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Spatially variable effects of a marine pest on ecosystem function

  • Ecosystem ecology - Original research
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Abstract

The broad spectrum of anthropogenic pressures on many of the world’s coastal bays and estuaries rarely act in isolation, yet few studies have directly addressed the interactive effects of multiple pressures. Port Phillip Bay in southeastern Australia is a semi-enclosed bay in which nutrient management is a major concern. In recent years it has been heavily invaded by marine pests. We manipulated the density of one such invader, the European fanworm Sabella spallanzanii, and showed that it causes changes in the composition of macrofauna in the surrounding sediments, provides habitat for epibiota (both fauna and flora) on Sabella tubes, and reduces the biomass of microphytobenthos on the surrounding sediments. Of greatest concern, however, was the indirect impact on nutrient cycling. We suggest that the impacts on nutrient cycling are largely due to the feeding of Sabella and the epifauna on its tubes, capturing organic N before it reaches the sediment, excreting it back up into the water column as NH4, thereby bypassing sedimentary processes such as denitrification. Most notably, the efficiency of denitrification, the key ecosystem process that permanently removes N from the system, fell by 37–53 % in the presence of Sabella. Importantly though, this study also demonstrated significant spatial variability in fauna, geochemistry and the magnitude of Sabella effects. Given that the effect of Sabella is also likely to vary in time and with changes in density, all of these sources of variability need to be considered when incorporating the effects of Sabella in nutrient management strategies.

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References

  • Aller RC (1982) The effects of macrobenthos on chemical properties of marine sediment and overlying water. In: McCall PL, Tevesz MJS (eds) Animal-sediment relations. Plenum, New York, pp 53–102

    Google Scholar 

  • Aller RC, Yingst JY (1985) Effects of the marine deposit-feeders Heteromastus filiformis (Polychaeta), Macoma balthica (Bivalvia), and Tellina texana (Bivalvia) on averaged sedimentary solute transport, reaction-rates, and microbial distributions. J Mar Res 43:615–645

    Article  CAS  Google Scholar 

  • Alpine AE, Cloern JE (1992) Trophic interactions and direct physical effects control phytoplankton biomass and production in an estuary. Limnol Oceanogr 37:946–955

    Article  Google Scholar 

  • An S, Joye SB (2001) Enhancement of coupled nitrification–denitrification by benthic photosynthesis in shallow estuarine sediments. Limnol Oceanogr 46:62–74

    Article  CAS  Google Scholar 

  • Anderson MJ, Gorley RN, Clarke KR (2008) PERMANOVA+ for PRIMER: guide to software and statistical methods. PRIMER-E, Plymouth

    Google Scholar 

  • Beardall J, Light B (1997) Microphytobenthos in Port Phillip Bay: distribution and primary productivity. Port Phillip Bay technical report no. 30, Melbourne

  • Boynton WR, Garber JH, Summers R, Kemp WM (1995) Inputs, transformations, and transport of nitrogen and phosphorus in Chesapeake Bay and selected tributaries. Estuaries 18:285–314

    Article  CAS  Google Scholar 

  • Carey JM, Watson JE (1992) Benthos of the muddy bottom habitat of the Geelong Arm of Port Phillip Bay, Victoria, Australia. Vic Nat 109:196–202

    Google Scholar 

  • Carlton JT, Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261:78–82

    Article  Google Scholar 

  • Clapin G (1996) The filtration rate, oxygen consumption and biomass of the introduced polychaete Sabella spallanzanii Gmelin within Cockburn Sound: can it control phytoplankton levels and is it an efficient filter feeder? Honours thesis, Edith Cowan University

  • Cloern JE (2007) Habitat connectivity and ecosystem productivity: implications from a simple model. Am Nat 169:E21–E33

    Article  PubMed  Google Scholar 

  • Cohen BF, Currie DR, McArthur MA (2000) Epibenthic community structure in Port Phillip Bay, Victoria, Australia. Mar Freshwater Res 51:689–702

    Article  Google Scholar 

  • Cornwell JC, Kemp WM, Kana TM (1999) Denitrification in coastal ecosystems: methods, environmental controls, and ecosystems level controls, a review. Aquat Ecol 33:41–54

    Article  CAS  Google Scholar 

  • Crain CM, Kroeker K, Halpern BS (2008) Interactive and cumulative effects of multiple human stressors in marine systems. Ecol Lett 11:1304–1315

