in the lower Chesapeake Bay. Marine Geology 141: 27–50.
Yallop M.L., D.M. Paterson, and P. Wellsbury. 2000. Interrelationships between rates of microbial production, exopolymers production, microbial biomass, and sediment stability in biofilms of intertidal sediments. Microbial Ecology 39: 116–127.
Acknowledgments
We would like to thank Clarisse Niemand, Rebecca Gladstone-Gallagher, Daniel Pratt, Lisa McCartain, and Laura Haines for their aid in sample collection and Rolf Riethmüller for his support in constructing the EROMES device. We would also like to acknowledge the two anonymous reviewers for the constructive comments that have improved this manuscript. This research was funded by the University of Waikato International Doctoral Scholarship awarded to Rachel J. Harris as part of INTERCOAST, a joint research program between the Universities of Waikato and Bremen.
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Harris, R.J., Pilditch, C.A., Greenfield, B.L. et al. The Influence of Benthic Macrofauna on the Erodibility of Intertidal Sediments with Varying mud Content in Three New Zealand Estuaries. Estuaries and Coasts 39, 815–828 (2016). https://doi.org/10.1007/s12237-015-0036-2
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DOI: https://doi.org/10.1007/s12237-015-0036-2