Abstract
Burrowing benthic animals belonging to the same functional group may produce species-specific effects on microbially mediated nitrogen (N) processes depending upon different ecological traits. We investigated the effects of two tube-dwelling organisms, amphipods (Corophium insidiosum) and chironomid larvae (Chironomus plumosus), on benthic N cycling in bioturbated estuarine sediments. Aims of this work were to analyze the interactions among burrowers and N-related microbial processes in two distinct sedimentary environments colonized by benthic animals with different ecological traits. We hypothesized higher rates of nitrification and higher coupled nitrification–denitrification in sediments with C. insidiosum due to continuous ventilation rates. We expected higher denitrification of water column nitrate in sediments with C. plumosus due to lower and intermittent ventilation activity and lower oxygen levels in burrows. To this purpose, we combined process–specific (nitrification and denitrification) with net N flux measurements in intact and reconstructed sediments. Sediments with C. insidiosum had higher rates of oxygen demand and of potential nitrification and higher concentration of pore water NH4+ as compared to sediments with C. plumosus. Sediments with both species displayed comparable net N2 fluxes, mostly sustained by respiration of water column NO3− in sediments with chironomid larvae and by NO3− produced within sediments in sediments with corophiid amphipods. Corophium insidiosum stimulated nitrification nearly 15-fold more as compared to C. plumosus. Overall, our results demonstrate that sediments with burrowing fauna may display similar rates of denitrification, but underlying mechanisms may deeply vary and be species-specific.
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Bartoli, M., D. Nizzoli, D. T. Welsh & P. Viaroli, 2000. Short-term influence of recolonisation by the polychaete worm Nereis succinea on oxygen and nitrogen fluxes and denitrification: a microcosm simulation. Hydrobiologia 431: 165–174.
Bartoli, M., G. Castaldelli, D. Nizzoli & P. Viaroli, 2012. Benthic primary production and bacterial denitrification in a Mediterranean eutrophic coastal lagoon. Journal of Experimental Marine Biology and Ecology 438: 41–51.
Belser, L. W. & E. L. Mays, 1980. Specific inhibition of nitrite oxidation by chlorate and its use in assessing nitrification in soils and sediments. Applied Environmental Microbiology 39: 505–510.
Bower, C. E. & T. Holm-Hansen, 1980. A salicylate-hypochlorite method for determining ammonia in seawater. Canadian Journal of Fish and Aquatic Science 37: 794–798.
Brand, A., J. Lewandowski, E. Hamann & G. Nützmann, 2013. Advection around ventilated U-shaped burrows: a model study. Water Resources Research 49: 2907–2917.
Brin, L. D., A. E. Giblin & J. J. Rich, 2014. Environmental controls of anammox and denitrification in southern New England estuarine and shelf sediments. Limnology and Oceanography 59: 851–860.
Burgin, A. J. & S. K. Hamilton, 2007. Have we overemphasized the role of denitrification in aquatic ecosystems? A review of nitrate removal pathways. Frontiers in Ecology and the Environment 5: 89–96.
Cornwell, J. C., W. M. Kemp & T. M. Kana, 1999. Denitrification in coastal ecosystems: methods, environmental controls, and ecosystem level controls, a review. Aquatic Ecology 33: 41–55.
Dalsgaard, T., L.P. Nielsen, V. Brotas & et al., 2000. Protocol handbook for NICE-nitrogen cycling in estuaries: a project under the EU research programme. In: Marine Science and Technology (MAST III), National Environmental Research Institute, Silkeborg.
Dollhopf, S. L., J. H. Hyun, A. C. Smith, H. J. Adams, S. O’Brien & J. E. Kostka, 2005. Quantification of ammonium-oxidizing bacteria and factors controlling nitrification in salt marsh sediments. Applied Environmental Microbiology 71: 240–246.
