Abstract
This study investigated the effects of the invasive polychaete Marenzelleria viridis (Marenzelleria) on the biogeochemistry of sandy marine sediments. A 27-day microcosm experiment was conducted to evaluate net microbial reactions, fluxes and porewater profiles of key solutes under the presence of Marenzelleria in two sediment types; one containing autochthonous organic matter (0.4 %) and another slightly amended with seagrass detritus (Ruppia maritima; 0.5 %). Fluxes of TCO2 and O2 were two- to three-fold increased in the presence of Marenzelleria and were higher in amended (256 mmol m−2 d−1) than in non-amended sediments (117 mmol m−2 d−1). Marenzelleria stimulated carbon degradation and sulfate reduction in both sediment treatments by influencing porewater chemistry and DOC availability. Marenzelleria flushed out inhibitory porewater metabolites (i.e. TCO2, TH2S and NH4 +) while replenishing SO4 2−. Furthermore, sulfate consumption was significantly higher in Marenzelleria sediment (79–87 mmol m−2 d−1) than in defaunated controls (36–50 mmol m−2 d−1), which indicated a 75–92 % lower DOC availability in the former. DOC excreted by Marenzelleria may have sustained 17–32 % of SO4 2− reduction. Lower C:S ratios (1.6–1.7) in Marenzelleria compared to defaunated sediments (2.4–2.8) suggest basic differences in carbon mineralization pathways, with e.g. H2 as a possible substrate for sulfate reduction in the former treatment and higher fermentative TCO2 formation in the latter. No significant stimulatory effect of Marenzelleria was evident for microbial NH4 + production. Total budgets revealed that Marenzelleria increased C mineralization by 50 % in amended sediment, compared to only 9 % in non-amended sediment. This study suggests that the presence of Marenzelleria may lead to a marked stimulation of sulfate reduction and degradation of refractory organic matter. Marenzelleria invasion may therefore have widespread consequences for microbial pathways and organic matter processing in sandy marine sediments.
Similar content being viewed by others
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 Press, New York
Aller R, Yingst A (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
Banta GT, Holmer M, Jensen MH, Kristensen E (1999) Effects of two polychaete worms, Nereis diversicolor and Arenicola marina, on aerobic and anaerobic decomposition in sandy marine sediment. Aquat Microb Ecol 19:189–204
Bower CE, Holm-Hansen T (1980) A salisylate-hypochlorite method for determining ammonia in seawater. Can J Fish Aquat Sci 37:794–798
Canfield DE, Thamdrup B, Kristensen E (2005) Aquatic geomicrobiology. Elsevier Academic, San Diego
Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458
Delefosse M, Banta GT, Canal-Vérges P, Penha-Lopes G, Quintana CO, Valdemarsen T, Kristensen E (2012) Macrobenthic community response to the Marenzelleria viridis (Polychaeta) invasion of a Danish estuary. Mar Ecol Prog Ser 461:83–94
Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80
Essink K, Kleef HL (1988) Marenzelleria viridis (Verrill, 1873) (Polychaeta: spionidae): a new record from the Ems Estuary (The Netherlands/Federal Republic of Germany). Zool Bijdr 38:1–13
George JD (1966) Reproduction and early development of the Spionid polychaete, Scolecolepides viridis (Verril). Biol Bull 130:76–93
Hall POJ, Aller RC (1992) Rapid, small-volume, flow injection analysis for ΣCO2 and NH4 + in marine and freshwaters. Limnol Oceanogr 37:1113–1119
Hansen K, Kristensen E (1998) The impact of the polychaete Nereis diversicolor and enrichment with macroalgal (Chaetomorpha linum) detritus on benthic metabolism and nutrient dynamics in organic-poor and organic-rich sediment. J Exp Mar Biol Ecol 231:201–223
Holmboe N, Kristensen E (2002) Ammonium adsorption in sediments of a tropical mangrove forest (Thailand) and a temperate Wadden Sea area (Denmark). Wetl Ecol Manag 10:453–460
Josefson A, Norkko J, Norkko A (2012) Burial and decomposition of plant pigments in surface sediments of the Baltic Sea -role of oxygen and benthic fauna. Mar Ecol Progr Ser 455:33–49
Karlson AML, Näslund J, Rydén SB, Elmgren R (2011) Polychaete invader enhances resource utilization in a species-poor system. Oecologia 166:1055–1065
Kotta K, Kotta I, Simm M, Lankov A, Lauringson V, Põllumäe A, Ojaveer H (2006) Ecological consequences of biological invasions: three invertebrate case studies in the north-eastern Baltic Sea. Helgol Mar Res 60:106–112
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, Andersen FØ (1987) Determination of organic carbon in marine sediments: comparison of two CHN-analyzer methods. J Exp Mar Biol Ecol 109:15–23
Kristensen E, Hansen K (1995) Decay of plant detritus in organic-poor marine sediment: production rates and stoichiometry of dissolved C and N compounds. J Mar Res 53:675–702
Kristensen E, Holmer M (2001) Decomposition of plant materials exposed to different electron acceptors (O2, NO -3 , and SO 2-4 ) with emphasis on substrate origin, degradation kinetics and role of bioturbation. Geochim Cosmochim Acta 65:419–433
