Biological Invasions

, Volume 12, Issue 10, pp 3579–3589 | Cite as

Does climatic warming explain why an introduced barnacle finally takes over after a lag of more than 50 years?

  • Sophia Witte
  • Christian Buschbaum
  • Justus E. E. van Beusekom
  • Karsten ReiseEmail author
Original Paper


Invading alien species may have to await appropriate conditions before developing from a rare addition to the recipient community to a dominance over native species. Such a retarded invasion seems to have happened with the antipodean cirripede crustacean Austrominius modestus Darwin, formerly known as Elminius modestus, at its northern range in Europe due to climatic change. This barnacle was introduced to southern Britain almost seven decades ago, and from there spread north and south. At the island of Sylt in the North Sea, the first A. modestus were observed already in 1955 but this alien remained rare until recently, when in summer of 2007 it had overtaken the native barnacles Semibalanus balanoides and Balanus crenatus in abundance. At the sedimentary shores of Sylt, mollusc shells provide the main substrate for barnacles and highest abundances were attained on mixed oyster and mussel beds just above low tide level. A. modestus ranged from the upper intertidal down to the subtidal fringe. Its realized spatial niche was wider than that of the two natives. We suggest that at its current northern range in Europe a long series of mild winters and several warm summers in a row has led to an exponential population growth in A. modestus.


Alien species Austrominius modestus Invasion Climate change North Sea 



We thank Elisabeth Herre for substantial help with the figures. Patrick Polte, Nils Volkenborn, Alfred Resch and Kay von Böhlen were essential to set-up the ring-experiment. Heike Büttger and Georg Nehls provided long-term data on barnacle abundance attached to beds of mussels and oysters.