Eyre, B. D. & A. J. P. Ferguson, 2009. Denitrification efficiency for defining critical loads of carbon in shallow coastal ecosystems. Hydrobiologia 629: 137–146.
Fulweiler, R. W., E. M. Heiss, M. K. Rogener, M. K. Rogener, S. E. Newell, G. R. LeCleir, S. M. Kortebein & S. W. Wilhelm, 2015. Examining the impact of acetylene on N-fixation and the active sediment microbial community. Frontiers in Microbiology 6: 418.
Gamble, J. C., 1970. Anaerobic survival of the crustaceans Corophium volutator, C. arenarium and Tanais chevreuxi. Journal of the Marine Biological Association of the United Kingdom 50: 657–671.
Gasiūnaitė, Z. R., D. Daunys, S. Olenin & A. Razinkovas, 2008. The Curonian lagoon. In Schiewer, U. (ed.), Ecology of Baltic coastal waters. Springer, Berlin: 197–215.
Grasshoff, K., M. Ehrhardt & K. Kremling, 1983. Methods of seawater analysis, 2nd ed. Berlin, Wiley.
Gutiérrez, J. L. & C. G. Jones, 2006. Physical ecosystem engineers as agents of biogeochemical heterogeneity. Bioscience 56: 227–236.
Henriksen, K., J. I. Hansen & T. H. Blackburn, 1981. Rates of nitrification, distribution of nitrifying bacteria, and nitrate fluxes in different types of sediment from Danish waters. Marine Biology 61: 299–304.
Hölker, F., M. J. Vanni, J. J. Kuiper, et al., 2015. Tube-dwelling invertebrates: tiny ecosystem engineers have large effects in lake ecosystems. Ecological Monographs 85: 333–351.
Kajan, R. & P. Frenzel, 1999. The effect of chironomid larvae on production, oxidation and fluxes of methane in a flooded rice soil. FEMS Microbiology Ecology 28: 121–129.
Kana, T. M., C. Darkangelo, D. Hunt, J. B. Oldham, G. E. Bennett & J. C. Cornwell, 1994. A membrane inlet mass spectrometer for rapid high-precision determination of N2, O2, and Ar in environmental water samples. Analytical Chemistry 66: 4166–4170.
Kristensen, E., 2000. Organic matter diagenesis at the oxic/anoxic interface in coastal marine sediments, with emphasis on the role of burrowing animals. Hydrobiologia 426: 1–24.
Kristensen, E. & K. Hansen, 1999. Transport of carbon dioxide and ammonium in bioturbated (Nereis diversicolor) coastal, marine sediments. Biogeochemistry 45: 147–168.
Kristensen, E., M. H. Jensen & R. C. Aller, 1991. Direct measurement of dissolved inorganic nitrogen exchange and denitrification in individual polychaete (Nereis virens) burrows. Journal of Marine Research 49: 355–377.
Kristensen, E., G. Penha-Lopes, M. Delefosse, T. Valdemarsen, C. O. Quintana & G. T. Banta, 2012. What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Marine Ecology Progress Series 446: 285–302.
Lewandowski, J., C. Laskov & M. Hupfer, 2007. The relationship between Chironomus plumosus burrows and the spatial distribution of pore-water phosphate, iron and ammonium in lake sediments. Freshwater Biology 52: 331–343.
Mayer, M. S., L. Schaffner & W. M. Kemp, 1995. Nitrification potentials of benthic macrofaunal tubes and burrow walls: effects of sediment NH4 + and animal irrigation behaviour. Marine Ecology Progress Series 121: 157–169.
Mermillod-Blondin, F., R. Rosenberg, F. François-Carcaillet, K. Norling & L. Mauclaire, 2004. Influence of bioturbation by three benthic infaunal species on microbial communities and biogeochemical processes in marine sediment. Aquatic Microbial Ecology 36: 271–284.
Møller, L. F. & H. U. Riisgård, 2006. Filter feeding in the burrowing amphipod Corophium volutator. Marine Ecology Progress Series 322: 213–224.
