Biological Invasions

, Volume 4, Issue 4, pp 359–368 | Cite as

General Patterns in Invasion Ecology Tested in the Dutch Wadden Sea: The Case of a Brackish-Marine Polychaetous Worm

  • Karel Essink
  • Rob Dekker


The success of invasive aquatic species is determined by a variety of attributes such as wide environmental tolerance, high genetic variability, short generation time, early sexual maturity, high reproductive capacity, and a broad diet. Usually, introduced species, after some time lag since inoculation, show an exponential population increase and expansion. Maintenance of the immigrant species at a high population level will be dependent on interspecific competition with native species and availability of habitat and food. Eventually, the immigrant population may decline, for instance due to increased predation pressure, parasite infestation or loss of genetic vigour. These characteristic patterns in invasive species are reviewed for the case of the North American spionid polychaete Marenzelleria cf. wireni in the Dutch Wadden Sea. This species was first recorded in estuaries and coastal waters of the European continent in the Ems estuary (eastern Dutch Wadden Sea) in 1983. In the western part of the Dutch Wadden Sea the first specimens were found in 1989. The Ems estuary population showed the typical lag-phase, explosive increase, stabilisation, and eventual decline. In the western part of the Dutch Wadden Sea the latter two phases have not yet developed. The strong development and stabilisation of the population in the Ems estuary may have been caused by the availability of a yet not utilised food source. The species' final decline remains largely unexplained.

