Skip to main content
SpringerLink
Log in

Large-scale species invasion into a low-diversity system: spatial and temporal distribution of the invasive polychaetes Marenzelleria spp. in the Baltic Sea

  • Original Paper
  • Published:
Biological Invasions Aims and scope Submit manuscript

Abstract

Invasive species are considered to be a major threat to both terrestrial and aquatic ecosystems worldwide due to their negative effects on biodiversity, ecosystem functioning and species interactions. This study investigates with the help of large-scale monitoring datasets the spatial and temporal distribution of a successful invader, the polychaete species complex Marenzelleria spp. Mesnil 1896 into a species-poor, brackish water ecosystem in northern Europe, the Baltic Sea. The species complex has spread throughout the entire Baltic Sea and has become a dominant member of the communities especially in deeper, hypoxia-affected areas. The dynamics of the invasion follow a boom-and-bust pattern, with abundances peaking almost simultaneously throughout the Baltic Sea in 2005–2006. Possible mechanisms behind the successful establishment are changes in hydrography and species composition. Hypothesized and observed ecological impacts are reviewed. Evidence suggests a multitude of potential, sometimes contrasting, impacts. Due to the widespread distribution and high abundances, the biology and ecology of Marenzelleria spp. in the Baltic Sea need to be investigated further in order to assess its impact on ecosystem structure and functioning.

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

Access this article

Log in via an institution

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

  • Anttila-Huhtinen M (2010) Pohjaeläintutkimukset merialueella Pyhtää-Kotka-Hamina vuosina 2006–2009 ja vertailua aikaisempiin tuloksiin

  • Bastrop R, Blank M (2006) Multiple invasions—a polychaete genus enters the Baltic Sea. Biol Invasions 8:1195–1200

    Article  Google Scholar 

  • Bastrop R, Jürss K, Sturmbauer C (1998) Cryptic species in marine polychaete and their independent introduction from North America to Europe. Mol Biol Evol 15:97–103

    Article  CAS  PubMed  Google Scholar 

  • Bax N, Williamson A, Aguero M et al (2003) Marine invasive alien species: a threat to global biodiversity. Mar Policy 27:313–323

    Article  Google Scholar 

  • Bick A, Burckhardt R (1989) Erstnachweis von Marenzelleria viridis (Polychaeta, Spionidae) für den Ostseeraum, mit einem Bestimmungsschlüssel der Spioniden der Ostsee. Mitteilungen aus dem Museum für Naturkunde in Berlin. Zoologisches Museum und Institut für Spezielle Zoologie 65:237–247

    Article  Google Scholar 

  • Blank M, Laine AO, Jürss K et al (2008) Molecular identification key based on PCR/RFLP for three polychaete sibling species of the genus Marenzelleria, and the species’ current distribution in the Baltic Sea. Helgol Mar Res 62:129–141

    Article  Google Scholar 

  • Bochert R (1997) Marenzelleria viridis (Polychaeta: Spionidae): a review of its reproduction. Aquat Ecol 31:163–175

    Article  Google Scholar 

  • Bonaglia S, Bartoli M, Gunnarsson J et al (2013) Effect of reoxygenation and Marenzelleria spp. bioturbation on Baltic Sea sediment metabolism. Mar Ecol Prog Ser 482:43–55

  • Bonsdorff E (2006) Zoobenthic diversity-gradients in the Baltic Sea: continuous post-glacial succession in a stressed ecosystem. J Exp Mar Biol Ecol 330:383–391

    Article  Google Scholar 

  • Carstensen J, Conley DJ, Bonsdorff E et al (2014) Hypoxia in the Baltic Sea: biogeochemical cycles, benthic fauna, and management. Ambio 43:26–36

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cohen AN, Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279:555–558

    Article  CAS  PubMed  Google Scholar 

  • Conley DJ, Björck S, Bonsdorff E et al (2009) Hypoxia-related processes in the Baltic Sea. Environ Sci Technol 43:3412–3420