Murphy, A. E., D. Nizzoli, M. Bartoli, A. R. Smyth, G. Castaldelli & I. C. Anderson, 2018. Variation in benthic metabolism and nitrogen cycling across clam aquaculture sites. Marine Pollution Bulletin 127: 524–535.
Nielsen, L. P., 1992. Denitrification in sediment determined from nitrogen isotope paring. FEMS Microbiology Ecology 86: 357–362.
Nizzoli, D., M. Bartoli, M. Cooper, D. T. Welsh, G. J. C. Underwood & P. Viaroli, 2007. Implications for oxygen, nutrient fluxes and denitrification rates during the early stage of sediment colonisation by the polychaete Nereis spp. in four estuaries. Estuarine, Coastal and Shelf Science 75: 125–134.
Pelegrí, S. P. & T. H. Blackburn, 1994. Bioturbation effects of the amphipod Corophium volutator on microbial nitrogen transformations in marine sediments. Marine Biology 121: 253–258.
Pelegrí, S. P. & T. H. Blackburn, 1995a. Effects of Tubifex tubifex (Oligochaeta: Tubificidae) on N-mineralization in freshwater sediments, measured with 15N isotopes. Aquatic Microbial Ecology 9: 289–294.
Pelegrí, S. P. & T. H. Blackburn, 1995b. Effect of bioturbation by Nereis sp., Mya arenaria and Cerastoderma sp. on nitrification and denitrification in estuarine sediments. Ophelia 42: 289–299.
Pelegrí, S. P. & T. H. Blackburn, 1996. Nitrogen cycling in lake sediments bioturbated by Chironomus plumosus larvae, under different degrees of oxygenation. Hydrobiologia 325: 231–238.
Riisgård, H. U., 2007. Biomechanics and energy cost of the amphipod Corophium volutator filter-pump. Biological Bulletin 212: 104–114.
Roskosch, A., M. R. Morad, A. Khalili & J. Lewandowski, 2010. Bioirrigation by Chironomus plumosus: advective flow investigated by particle image velocimetry. Journal of North American Benthological Society 29: 789–802.
Rysgaard, S., N. Risgaard-Petersen, L. P. Nielsen & N. P. Revsbech, 1993. Nitrification and denitrification in lake and estuarine sediments measured by the 15N dilution technique and isotope pairing. Applied Environmental Microbiology 59: 2093–2098.
Rysgaard, S., N. Risgaard-Petersen, N. P. Sloth, K. Jensen & L. P. Nielsen, 1994. Oxygen regulation of nitrification and denitrification in freshwater sediments. Limnology and Oceanography 39: 1643–1652.
Rysgaard, S., P. B. Christensen & L. P. Nielsen, 1995. Seasonal variation in nitrification and denitrification in estuarine sediment colonized by benthic microalgae and bioturbating infauna. Marine Ecology Progress Series 126: 111–121.
Sloth, N. P., L. P. Nielsen & T. H. Blackburn, 1992. Nitrification in sediment cores measured with acetylene inhibition. Limnology and Oceanography 37: 1108–1112.
Steingruber, S. M., J. Friedrich, R. Gächter & B. Wehrli, 2001. Measurement of denitrification in sediments with the 15N isotope pairing technique. Applied Environmental Microbiology 67: 3771–3778.
Stief, P., 2013. Stimulation of microbial nitrogen cycling in aquatic ecosystems by benthic macrofauna: mechanisms and environmental implications. Biogeosciences 10: 7829–7846.
Stief, P. & D. de Beer, 2002. Bioturbation effects of Chironomus riparius on the benthic N-cycle as measured using microsensors and microbiological assays. Aquatic Microbial Ecology 27: 175–185.
Stief, P. & D. de Beer, 2006. Probing the microenvironment of freshwater sediment macrofauna: implications of deposit-feeding and bioirrigation for nitrogen cycling. Limnology and Oceanography 51: 2538–2548.
