Skip to main content
Log in

Impact of the invasive polychaete Marenzelleria viridis on the biogeochemistry of sandy marine sediments

  • Published:
Biogeochemistry Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Bower CE, Holm-Hansen T (1980) A salisylate-hypochlorite method for determining ammonia in seawater. Can J Fish Aquat Sci 37:794–798

    Article  Google Scholar 

  • Canfield DE, Thamdrup B, Kristensen E (2005) Aquatic geomicrobiology. Elsevier Academic, San Diego

    Google Scholar 

  • Cline JD (1969) Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol Oceanogr 14:454–458

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Ehrenfeld JG (2010) Ecosystem consequences of biological invasions. Annu Rev Ecol Evol Syst 41:59–80

    Article  Google Scholar 

  • 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

    Google Scholar 

  • George JD (1966) Reproduction and early development of the Spionid polychaete, Scolecolepides viridis (Verril). Biol Bull 130:76–93

    Article  Google Scholar 

  • Hall POJ, Aller RC (1992) Rapid, small-volume, flow injection analysis for ΣCO2 and NH4 + in marine and freshwaters. Limnol Oceanogr 37:1113–1119

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Karlson AML, Näslund J, Rydén SB, Elmgren R (2011) Polychaete invader enhances resource utilization in a species-poor system. Oecologia 166:1055–1065

    Article  Google Scholar 

  • 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

    Article  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  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Olenin S, Leppäkoski E (1999) Non-native animals in Baltic Sea: alteration of benthic habitats in coastal inlets and lagoons. Hydrobiol 393:233–243

    Article  Google Scholar 

  • Pallud C, Van Cappellen P (2006) Kinetics of microbial sulfate reduction in estuarine sediments. Geochim Cosmochim Acta 70:1148–1162

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Strayer DL, Eviner VT, Jeschke JM, Pace ML (2006) Understanding the long-term effects of species invasions. Trends Ecol Evol 21:645–651

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • Wallentinus I, Nyberg CD (2007) Introduced marine organisms as habitat modifiers. Mar Pollut Bull 55:323–332

    Article  Google Scholar 

Download references

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

Authors

Corresponding author

Correspondence to Cintia O. Quintana.

Rights and permissions

Reprints 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

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10533-012-9820-2

Keywords

Navigation