  1. Albrecht A, Reise K (1994) Effect of Fucus vesiculosus covering intertidal mussel beds in the Wadden Sea. Helgol Meeresunters 48:243–256CrossRefGoogle Scholar
  2. Alpert P (2006) The advantages and disadvantages of being introduced. Biol Invasions 8:1523–1534CrossRefGoogle Scholar
  3. Armonies W, Herre E, Sturm M (2001) Effects of the severe winter 1995/96 on the benthic macro fauna of the Wadden Sea and the coastal North Sea near the island of Sylt. Helgol Mar Res 55:170–175CrossRefGoogle Scholar
  4. Barnes H, Barnes M (1968) Elminius modestus Darwin: a recent extension of the distribution and its present status on the southern part of the French Atlantic coast. Cahiers des Biologie Marine 9:261–268Google Scholar
  5. Barney JN, Whitlow TH (2008) A unifying framework for biological invasions: the state factor model. Biol Invasions 10:259–272CrossRefGoogle Scholar
  6. Beare DJ, Burns F, Greig A, Jones EG, Peach K, Kienzle M, McKenzie E, Reid DG (2004) Long-term increases in prevalence of North Sea fishes having southern biogeographic affinities. Mar Ecol Prog Ser 284:269–278CrossRefGoogle Scholar
  7. Beaugrand G, Brander KM, Lindley JA, Souissi S, Reid PC (2003) Plankton effect on cod recruitment in the North Sea. Nature 426:661–664CrossRefPubMedGoogle Scholar
  8. Bishop MWH (1947) Establishment of an immigrant barnacle in British coastal waters. Nature 159:501CrossRefGoogle Scholar
  9. Bishop MWH (1951) Distribution of barnacles by ships. Nature 167:531CrossRefPubMedGoogle Scholar
  10. Buckeridge JS, Newman WA (2010) A review of the subfamily Elminiinae (Cirripedia: Thoracica: Austrobalanidae), including a new genus, Protelminius nov., from the Oligocene of New Zealand. Zootaxa 2349:39–54Google Scholar
  11. Buschbaum C (2002a) Predation on barnacles of intertidal and sub tidal mussel beds in the Wadden Sea. Helgol Mar Res 56:37–43CrossRefGoogle Scholar
  12. Buschbaum C (2002b) Recruitment patterns and biotic interactions of barnacles (Cirripedia) on mussel beds (Mytilus edulis L.) in the Wadden Sea. Berichte zur Polar- und Meeresforschung 408:143Google Scholar
  13. Büttger H, Asmus H, Asmus R, Buschbaum C, Dittmann S, Nehls G (2008) Community dynamics of intertidal soft-bottom mussel beds over two decades. Helgol Mar Res 62:23–36CrossRefGoogle Scholar
  14. Carlton JT (1985) Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanogr Mar Biol Ann Rev 23:313–374Google Scholar
  15. Crisp DJ (1958) The spread of Elminius modestus Darwin in North-West-Europe. J Mar Biol Ass UK 37:483–520CrossRefGoogle Scholar
  16. Crisp DJ (1964) The effects of the winter of 1962/63 on the British marine fauna. Helgol wiss Meeresunters 10:313–327CrossRefGoogle Scholar
  17. Crooks JA (2005) Lag times and exotic species: the ecology and management of biological invasions in slow-motion. Ecoscience 12(3):316–329CrossRefGoogle Scholar
  18. Crooks JA, Soulé ME (1999) Lag times in population explosions of invasive species: causes and implications. In: Sandlund OT, Schei PJ, Viken A (eds) Invasive species and biodiversity management. Kluwer Academic Press, Dordrecht, pp 103–125Google Scholar
  19. Darwin C (1854) A monograph on the subclass Cirripedia, with figures of all species. The Balanidae (or sessile cirripedes), the Verrucidae, etc. Ray Society, London, p 684Google Scholar
  20. Diederich S, Nehls G, van Beusekom JEE, Reise K (2005) Introduced Pacific oysters (Crassostrea gigas) in the northern Wadden Sea: invasion accelerated by warm summers? Helgol Mar Res 59:97–106CrossRefGoogle Scholar
  21. Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139CrossRefPubMedGoogle Scholar
  22. Foster BA (1971) Desiccation as a factor in the intertidal zonation of barnacles. Mar Biol 8:12–29CrossRefGoogle Scholar
  23. Franke H-D, Gutow L (2004) Long-term changes in the macrozoobenthos around the rocky island of Helgoland (German Bight, North Sea). Helgol Mar Res 58:303–310CrossRefGoogle Scholar
  24. Galil BS (2009) Taking stock: inventory of alien species in the Mediterranean sea. Biol Invasions 11:359–372CrossRefGoogle Scholar
  25. Gätje C, Reise K (1998) Ökosystem Wattenmeer, Austausch-, Transport- und Stoffumwandlungsprozesse. Springer, Berlin, p 570Google Scholar
  26. Görlitz S (2005) Neue Riffe im Wattenmeer: Die Pazifische Auster Crassostrea gigas und ihre assoziierte Lebensgemeinschaft. Diploma thesis, University of Kiel, pp 66Google Scholar
  27. Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17:22–27CrossRefGoogle Scholar
  28. Harms J (1999) The neozoan Elminius modestus Darwin (Crustacea, Cirripedia): possible explanations for its successful invasion in European water. Helgol Meeresunters 52:337–345CrossRefGoogle Scholar