Stief, P., M. Poulsen, L. P. Nielsen, H. Brix & A. Schramm, 2009. Nitrous oxide emission by aquatic macrofauna. Proceedings of the National Academy of Sciences 106: 4296–4300.
Stocum, E. T. & C. J. Plante, 2006. The effect of artificial defaunation on bacterial assemblages of intertidal sediments. Journal of Experimental Marine Biology and Ecology 337: 147–158.
Strauss, E. A., N. L. Mitchel & G. A. Lamberti, 2002. Factors regulating nitrification in aquatic sediments: effects of organic carbon, nitrogen availability, and pH. Canadian Journal of Fish and Aquatic Science 59: 554–563.
Svensson, J. M., 1997. Influence of Chironomus plumosus L. on ammonium flux and denitrification (measured by the acetylene blockage- and the isotope pairing-technique) eutrophic lake sediment. Hydrobiologia 346: 157–168.
Svensson, J. M., A. Enrich-Prast & L. Leonardson, 2001. Nitrification and denitrification in a eutrophic lake sediment bioturbated by oligochaetes. Aquatic Microbial Ecology 23: 177–186.
Tuominen, L., K. Mäkelä, K. K. Lehtonen, H. Haahti, S. Hietanen & J. Kuparinen, 1999. Nutrient fluxes, porewater profiles and denitrification in sediment influenced by algal sedimentation and bioturbation by Monoporeia. Estuarine, Coastal and Shelf Science 49: 83–97.
Viaroli, P., G. Giordani, M. Bartoli, M. Naldi, R. Azzoni, D. Nizzoli, I. Ferrari, J. M. Zaldìvar, S. Bencivelli, G. Castaldelli & E. A. Fano, 2006. The Sacca di Goro lagoon and an arm of the Po River. In Wangersky, P. J. (ed.), The Handbook of Environmental Chemistry, Estuaries, Vol. 5. Springer, Berlin: 197–232.
Waldbusser, G. G. & R. L. Marinelli, 2006. Macrofaunal modification of porewater advection: role of species function, species interaction, and kinetics. Marine Ecology Progress Series 311: 217–231.
Weiss, R. F., 1970. The solubility of nitrogen, oxygen and argon in water and seawater. Deep Sea Research and Oceanographic Abstracts 17: 721–735.
Zettler, M. L. & D. Daunys, 2007. Long-term macrozoobenthos changes in a shallow boreal lagoon: comparison of a recent biodiversity inventory with historical data. Limnologica 37: 107–185.
Zhang, L., X. Gu, C. Fan, J. Shang, Q. Shen, Z. Wang & J. Shen, 2010. Impact of different benthic animals on phosphorus dynamics across the sediment-water interface. Journal of Environmental Science 22: 1674–1682.
Zilius, M., G. Giordani, J. Petkuviene, I. Lubiene, T. Ruginis & M. Bartoli, 2015. Phosphorus mobility under short-term anoxic conditions in two shallow eutrophic coastal systems (Curonian and Sacca di Goro lagoons). Estuarine, Coastal and Shelf Science 164: 134–146.
Acknowledgements
Paula Carpintero Moraes was supported by Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq-Brasil). Mindaugas Zilius and Marco Bartoli were partly supported by the BONUS project “Nutrient Cocktails in Coastal zones of the Baltic Sea (COCOA)” (No. BONUS-2/2014). We kindly acknowledge Irma Vybernaite-Lubiene and Tomas Ruginis for assistance in laboratory analysis.
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Carpintero Moraes, P., Zilius, M., Benelli, S. et al. Nitrification and denitrification in estuarine sediments with tube-dwelling benthic animals. Hydrobiologia 819, 217–230 (2018). https://doi.org/10.1007/s10750-018-3639-3
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DOI: https://doi.org/10.1007/s10750-018-3639-3