    Article  CAS  PubMed  Google Scholar 

  • Conley DJ, Carstensen J, Aigars J et al (2011) Hypoxia is increasing in the coastal zone of the Baltic Sea. Environ Sci Technol 45:6777–6783

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Crawley MJ (2012). The R book. John Wiley & Sons

  • Daunys D, Schiedek D, Olenin S (2000) Species strategy near its boundary: the Marenzelleria cf. viridis (Polychaeta, Spionidae) case in the South-Eastern Baltic Sea. Int Rev Hydrobiol 85:639–651

    Article  Google Scholar 

  • Davis MA, Chew MK, Hobbs RJ et al (2011) Don’t judge species on their origins. Nature 474:153–154

    Article  CAS  PubMed  Google Scholar 

  • Delefosse M, Banta G, Canal-Vergés P et al (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 

  • Elton CS (1958) The ecology of invasions by plants and animals. Methuen, London 18

    Book  Google Scholar 

  • Ezhova E, Spirido O (2005) Patterns of spatial and temporal distribution of the Marenzelleria cf.viridis population in the lagoon and marine environment in the Southeastern Baltic Sea. Oceanol Hydrobiol Stud 34:209–226

    Google Scholar 

  • Feistel R, Nausch G, Hagen E (2006) Unusual Baltic inflow activity in 2002–2003 and varying deep-water properties. Oceanologia 48:21–35

    Google Scholar 

  • Fridley JD, Stachowicz JJ, Naeem S et al (2007) The invasion paradox: reconciling pattern and process in species invasions. Ecology 88:3–17

    Article  CAS  PubMed  Google Scholar 

  • George JD (1966) Reproduction and early development of the spionid polychaete, Scolecolepides viridis (Verrill). The Biological Bulletin 130:76–93

    Article  Google Scholar 

  • Granberg ME, Gunnarsson JS, Hedman JE et al (2008) Bioturbation-driven release of organic contaminants from Baltic Sea sediments mediated by the invading polychaete Marenzelleria neglecta. Environ Sci Technol 42:1058–1065

    Article  CAS  PubMed  Google Scholar 

  • Hedman JE, Gunnarsson JS, Samuelsson G et al (2011) Particle reworking and solute transport by the sediment-living polychaetes Marenzelleria neglecta and Hediste diversicolor. J Exp Mar Biol Ecol 407:294–301

    Article  CAS  Google Scholar 

  • HELCOM (2009) Eutrophication in the Baltic Sea—an integrated thematic assessment of the effects of nutrient enrichment and eutrophication in the Baltic Sea region. Balt Sea Environ Proc No 115B:1–48

    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 

  • Hobbs RJ, Huenneke LF (1992) Disturbance, diversity, and invasion: implications for conservation. Conserv Biol 6:324–337

    Article  Google Scholar 

  • Jansson K (1994) Alien species in the marine environment. Introductions to the Baltic Sea and the Swedish west coast. Swedish Environmental Protection Agency, Solna

    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 Prog Ser 455:33–49

    Article  CAS  Google Scholar 

  • Karlson AL, Näslund J, Rydén S et al (2011) Polychaete invader enhances resource utilization in a species-poor system. Oecologia 166:1055–1065

    Article  PubMed Central  PubMed  Google Scholar 

  • Karlson AML, Nascimento FJA, Suikkanen S et al (2012) Benthic fauna affects recruitment from sediments of the harmful cyanobacterium Nodularia spumigena. Harmful Algae 20:126–131

    Article  Google Scholar 

  • Kotta J, Ólafsson E (2003) Competition for food between the introduced polychaete Marenzelleria viridis (Verrill) and the native amphipod Monoporeia affinis Lindström in the Baltic Sea. J Sea Res 50:27–35