alien species biological invasion Ems estuary interspecific competition intertidal Marenzelleria 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Ashton PJ and Mitchell DS (1989) Aquatic plants: patterns and modes of invasion, attributes of invading species and assessment of control programmes. In: Drake JA, Mooney HA, di Castri F, Groves RH, Kruger FJ, Rejmanek M and Williamson M (eds) Biological Invasions. A Global Perspective, pp 111–154. John Wiley &: Sons, New YorkGoogle Scholar
  2. Atkins SM, Jones AM and Garwood PR (1987) The ecology and reproduction cycle of a population of Marenzelleria viridis (Annelida: Polychaeta: Spionidae) in the Tay Estuary. Proceedings of the Royal Society of Edinburgh 92B: 311–322Google Scholar
  3. Bastrop R, Röhner M, Sturmbauer C and Jürss K (1997) Where did Marenzelleria spp. in Europe come from? Aquatic Ecology 31: 119–136Google Scholar
  4. Beukema JJ (1993) Successive changes in distribution patterns as an adaptive strategy in the bivalve Macoma balthica (L.) in the Wadden Sea. Helgoländer Meeresuntersuchungen 47: 287–304Google Scholar
  5. Beukema JJ, Dekker R and Essink K (2000) Long-term observations on the dynamics of three species of polychaetes living on tidal flats of the Wadden Sea: the role of weather and predator–prey interactions. Journal of Animal Ecology 69: 31–44Google Scholar
  6. Bick A and Zettler ML (1997) On the identity and distribution of two species of Marenzelleria (Polychaeta: Spionidae) in Europe and North America. Aquatic Ecology 31: 137–148Google Scholar
  7. Bochert R (1997) Marenzelleria viridis (Polychaeta: Spionidae): a review of its reproduction. Aquatic Ecology 31: 163–175Google Scholar
  8. Bochert R, Bick A, Zettler ML and Arndt EA (1997a) Marenzelleria viridis (Verrill 1873) (Polychaeta: Spionidae), an invader in the benthic community in Baltic coastal inlets – investigations of reproduction. Proceedings of the 13th BMB-Symposium, 1993, pp 131–139. Riga, LatviaGoogle Scholar
  9. Bochert A, Richard D and Bochert R(1997b) Marenzelleria cf.viridis and the sulphide regime. Aquatic Ecology 31: 223–231Google Scholar
  10. Boudouresque CF (1994) Les espéces introduites dans les eaux côtières d'Europe et de Méditerranée: état de la question et conséquences. In: Boudouresque CF, Briand F and Nolan C (eds) Introduced Species in European Coastal Waters, pp 8–27. European Commission, LuxembourgGoogle Scholar
  11. Carlton JT (1985) Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanography and Marine Biology Annual Review 23: 313–371Google Scholar
  12. Carlton JT (1996) Pattern, process, and prediction in marine invasion ecology. Biological Conservation 78: 97–106Google Scholar
  13. Carlton JT and Geller JB (1993) Ecological roulette: the global transport of nonindigenous marine organisms. Science 261: 78–82Google Scholar
  14. Cohen AN and Carlton JT (1998) Accelerating invasion rate in a highly invaded estuary. Science 279: 555–558Google Scholar
  15. Cornell HV and Lawton JH (1993) Species interactions, local and regional processes, and limits to the richness of ecological com-munities: a theoretical perspective. Journal of Animal Ecology 61: 1–12Google Scholar
  16. Crooks JA and Soulé ME (1999) Lag times in population explosions of invasive species: causes and implications. In: Sandlund OT, Schei PJ and Viken A (eds) Invasive Species and Biodiversity Management, Population and Community Biology Series 24, pp 103–125. Kluwer Academic Publishers, Dordrecht, The NetherlandsGoogle Scholar
  17. Dauer DM, Maybury CA and Ewing RM (1981) Feeding behaviour and general ecology of several spionid polychaetes from the Chesapeake Bay. Journal of Experimental Marine Biology and Ecology 54: 21–38Google Scholar
  18. Daunys D, Schiedek D and Olenin S (2000) Species strategy near its boundary: the Marenzelleria cf. viridis (Polychaeta, Spionidae) in the south-eastern Baltic Sea. International Review of Hydrobiology 85: 639–651Google Scholar
  19. Davis MA, Grime JP and Thompson K (2000) Fluctuating resources in plant communities: a general theory of invasibility. Journal of Ecology 88: 528–534Google Scholar