    Article  PubMed  Google Scholar 

  • Crain CM, Halpern BS, Beck MW, Kappel CV (2009) Understanding and managing human threats to the coastal marine environment. Ann N Y Acad Sci 1162:39–62

    Google Scholar 

  • Eyre BD, Maher D (2011) Mapping ecosystem processes and function across shallow seascapes. Cont Shelf Res 31:S162–S172

    Article  Google Scholar 

  • Eyre BD, Rysgaard S, Dalsgaard T, Christensen PB (2002) Comparison of isotope pairing and N-2: Ar methods for measuring sediment-denitrification-assumptions, modifications, and implications. Estuaries 25:1077–1087

    Article  CAS  Google Scholar 

  • Eyre BD, Maher D, Oakes JM, Erler DV, Glasby TM (2011) Differences in benthic metabolism, nutrient fluxes, and denitrification in Caulerpa taxifolia communities compared to uninvaded bare sediment and seagrass (Zostera capricorni) habitats. Limnol Oceanogr 56:1737–1750

    CAS  Google Scholar 

  • Forster S, Graf G (1995) Impact of irrigation on oxygen flux into the sediment: intermittent pumping by Callianassa subterranea and “piston pumping” by Lanice conchilega. Mar Biol 123:335–246

    Google Scholar 

  • Gibbs M, Funnell G, Pickmere S, Norkko A, Hewitt J (2005) Benthic nutrient fluxes along an estuarine gradient: influence of the pinnid bivalve Atrina zelandica in summer. Mar Ecol Prog Ser 288:151–164

    Article  Google Scholar 

  • Halpern BS, Kappel CV, Selkoe KA, Micheli F, Ebert CM, Kontgis C, Crain CM, Martone RG, Shearer C, Teck SJ (2009) Mapping cumulative human impacts to California Current marine ecosystems. Conserv Lett 2:138–148

    Article  Google Scholar 

  • Halpern BS, Longo C, Hardy D, McLeod KL, Samhouri JF, Katona SK, Kleisner K, Lester SE, O’Leary J, Ranelletti M, Rosenberg AA, Scarborough C, Selig ER, Best BD, Brumbaugh DR, Chapin FS, Crowder LB, Daly KL, Doney SC, Elfes C, Fogarty MJ, Gaines SD, Jacobsen KI, Karrer LB, Leslie HM, Neeley E, Pauly D, Polasky S, Ris B, Martin KS, Stone GS, Sumaila UR, Zeller D (2012) An index to assess the health and benefits of the global ocean. Nature. doi:10.1038/nature11397

  • Harris GP, Batley G, Fox D, Hall D, Jernakoff P, Molloy R, Murray A, Newell B, Parslow J, Skyring G, Walker S (1996) Port Phillip Bay Environmental Study: final report. CSIRO, Dickson, ACT, Australia

  • Heggie DT, Skyring GW, Orchardo J, Longmore AR, Nicholson GJ, Berelson WM (1999) Denitrification and denitrifying efficiencies in sediments of Port Phillip Bay: direct determinations of biogenic N-2 and N-metabolite fluxes with implications for water quality. Mar Freshwater Res 50:589–596

    Article  CAS  Google Scholar 

  • Henriksen K, Blackburn TH, Lomstein BA, McRoy CP (1993) Rates of nitrification, distribution of nitrifying bacteria and inorganic n fluxes in Northern Bering Chukchi shelf sediments. Cont Shelf Res 13:629–651

    Article  Google Scholar 

  • Herbert RA (1999) Nitrogen cycling in coastal marine ecosystems. FEMS Microbiol Rev 23:563–590

    Article  PubMed  CAS  Google Scholar 

  • Hewitt CL, Campbell ML, Thresher RE, Martin RB, Boyd S, Cohen BF, Currie DR, Gomon MF, Keough MJ, Lewis JA, Lockett MM, Mays N, McArthur MA, O’Hara TD, Poore GCB, Ross DJ, Storey MJ, Watson JE, Wilson RS (2004) Introduced and cryptogenic species in Port Phillip Bay, Victoria, Australia. Mar Biol 144:183–202