    Article  Google Scholar 

  • Kotta J, Orav H, Sandberg-Kilpi E (2001) Ecological consequence of the introduction of the polychaete Marenzelleria cf. viridis into a shallow-water biotope of the northern Baltic Sea. J Sea Res 46:273–280

    Article  Google Scholar 

  • Kotta J, Kotta I, Simm M et al (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, Hansen T, Delefosse M et al (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  CAS  Google Scholar 

  • Kube J, Powilleit M (1997) Factors controlling the distribution of Marenzelleria cf. viridis, Pygospio elegans and Streblospio shrubsoli (Polychaeta: Spionidae) in the southern Baltic Sea, with special attention for the response to an event of hypoxia. Aquat Ecol 31:187–198

    Article  Google Scholar 

  • Kube J, Zettler ML, Gosselck F, Ossig S, Powilleit M (1996) Distribution of Marenzelleria viridis (Polychaeta: Spionidae) in the southwestern Baltic Sea in 1993/94—ten years after introduction. Sarsia 81:131–142

    Google Scholar 

  • Laine AO, Andersin A-B, Leiniö S et al (2007) Stratification-induced hypoxia as a structuring factor of macrozoobenthos in the open Gulf of Finland (Baltic Sea). J Sea Res 57:65–77

    Article  Google Scholar 

  • Leppäkoski E, Olenin S (2000) Non-native species and rates of spread: lessons from the Brackish Baltic Sea. Biol Invasions 2:151–163

    Article  Google Scholar 

  • Leppäkoski E, Gollasch S, Gruszka P et al (2002) The Baltic—a sea of invaders. Can J Fish Aquat Sci 59:1175–1188

    Article  Google Scholar 

  • Leppäranta M, Myrberg K (2009) Physical oceanography of the Baltic Sea. Praxis, Chichester

    Book  Google Scholar 

  • MacDougall AS, Turkington R (2005) Are invasive species the drivers or passengers of change in degraded ecosystems? Ecology 86:42–55

    Article  Google Scholar 

  • Mack RN, Simberloff D, Mark Lonsdale W et al (2000) Biotic invasions: causes, epidemiology, global consequences, and control. Ecol Appl 10:689–710

    Article  Google Scholar 

  • Mata TM, Haddad NM, Holyoak M (2013) How invader traits interact with resident communities and resource availability to determine invasion success. Oikos 122:149–160

    Article  Google Scholar 

  • Maximov AA (2011) Large-scale invasion of Marenzelleria spp. (Polychaeta; Spionidae) in the eastern Gulf of Finland, Baltic Sea. Russ J Biol Invasions 2:11–19

    Article  Google Scholar 

  • Maximov AA, Eremina TR, Lange EK et al (2014) Regime shift in the ecosystem of the eastern Gulf of Finland caused by the invasion of the polychaete Marenzelleria arctia. Oceanology 54:46–53

    Article  Google Scholar 

  • Middelburg JJ, Levin LA (2009) Coastal hypoxia and sediment biogeochemistry. Biogeosciences 6:1273–1293

    Article  CAS  Google Scholar 

  • Milborrow S (2013) rpart.plot: plot rpart models. An enhanced version of plot.rpart. R package version 1.4–3

  • Naeem S, Knops JMH, Tilman D et al (2000) Plant diversity increases resistance to invasion in the absence of covarying extrinsic factors. Oikos 91:97–108

    Article  Google Scholar 

  • Neideman R, Wenngren J, Ólafsson E (2003) Competition between the introduced polychaete Marenzelleria sp. and the native amphipod Monoporeia affinis in Baltic soft bottoms. Mar Ecol Prog Ser 264:49–55

    Article  Google Scholar 

  • Neira C, Levin LA, Grosholz ED (2005) Benthic macrofaunal communities of three sites in San Francisco Bay invaded by hybrid Spartina, with comparison to uninvaded habitats. Mar Ecol Prog Ser 292:111–126

    Article  CAS  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 oi a former community. Mar Ecol Prog Ser 66:95–101