  20. Dekker R and de Bruin W (2000) Het macrozoobenthos op twaalf raaien in de Waddenzee en de Eems-Dollard in 1999. [The macro-zoobenthos at twelve transects in the Wadden Sea and Ems-Dollard estuary in 1999.] National Institute for Sea Research (NIOZ), NIOZ-Report 2000–8Google Scholar
  21. Elton CS (1958) The Ecology of Invasions by Animals and Plants. Methuen &: Co, London, 118 ppGoogle Scholar
  22. Eno C, Clark RA and Sanderson WG (eds) (1997) Non-native Species in British Waters: a Review and Directory. Joint Nature Conservation Committee, Peterborough, UK, 152 ppGoogle Scholar
  23. Esselink P, Van Belkum J and Essink K (1989) The effect of organic pollution on local distribution of Nereis diversicolor and Corophium volutator. Netherlands Journal of Sea Research 23: 323–332Google Scholar
  24. Essink K (1978) The effects of pollution by organic waste on macro-fauna in the eastern Dutch Wadden Sea. Netherlands Institute for Sea Research, Publication Series No 1–1978, 135 pp.Google Scholar
  25. Essink K (1999) Dispersal and development of Marenzelleria spp. (Polychaeta, Spionidae) populations in NW Europe and The Netherlands. Helgoländer Meeresuntersuchungen 52: 367–372Google Scholar
  26. Essink K (2003) Response of an estuarine ecosystem to reduced organic waste discharge. Aquatic Ecology 37: 65–76Google Scholar
  27. Essink K and Keidel H (1998) Changes in estuarine nematode communities following a decrease of organic pollution. Aquatic Ecology 32: 195–202Google Scholar
  28. Essink K and Kleef HL (1988) Marenzelleria viridis (Verrill 1873) (Polychaeta: Spionidae): a new record from the Ems estuary (The Netherlands/Federal Republic of Germany). Zoologische Bijdragen (Leiden) 38: 1–13Google Scholar
  29. Essink K and Kleef HL(1993) Distribution and life cycle of the North American spionid polychaete Marenzelleria viridis (Verrill 1873) in the Ems estuary. Netherlands Journal of Aquatic Ecology 27: 237–246Google Scholar
  30. Essink K, Eppinga J and Dekker R (1998) Long-term changes in intertidal macrozoobenthos of the Dollard (Ems estuary) and effects of introduction of the North American spionid poly-chaete Marenzelleria cf. wireni. Senckenbergiana Maritima 8: 211–225Google Scholar
  31. George JD (1966) Reproduction and early development of the spionid polychaete Scolecolepides viridis (VERRIL). Biological Bulletin 130: 76–93Google Scholar
  32. Goerke H (1966) Nahrungsfiltration von Nereis diversicolor O.F. Müller (Nereidae, Polychaeta). [Food filtration by Nereis diversicolor O.F. Müller (Nereidae, Polychaeta).] Veröffentlichungen des Instituts für Meeresforschung in Bremerhaven 10: 49–58Google Scholar
  33. Goerke H (1971) Die Ernährungsweise der Nereis-Arten (Polychaeta, Nereidae) der deutschen Küsten. [The way of feeding of Nereis-species (Polychaeta, Nereidae) on the German coasts.] Veröffentlichungen des Instituts für Meeresforschung in Bremerhaven 13: 1–50Google Scholar
  34. Gollasch S (1996) Untersuchungen des Arteintrages durch den internationalen Schiffsverkehr unter besonderer Berucksichti-gung nichtheimischer Arten. [Investigations into introduction of species by international shipping with special attention to non-native species.] Dissertation, University of Hamburg, Dr. Kovac Verlag, Hamburg, 314 ppGoogle Scholar
  35. Gruszka P (1999) The river Odra estuary as a gateway for alien species immigration to the Baltic Sea basin. Acta Hydrochimica Hydrobiology 27: 374–382Google Scholar
  36. Herbold B and Moyle PB (1986) Introduced species and vacant niches. American Naturalist 128: 751–760Google Scholar
  37. Kaufman L (1992) Catastrophic change in species-rich freshwa-ter ecosystems: the lessons of Lake Victoria. BioScience 42: 846–858Google Scholar
  38. Ketelaars HAM, Lambregts-van de Clundert FE, Carpentier CJ, Wagenvoort AJ and Hoogenboezem W (1999) Ecological effect of the mass occurrence of the Ponto-Caspian invader, Hemimysis anomala G.O. Sars, 1907 (Crustacea: Mysidacea), in a freshwater storage reservoir in The Netherlands, with notes on its autecology and new records. Hydrobiologia 394: 233–248Google Scholar