    Article  Google Scholar 

  • Hietanen S, Laine AO, Lukkari K (2007) The complex effects of the invasive polychaetes Marenzelleria spp. on benthic nutrient dynamics. J Exp Mar Biol Ecol 352:89–102

    Article  CAS  Google Scholar 

  • Howarth RW, Marino R (2006) Nitrogen as the limiting nutrient for eutrophication in coastal marine ecosystems: evolving views over three decades. Limnol Oceanogr 51:364–376

    Article  CAS  Google Scholar 

  • Huettel M, Gust G (1992) Solute release mechanisms from confined sediment cores in stirred benthic chambers and flume flows. Mar Ecol Prog Ser 82:187–197

    Article  Google Scholar 

  • Hughes TP, Connell JH (1999) Multiple stressors on coral reefs: a long-term perspective. Limnol Oceanogr 44:932–940

    Article  Google Scholar 

  • Kana TM, Darkangelo C, Hunt MD, Oldham JB, Bennett GE, Cornwell JC (1994) Membrane inlet mass-spectrometer for rapid high-precision determination of N-2, O-2, and Ar in environmental water samples. Anal Chem 66:4166–4170

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Kristensen E, Blackburn TH (1987) The fate of organic carbon and nitrogen in experimental marine sediment systems: influence of bioturbation and anoxia. J Mar Res 45:231–257

    Article  CAS  Google Scholar 

  • Kristensen E, Jensen MH, Aller RC (1991) Direct measurement of dissolved inorganic nitrogen exchange and denitrification in individual polychaete (Nereis virens) burrows. J Mar Res 49:355–377

    Article  CAS  Google Scholar 

  • Lambert WJ, Levin D, Berman J (1992) Changes in the structure of a New England (USA) kelp bed: the effects of an introduced species. Mar Ecol Prog Ser 88:303–307

    Article  Google Scholar 

  • Lavrentyev PJ, Gardner WS, Yang LY (2000) Effects of the zebra mussel on nitrogen dynamics and the microbial community at the sediment–water interface. Aquat Microb Ecol 21:187–194

    Article  Google Scholar 

  • Lemmens JWTJ, Clapin G, Lavery P, Cary J (1996) Filtering capacity of seagrass meadows and other habitats of Cockburn Sound, Western Australia. Mar Ecol Prog Ser 143:187–200

    Article  Google Scholar 

  • Lenihan HS, Peterson CH, Kim SL, Conlan KE, Fairey R, McDonald C, Grabowski JH, Oliver JS (2003) Variation in marine benthic community composition allows discrimination of multiple stressors. Mar Ecol Prog Ser 261:63–73

    Article  Google Scholar 

  • Lillebo AI, Flindt MR, Pardal MA, Marques JC (1999) The effect of macrofauna, meiofauna add microfauna on the degradation of Spartina maritima detritus from a salt marsh area. Acta Oecol Int J Ecol 20:249–258

    Article  Google Scholar 

  • Lohrer AM, Thrush SF, Gibbs MM (2004) Bioturbators enhance ecosystem function through complex biogeochemical interactions. Nature 431:1092–1095

    Article  PubMed  CAS  Google Scholar 

  • Lohrer AM, Thrush SF, Hunt L, Hancock N, Lundquist C (2005) Rapid reworking of subtidal sediments by burrowing spatangoid urchins. J Exp Mar Biol Ecol 321:155–169

    Article  Google Scholar 

  • Longmore A, Nicholson G, Parry G (1996) The effect of Sabella spallanzanii on nitrogen cycling in Port Phillip Bay, a report to the Centre for Research on Introduced Marine Pests, CSIRO Division of Fisheries. Victorian Fisheries Research Institute, Queenscliff. Internal report no. 219

  • McCook LJ (1999) Macroalgae, nutrients and phase shifts on coral reefs: scientific issues and management consequences for the Great Barrier Reef. Coral Reefs 18:357–367

    Article  Google Scholar 

  • Mora C, Metzger R, Rollo A, Myers RA (2007) Experimental simulations about the effects of overexploitation and habitat fragmentation on populations facing environmental warming. Proc R Soc B Biol Sci 274:1023–1028

    Article  Google Scholar 

  • Murray AG, Parslow JS (1999) Modelling of nutrient impacts in Port Phillip Bay—a semi-enclosed marine Australian ecosystem. Mar Freshwater Res 50:597–611