    Article  Google Scholar 

  • Norkko A, Bonsdorff E, Boström C (1993) Observations of the polychaete Marenzelleria viridis (Verrill) on a shallow sandy bottom on the south coast of Finland. Memo Soc Fauna Flora Fenn 69:112–113

    Google Scholar 

  • Norkko A, Rosenberg R, Thrush SF et al (2006) Scale-and intensity-dependent disturbance determines the magnitude of opportunistic response. J Exp Mar Biol Ecol 330:195–207

    Article  Google Scholar 

  • Norkko J, Reed DC, Timmermann K et al (2012) A welcome can of worms? Hypoxia mitigation by an invasive species. Glob Change Biol 18:422–434

    Article  Google Scholar 

  • Orlova M, Telesh I, Berezina N et al (2006) Effects of nonindigenous species on diversity and community functioning in the eastern Gulf of Finland (Baltic Sea). Helgol Mar Res 60:98–105

    Article  Google Scholar 

  • Quintana CO, Hansen T, Delefosse M et al (2011) Burrow ventilation and associated porewater irrigation by the polychaete Marenzelleria viridis. J Exp Mar Biol Ecol 397:179–187

    Article  Google Scholar 

  • R Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Rousi H, Laine AO, Peltonen H et al (2013) Long-term changes in coastal zoobenthos in the northern Baltic Sea: the role of abiotic environmental factors. ICES J Mar Sci J du Conseil 70:440–451

    Article  Google Scholar 

  • Rudnick DA, Hieb K, Grimmer KF et al (2003) Patterns and processes of biological invasion: the Chinese mitten crab in San Francisco Bay. Basic Appl Ecol 4:249–262

    Article  Google Scholar 

  • Ruiz GM, Carlton JT, Grosholz ED et al (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanisms, extent, and consequences. Am Zool 37:621–632

    Google Scholar 

  • Schiedek D (1997a) Marenzelleria cf. viridis (Polychaeta: Spionidae)—ecophysiological adaptations to a life in the coastal waters of the Baltic Sea. Aquat Ecol 31:199–210

    Article  CAS  Google Scholar 

  • Schiedek D (1997b) Marenzelleria viridis (Verrill, 1873) (Polychaeta), a new benthic species within European coastal waters. Some metabolic features. J Exp Mar Biol Ecol 211:85–101

    Article  Google Scholar 

  • Sellheim K, Stachowicz J, Coates R (2010) Effects of a nonnative habitat-forming species on mobile and sessile epifaunal communities. Mar Ecol Prog Ser 398:69–80

    Article  Google Scholar 

  • Shea K, Chesson P (2002) Community ecology theory as a framework for biological invasions. Trends Ecol Evol 17:170–176

    Article  Google Scholar 

  • Sikorski AV, Bick A (2004) Revision of Marenzelleria Mesnil, 1896 (Spionidae, Polychaeta). Sarsia 89:253–275

    Article  Google Scholar 

  • Simberloff D, Souza L, Nuñez MA et al (2011) The natives are restless, but not often and mostly when disturbed. Ecology 93:598–607

    Article  Google Scholar 

  • Simberloff D, Martin J-L, Genovesi P et al (2013) Impacts of biological invasions: what’s what and the way forward. Trends Ecol Evol 28:58–66

    Article  PubMed  Google Scholar 

  • Simm M, Kukk H, Viitasalo M (2003) Dynamics of Marenzelleria viridis (Polychaeta: Spionidae) pelagic larvae in Pärnu Bay, NE Gulf of Riga, in 1991–99. Proc Est Acad Sci Biol Ecol 52:394–406

    Google Scholar 

  • Skei J, Larsson P, Rosenberg R et al (2000) Eutrophication and contaminants in aquatic ecosystems. AMBIO J Hum Environ 29:184–194

    Google Scholar 

  • Sousa R, Gutiérrez J, Aldridge D (2009) Non-indigenous invasive bivalves as ecosystem engineers. Biol Invasions 11:2367–2385