  39. Kleef HL and Jager Z (1999) Het functioneren van de Eems-Dollard als kinderkamer voor platvis. Deel 2. Vestiging van schol, bot en tong in het intergetijdengebied in relatie tot sedimentsamensteling en hoogteligging. [The functioning of the Ems-Dollard estuary as a nursery for flatfish. Part 2. Settlement of plaice, flounder and sole in the intertidal area in relation to sediment type and elevation.] National Institute for Coastal and Marine Management (RIKZ). Report RIKZ-99.040Google Scholar
  40. Kotta J and Kotta I (1998) Distribution and invasion ecology of Marenzelleria viridis in the Estonian coastal waters. Proceedings of the Estonian Academy of Science, Biology, Ecology 47: 212–220Google Scholar
  41. Kube J and 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. Aquatic Ecology 31: 187–198Google Scholar
  42. Leppäkoski E (1984) Introduced species in the Baltic Sea and its coastal ecosystems. Ophelia Supplement 3: 123–135Google Scholar
  43. Leppäkoski E and Olenin S (2000) Non-native species and rates of spread: lessons from the brackish Baltic Sea. Biological Invasions 2: 151–163Google Scholar
  44. Locke A, Reid DM, van Leeuwen HC, Sprules WG and Carlton JT (1993) Ballast water exchange as a means of controlling dispersal of freshwater organisms by ships. Canadian Journal of Fisheries and Aquatic Sciences 50: 2086–2093Google Scholar
  45. Lodge DM (1993) Biological invasions: lessons for ecology. Trends in Ecology and Evolution 8: 133–137Google Scholar
  46. McLusky DS, Hull SC and Elliott M (1993) Variations in the inter-tidal and subtidal macrofauna and sediments along a salinity gradient in the upper Forth Estuary. Netherlands Journal of Aquatic Ecology 27: 101–109Google Scholar
  47. Mooney HA and Drake JA (eds) (1986) Ecology of Biological Invasions of North America and Hawaii. Springer-Verlag, New YorkGoogle Scholar
  48. Moyle PB and Light T (1996) Biological invasions of fresh water: empirical rules and assembly theory. Biological Conservation 78: 149–162Google Scholar
  49. Olenin S and Leppäkoski E (1999) Non-native animals in the Baltic Sea: alteration of benthic habitats in coastal inlets and lagoons. Hydrobiologia 393: 233–243Google Scholar
  50. Parker IM, Simberloff D, Lonsdale WM, Goodell K, Wonham M, Kareiva PM, Williamson MH, Von Holle B, Moyle PB, Byers JE and Goldwasser L (1999) Impact: toward a framework for under-standing the ecological effects of invaders. Biological Invasions 1: 3–19Google Scholar
  51. Prop J (1998) Effecten van afvalwaterlozingen op trekvogels in de Dollard: een analyse van tellingen uit de periode 1974– 1995. [Effects of waste discharge on migratory birds in the Dollard: an analysis of counts in the period 1974–1995.] In: Essink K and Esselink P (eds) Het Eems-Dollard estuarium: interacties tussen menselijke be¨ýnvloeding en natuurlijke dynamiek [The Ems-Dollard estuary: interactions between human impact and natural dynamics], pp 145–167. National Institute for Coastal and Marine Management (RIKZ), Report RIKZ-98.020Google Scholar
  52. Ribera MA and Boudouresque C-F (1995) Introduced marine plants, with special reference to macroalgae: mechanisms and impact. Progress in Phycology Research 11: 187–268Google Scholar
  53. Ricciardi A and MacIsaac HJ (2000) Recent mass invasion of the North American Great Lakes by Ponto-Caspian species. Trends in Ecology and Evolution 15: 62–65PubMedGoogle Scholar
  54. Ricciardi A and Rasmussen JB (1998) Predicting the identity and impact of future biological invaders: a priority for aquatic resource management. Canadian Journal of Fisheries and Aquatic Sciences 55: 1759–1765.Google Scholar
  55. Ricciardi A, Neves RJ and Rasmussen JB (1998) Impending extinc-tions of North American freshwater mussels (Unionidae) following the zebra mussel (Dreissena polymorpha) invasion. Journal of Animal Ecology 67: 613–619Google Scholar
  56. Sanders HL, Goudsmit EM, Mills EL and Hampson GE (1962) A study of the intertidal fauna of Barnstaple Harbor, Massachusetts. Limnology and Oceanography 7: 63–79Google Scholar
  57. Sandlund OT, Schei PJ and Viken A (1999) Introduction: the many aspects of the invasive alien species problem. In:Sandlund OT, Schei PJ and Viken A (eds) Invasive Species and Biodiversity Management, Population and Community Biology Series 24, pp 1–7. Kluwer Academic Publisher, Dordrecht, The NetherlandsGoogle Scholar