    Article  CAS  Google Scholar 

  • Newell RIE, Cornwell JC, Owens MS (2002) Influence of simulated bivalve biodeposition and microphytobenthos on sediment nitrogen dynamics: a laboratory study. Limnol Oceanogr 47:1367–1379

    Article  Google Scholar 

  • Nichols FH, Thompson JK, Schemel LE (1990) Remarkable invasion of San Francisco Bay (California, USA) by the Asian clam Potamocorbula amurensis. II. Displacement of a former community. Mar Ecol Prog Ser 66:95–101

    Article  Google Scholar 

  • Nicholson GJ, Longmore AR (1999) Causes of observed temporal variability of nutrient fluxes from a southern Australian marine embayment. Mar Freshwater Res 50:581–588

    Article  CAS  Google Scholar 

  • Nicholson GJ, Longmore AR, Berelson WM (1999) Nutrient fluxes measured by two types of benthic chamber. Mar Freshwater Res 50:567–572

    Article  CAS  Google Scholar 

  • Nixon SW, Ammerman JW, Atkinson LP, Berounsky VM, Billen G, Boicourt WC, Boynton WR, Church TM, Ditoro DM, Elmgren R, Garber JH, Giblin AE, Jahnke RA, Owens NJP, Pilson MEQ, Seitzinger SP (1996) The fate of nitrogen and phosphorus at the land sea margin of the North Atlantic Ocean. Biogeochemistry 35:141–180

    Article  CAS  Google Scholar 

  • O’Brien A (2003) Effects of the introduced polychaete Sabella spallanzanii on soft sediment assemblages. Honours, The University of Melbourne

  • O’Brien AL, Ross DJ, Keough MJ (2006) Effects of Sabella spallanzanii physical structure on soft sediment macrofaunal assemblages. Mar Freshwater Res 57:363–371

    Article  Google Scholar 

  • O’Leary T, Leeming R, Nichols PD, Volkman JK (1994) The distributions and concentrations of biomarkers for sewage, primary producers and bacteria in the major sediment types of Port Phillip Bay, technical report no. 17. CSIRO Institute of Natural Resources and Environment, Port Phillip Bay Environmental Study

  • Ormerod SJ, Dobson M, Hildrew AG, Townsend CR (2010) Multiple stressors in freshwater ecosystems. Freshwater Biol 55:1–4

    Article  Google Scholar 

  • Parry GD, Lockett MM, Crookes DP, Coleman N, Sinclair M (1996) Mapping and distribution of Sabella spallanzanii in Port Phillip Bay. Project 94/164, Queenscliff

  • 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 105:285–290

    Article  Google Scholar 

  • Peterson CH, Summerson HC, Thomson E, Lenihan HS, Grabowski J, Manning L, Micheli F, Johnson G (2000) Synthesis of linkages between benthic and fish communities as a key to protecting essential fish habitat. Bull Mar Sci 66:759–774

    Google Scholar 

  • Probst TA, Crawford CM (2008) Population characteristics and planktonic larval stage of the New Zealand screwshell Maoricolpus roseus. J Mollusc Stud 74:191–197

    Article  Google Scholar 

  • Risgaard-Peterson N, Rysgaard S, Nielsen LP, Revsbech NP (1994) Diurnal-variation of denitrification and nitrification in sediments colonized by benthic microphytes. Limnol Oceanogr 39:573–579

    Article  Google Scholar 

  • Ross DJ, Johnson CR, Hewitt CL (2002) Impact of introduced seastars Asterias amurensis on survivorship of juvenile commercial bivalves Fulvia tenuicostata. Mar Ecol Prog Ser 241:99–112

    Article  Google Scholar 

  • Ross DJ, Johnson CR, Hewitt CL (2003) Variability in the impact of an introduced predator (Asterias amurensis: Asteroidea) on soft-sediment assemblages. J Exp Mar Biol Ecol 288:257–278

    Article  Google Scholar 

  • Ruiz GM, Fofonoff P, Hines AH, Grosholz ED (1999) Non-indigenous species as stressors in estuarine and marine communities: assessing invasion impacts and interactions. Limnol Oceanogr 44:950–972