    Article  Google Scholar 

  • Stachowicz JJ, Byrnes JE (2006) Species diversity, invasion success, and ecosystem functioning: disentangling the influence of resource competition, facilitation, and extrinsic factors. Mar Ecol Prog Ser 311:251–262

    Article  Google Scholar 

  • Stachowicz JJ, Fried H, Osman RW et al (2002) Biodiversity, invasion resistance, and marine ecosystem function: reconciling pattern and process. Ecology 83:2575–2590

    Article  Google Scholar 

  • Stigzelius J, Laine A, Rissanen J et al (1997) The introduction of Marenzelleria viridis (Polychaeta, Spionidae) into the Gulf of Finland and the Gulf of Bothnia (northern Baltic Sea). Ann Zool Fenn 34:205–212

    Google Scholar 

  • Therneau T, Atkinson B, Ripley B (2013) rpart: recursive partitioning. R package version 4.1–4

  • Tilman D (1999) The ecological consequences of changes in biodiversity: a search for general principles. Ecology 80:1455–1474

    Google Scholar 

  • Tilman D (2004) Niche tradeoffs, neutrality, and community structure: a stochastic theory of resource competition, invasion, and community assembly. Proc Natl Acad Sci USA 101:10854–10861

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Urban-Malinga B, Warzocha J, Zalewski M (2013) Effects of the invasive polychaete Marenzelleria spp. on benthic processes and meiobenthos of a species-poor brackish system. J Sea Res 80:25–34

    Article  Google Scholar 

  • Villnäs A, Norkko A (2011) Benthic diversity gradients and shifting baselines: implications for assessing environmental status. Ecol Appl 21:2172–2186

    Article  PubMed  Google Scholar 

  • Williams SL, Davidson IC, Pasari JR et al (2013) Managing multiple vectors for marine invasions in an increasingly connected world. Bioscience 63:952–966

    Article  Google Scholar 

  • Williamson MH, Fitter A (1996) The characters of successful invaders. Biol Conserv 78:163–170

    Article  Google Scholar 

  • Zettler ML, Bick Andreas, Bochert Ralf (1995) Distribution and population dynamics of Marenzelleria viridis (Polychaeta, Spionidae) in a coastal water of the southern Baltic. Arch Fish Mar Res 42:209–224

    Google Scholar 

Download references

Acknowledgments

We thank Nordenskiöld samfundet r.f. -foundation, Jenny and Antti Wihuri foundation, University of Helsinki (3-year grant to JN) and the COCOA-project (funded by BONUS, the joint Baltic Sea research and development programme (Art 185), funded jointly from EU’s 7th Programme for research, technological development and demonstration and from the Academy of Finland) for financial support. Anna Villnäs, Simon Thrush and Judi Hewitt are thanked for their valuable comments on the manuscript.

Author information

Authors and Affiliations

  1. Tvärminne Zoological Station, University of Helsinki, J.A. Palménin Tie 260, FI-10900, Hanko, Finland

    Laura Kauppi, Alf Norkko & Joanna Norkko

  2. Marine Research Centre, Finnish Environment Institute, FI-00251, Helsinki, Finland

    Alf Norkko

Authors
  1. Laura Kauppi
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Alf Norkko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Joanna Norkko
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Laura Kauppi.

Appendix

Appendix

See Table 2.

Table 2 A basin-wise summary of Marenzelleria spp. and total abundance and biomass, number of taxa and hydrographical parameters
Full size table

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kauppi, L., Norkko, A. & Norkko, J. Large-scale species invasion into a low-diversity system: spatial and temporal distribution of the invasive polychaetes Marenzelleria spp. in the Baltic Sea. Biol Invasions 17, 2055–2074 (2015). https://doi.org/10.1007/s10530-015-0860-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-015-0860-0

Keywords

Search

Navigation