Kristensen E, Mikkelsen OL (2003) Impact of the burrow dwelling polychaete Nereis diversicolor on degradation of fresh and aged macroalgal detritus in coastal marine sediment. Mar Ecol Prog Ser 265:141–153
Kristensen E, Hansen T, Delefosse M, Banta GT, Quintana CO (2011) Contrasting effects of the polychaetes Marenzelleria viridis and Nereis diversicolor on benthic metabolism and solute transport in sandy coastal sediment. Mar Ecol Prog Ser 425:125–139
Kristensen E, Penha-Lopes G, Delefosse M, Valdemarsen T, Quintana CO, Banta GT (2012) What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Mar Ecol Prog Ser 446:285–302
Leppäkoski E, Gollasch S, Gruszka P, Ojaveer H, Olenin S, Panov V (2002) The Baltic—a sea of invaders. Can J Fish Aquat Sci 59:1175–1188
Martin WR, Banta GT (1992) The measurement of sediment irrigation rates: a comparison of the Br− tracer and 222Rn/226Ra disequilibrium techniques. J Mar Res 50:125–154
Neideman R, Wenngren J, Oláfsson E (2003) Competition between introduced polychaete Marenzelleria sp. and the native amphipod Monoporea affinis in Baltic soft bottoms. Mar Ecol Prog Ser 264:49–55
Norkko J, Reed DC, Timmermann K, Norkko A, Bonsdorff E, Gustafsson BG, Slomp CP, Carstensen J, Conley DJ (2012) A welcome can of worms? Hypoxia mitigation by an invasive species. Glob Change Biol 18:422–434
Olenin S, Leppäkoski E (1999) Non-native animals in Baltic Sea: alteration of benthic habitats in coastal inlets and lagoons. Hydrobiol 393:233–243
Pallud C, Van Cappellen P (2006) Kinetics of microbial sulfate reduction in estuarine sediments. Geochim Cosmochim Acta 70:1148–1162
Papaspyrou S, Gregersen T, Kristensen E, Christensen B, Cox RP (2006) Microbial reaction rates and bacterial communities in sediment surrounding burrows of two nereidid polychaetes (Nereis diversicolor and N. virens). Mar Biol 148:541–550
Papaspyrou S, Kristensen E, Christensen B (2007) Arenicola marina (Polychaeta) and organic matter mineralisation in sandy marine sediments: in situ and microcosm comparison. Estuar Coast Shelf Sci 72:213–222
Preisler A, de Beer D, Lichtschlag A, Lavik G, Boetius A, Jørgensen BB (2007) Biological and chemical sulfide oxidation in a Beggiatoa inhabited marine sediment. ISME J 1:341–353
Quintana CO, Tang M, Kristensen E (2007) Simultaneous study of particle reworking, irrigation transport and reaction rates in sediment bioturbated by the polychaetes Heteromastus and Marenzelleria. J Exp Mar Biol Ecol 352:392–406
Quintana CO, Hansen T, Delefosse M, Banta GT, Kristensen E (2011) Burrow ventilation and associated porewater irrigation by the polychaete Marenzelleria viridis. J Exp Mar Biol Ecol 397:179–187
Sanz-Lázaro C, Valdemarsen T, Marín A, Holmer M (2011) Effects of temperature on biogeochemistry of marine organic-enriched systems: implications in a global warming scenario. Ecol Appl 21:2664–2677
Strayer DL, Eviner VT, Jeschke JM, Pace ML (2006) Understanding the long-term effects of species invasions. Trends Ecol Evol 21:645–651
Valdemarsen T, Kristensen E (2005) Diffusion scale dependent change in anaerobic carbon and nitrogen mineralization: true effect or experimental artifact? J Mar Res 63:645–669
Valdemarsen T, Kristensen E (2010) Degradation of dissolved organic monomers and short-chain fatty acids in sandy marine sediment by fermentation and sulfate reduction. Geochim Cosmchim Acta 74:1593–1605
Valdemarsen T, Canal-Verges P, Kristensen E, Holmer M, Kristiansen MD, Flindt MR (2010a) Vulnerability of Zostera marina seedlings to physical stress. Mar Ecol Prog Ser 418:119–130
Valdemarsen T, Kristensen E, Holmer M (2010b) Sulfur, carbon, and nitrogen cycling in faunated marine sediments impacted by repeated organic enrichment. Mar Ecol Prog Ser 400:37–53
Valdemarsen T, Bannister RJ, Hansen PK, Holmer M, Ervik A (2012) Biogeochemical malfunctioning in sediments beneath a deep-water fish farm. Environ Pollut 170:15–25
Wallentinus I, Nyberg CD (2007) Introduced marine organisms as habitat modifiers. Mar Pollut Bull 55:323–332
Acknowledgments
The authors would like to thank Birthe Christensen and Rikke Holm for laboratory assistance during the work. COQ was financed by Brazilian National Research Council (CNPq) (individual post-doctoral grant # 201912/2008-2). TV was supported by Danish Strategic Science Foundation Grant (contract # 09-063190) and EK by the Danish Council for Independent Research (contract # 272-08-0577 and # 09-071369). We also thank two anonymous reviewers for their constructive suggestions to improve the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Quintana, C.O., Kristensen, E. & Valdemarsen, T. Impact of the invasive polychaete Marenzelleria viridis on the biogeochemistry of sandy marine sediments. Biogeochemistry 115, 95–109 (2013). https://doi.org/10.1007/s10533-012-9820-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10533-012-9820-2