  58. Sarda R, Valiela I and Foreman K (1995a) Life cycle, demography, and production of Marenzelleria viridis in a salt marsh of southern NewEngland. Journal of the Marine Biological Association of the United Kingdom 75: 725–739Google Scholar
  59. Schiedek D (1997) Marenzelleria cf. viridis (Polychaeta: Spionidae) – ecophysiological adaptations to a life in the coastal waters of the Baltic Sea. Aquatic Ecology 31: 199–210Google Scholar
  60. Schiedek D (1999) Ecophysiological capability of Marenzelleria populations inhabiting North Sea estuaries: an overview. Helgoländer Meeresuntersuchungen 52: 373–382Google Scholar
  61. Schiedek D, Vogan C, Hardege J and Bentley M(1997) Marenzelleria cf. wireni (Polychaeta: Spionidae) from the Tay estuary. Metabolic response to severe hypoxia and hydrogen sulphide. Aquatic Ecology 31: 211–222Google Scholar
  62. Shiganova TA, Mirzoyan ZA, Studenikina EA, Volovik SP, Siokou-Frangou I, Zervoudaki S, Christou ED, Skirta AY and Dumont HJ (2001) Population development of the invader ctenophore Mnemiopsis leidyi, in the Black Sea and in other seas of the Mediterranean basin. Marine Biology 139: 431–445Google Scholar
  63. Simberloff D and Von Holle B (1999) Positive interactions on non-indigenous species: invasional meltdown? Biological Invasions 1: 21–32Google Scholar
  64. Smith LD, Wonham MJ, McCann LD, Ruiz GM, Hines AH and Carlton JT (1999) Invasion pressure to a ballast-flooded estuary and an assessment of inoculant survival. Biological Invasions 1: 67–87Google Scholar
  65. Stigzelius J, Laine A, Rissanen J, Andersin A-B and Ilus E (1997) The introduction of Marenzelleria viridis (Polychaeta, Spionidae) into the Gulf of Finland and the Gulf of Bothnia (northern Baltic Sea). Annales Zoologici Fennici 34: 205–212Google Scholar
  66. Talman SG and Keough MJ (2001) Impact of an exotic clam, Corbula gibba, on the commercial scallop Pecten fumatus in Port Philip Bay, south-east Australia: evidence of resource-restricted growth in a subtidal environment. Marine Ecology Progress Series 221: 135–143Google Scholar
  67. van Leussen W (1994) Estuarine macroflocs and their role in fine-grained sediment transport. Dissertation, University of Utrecht, The Netherlands, 488 ppGoogle Scholar
  68. Venema S (1998) Stomach food composition of postlarval floun-der Platichthys flesus in the Dollard, The Netherlands. National Institute for Coastal and Marine Management/RIKZ, Working document RIKZ/OS-98.602xGoogle Scholar
  69. Whitlatch RB (1980) Patterns of resource utilization and coexis-tence in marine intertidal deposit-feeding communities. Journal of Marine Research 38: 743–766Google Scholar
  70. Williamson M (1996) Biological Invasions. Chapman &: Hall, London, 256 ppGoogle Scholar
  71. Wolff WJ (1999) Exotic invaders of the meso-oligohaline zone of estuaries in the Netherlands: why are there so many? Helgoländer Meeresuntersuchungen 52: 393–400Google Scholar
  72. Zettler ML (1996) Successful establishment of the spionid poly-chaete, Marenzelleria viridis (Verrill 1873), in the Darss-Zingst estuary (southern Baltic) and its influence on the indigenous macrozoobenthos. Archives of Fisheries and Marine Research 43: 273–284Google Scholar
  73. Zettler ML (1997) The newcomer Marenzelleria viridis (Verrill 1873), its development and influence on the indigenous macrozoobenthos in a coastal water of the Southern Baltic. In: Ojaveer E (ed) Proceedings of the 14th Baltic Marine Biologists Symposium, 5–8 August 1995, Pärnu, Estonia, pp 280–296. Estonian Academy Publishers, TallinnGoogle Scholar
  74. Zmudzinski L (1996) The effects of the introduction of the American species Marenzelleria viridis (Polychaeta: Spionidae) on the benthic ecosystem of Vistula Lagoon. P.S.Z.N.I: Marine Ecology 17: 221–226Google Scholar

Copyright information

© Kluwer Academic Publishers 2002

Authors and Affiliations

  1. 1.HarenThe Netherlands
  2. 2.Netherlands Institute for Sea ResearchDen Burg/TexelThe Netherlands

Personalised recommendations