    Article  Google Scholar 

  • Rysgaard S, Thamdrup B, Risgaard-Petersen N, Fossing H, Berg P, Christensen PB, Dalsgaard T (1998) Seasonal carbon and nutrient mineralization in a high-Arctic coastal marine sediment, Young Sound, Northeast Greenland. Mar Ecol Prog Ser 175:261–276

    Article  CAS  Google Scholar 

  • Smith VH, Joye SB, Howarth RW (2006) Eutrophication of freshwater and marine ecosystems. Limnol Oceanogr 51:351–355

    Article  CAS  Google Scholar 

  • Steneck RS, Carlton JT (2001) Human alterations of marine communities—students beware! In: Bertness MD, Gaines SD, Hay ME (eds) Marine community ecology. Sinauer, Sunderland, pp 445–468

    Google Scholar 

  • Strickland JD, Parson TR (1972) A practical handbook of seawater analysis. Bulletin Fisheries Research Board of Canada, Ottawa

  • Sundback K, Graneli W (1988) Influence of microphytobenthos on the nutrient flux between sediment and water—a laboratory study. Mar Ecol Prog Ser 43:63–69

    Article  Google Scholar 

  • Sundback K, Enoksson V, Graneli W, Pettersson K (1991) Influence of sublittoral microphytobenthos on the oxygen and nutrient flux between sediment and water—a laboratory continuous-flow study. Mar Ecol Prog Ser 74:263–279

    Article  Google Scholar 

  • Vopel K, Thistle D, Rosenberg R (2003) Effect of the brittle star Amphiura filiformis (Amphiuridae, Echinodermata) on oxygen flux into the sediment. Limnol Oceanogr 48:2034–2045

    Article  CAS  Google Scholar 

  • Walton WC, MacKinnon C, Rodriguez LF, Proctor C, Ruiz GA (2002) Effect of an invasive crab upon a marine fishery: green crab, Carcinus maenas, predation upon a venerid clam, Katelysia scalarina, in Tasmania (Australia). J Exp Mar Biol Ecol 272:171–189

    Article  Google Scholar 

  • Wiltshire KH (1992) The influence of microphytobenthos on oxygen and nutrient fluxes between eulittoral sediments and associated water phases in the Elbe Estuary. In: Colombo G, Ferrari I, Ceccherilli VU, Rossi R (eds) Marine eutrophication and population dynamics. Proceedings of the 25th European Marine Biology Symposium. Olsen and Olsen, Fredensborg, pp 63–70

  • Windham L, Ehrenfeld JG (2003) Net impact of a plant invasion on nitrogen-cycling processes within a brackish tidal marsh. Ecol Appl 13:883–896

    Article  Google Scholar 

  • Young OR, Osherenko G, Ogden J, Crowder LB, Wilson JA, Day JC, Douvere F, Ehler CN, McLeod KL, Halperin BS, Peach R (2007) Solving the crisis in ocean governance: place-based management of marine ecosystems. Environment 49:20–32

    Article  Google Scholar 

  • Zann IP (1995) State of the marine environment for Australia, Great Barrier Reef Marine Park Authority for Ocean Rescue 2000

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Acknowledgments

We thank Allyson O’Brien, Dustin Marshall, Prue Addison and Sarah Metcalf for assisting with field work and Mr Gus Fabris, Department of Primary Industries Victoria, Queenscliff for conducting nutrient analysis. This work was supported by the Australian Research Council Linkage grant (LP0211152) to M. J. Keough and A. R. Longmore. We thank the Department of Primary Industries and the Department of Sustainability and Environment for financial and in-kind assistance.

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  1. Department of Zoology, University of Melbourne, Melbourne, VIC, 3010, Australia

    D. Jeff Ross & Michael J. Keough

  2. Institute for Marine and Antarctic Studies, University of Tasmania, Private Bag 49, Hobart, TAS, 7001, Australia

    D. Jeff Ross

  3. Department of Primary Industries, Fisheries Research Branch, Bellarine Highway, Queenscliff, VIC, 3225, Australia

    Andy R. Longmore

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  1. D. Jeff Ross
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Correspondence to D. Jeff Ross.

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Communicated by Pete Peterson.

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Ross, D.J., Longmore, A.R. & Keough, M.J. Spatially variable effects of a marine pest on ecosystem function. Oecologia 172, 525–538 (2013). https://doi.org/10.1007/s00442-012-2497-3

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