  29. Harms J, Anger K (1983) Seasonal, annual, and spatial variation in the development of hard bottom communities. Helgol Meeresunters 36:137–150CrossRefGoogle Scholar
  30. Harms J, Anger K (1989) Settlement of the barnacle Elminius modestus on test panels at Helgoland (North Sea): a ten year study. Topics in marine biology. Sci Mar 53:417–421 Ed by JD RosGoogle Scholar
  31. Kerckhof F, Cattrijsse A (2001) Exotic Cirripedia (Balanomorpha) from buoys off the Belgian coast. Senckenb Marit 31:245–254CrossRefGoogle Scholar
  32. Kerckhof F, Haelters J, Gollasch S (2007) Alien species in the marine and brackish ecosystem: the situation in Belgian waters. Aquat Invasions 2:243–257CrossRefGoogle Scholar
  33. Kirby RR, Beaugrand G, Lindley JA, Richrdson AJ, Edwards M, Reid PC (2007) Climate effects and benthic-pelagic coupling in the North Sea. Mar Ecol Prog Ser 330:31–38CrossRefGoogle Scholar
  34. Kochmann J, Buschbaum C, Volkenborn N, Reise K (2008) Shift from native to alien oysters: differential effects of ecosystem engineers. J Exp Mar Biol Ecol 364:1–10CrossRefGoogle Scholar
  35. Kühl H (1954) Über das Auftreten von Elminius modestus Darwin in der Elbmündung. Helgol wiss Meeresunters 5:53–56CrossRefGoogle Scholar
  36. Kühl H (1963) Die Verbreitung von Elminius modestus Darwin (Cirripedia, Thoracica) an der Deutschen Küste. Crustaceana 5:99–111CrossRefGoogle Scholar
  37. Lawson J, Davenport J, Whitaker A (2004) Barnacle distribution in Lough Hyne Marine nature reserve: a new baseline and an account of invasion by the introduced Australasian species Elminius modestus Darwin. Est Coast Shelf Sci 60:729–735CrossRefGoogle Scholar
  38. Loebl M, van Beusekom JEE, Reise K (2006) Is spread of the neophyte Spartina anglica recently enhanced by increasing temperatures? Aquat Ecol 40:315–324CrossRefGoogle Scholar
  39. Luther G (1977) Bewuchsuntersuchungen auf Natursteinsubstraten im Gezeitenbereich des Nordsylter Wattenmeeres: sessile und hemisessile Tiere. Helgol wiss Meeresunters 29:375–403CrossRefGoogle Scholar
  40. Luther G (1987) Seepocken der deutschen Küstengewässer. Helgol Meeresunters 41:1–43CrossRefGoogle Scholar
  41. MacKenzie BR, Schiedek D (2007) Daily ocean monitoring since the 1860 s shows record warming of northern European seas. Global Change Biology 13:1335–1347CrossRefGoogle Scholar
  42. Martens P, van Beusekom JEE (2008) Zooplankton response to a warmer northern Wadden Sea. Helgol Mar Res 62:67–75CrossRefGoogle Scholar
  43. Mieszkowska N, Kendall MA, Hawkins SJ, Leaper R, Williamson P, Hardman-Mountford NJ, Southward AJ (2006) Changes in the range of some common rocky shore species in Britain–a response to climate change? Hydrobiologia 555:241–251CrossRefGoogle Scholar
  44. Nehls G, Büttger H (2006) Miesmuschelmonitoring 1998–2005 im Nationalpark Schleswig-Holsteinisches Wattenmeer. Landesamt für den Nationalpark, Schleswig-Holsteinisches Wattenmeer, p 165Google Scholar
  45. Nehls G, Diedrich S, Thieltges D, Strasser M (2006) Wadden sea mussel beds invaded by oyster and slipper limpets: competition or climate control? Helgol Mar Res 60:135–143CrossRefGoogle Scholar
  46. O’Riordan RM, Muphy O (2000) Variation in the reproductive cycle of Elminius modestus in southern Ireland. J Mar Biol Ass UK 80:607–616CrossRefGoogle Scholar
  47. O’Riordan RM, Culloty S, Davenport J, McAllen R (2009) Increases in the abundance of the invasive barnacle Austrominius modestus on the Isle of Cumbrae, Scotland. Mar Biodivers Rec 2:1–4CrossRefGoogle Scholar
  48. Occhipinti-Ambrogi A (2007) Global change and marine communities: alien species and climate change. Mar Pollut Bull 55:342–352CrossRefPubMedGoogle Scholar
  49. Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42CrossRefPubMedGoogle Scholar
  50. Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915CrossRefPubMedGoogle Scholar
  51. Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97CrossRefPubMedGoogle Scholar
  52. Rainbow PS (1984) An introduction to the biology of British littoral barnacles. Field Stud 6:1–51Google Scholar
  53. Reichert K, Buchholz F (2006) Changes in the macrozoobenthos of the intertidal zone at Helgoland (German Bight, North Sea): a survey of 1984 repeated in 2002. Helgol Mar Res 60:213–223CrossRefGoogle Scholar
  54. Reise K (1998) Pacific oysters invade mussel beds in the European Wadden Sea. Senckenb Marit 28:167–175CrossRefGoogle Scholar
  55. Reise K, van Beusekom JEE (2008) Interactive effects of global and regional change on a coastal ecosystem. Helgol Mar Res 62:85–91CrossRefGoogle Scholar
  56. Reise K, Olenin S, Thieltges DW (2006) Are aliens threatening European aquatic coastal ecosystems? Helgol Mar Res 60:77–83CrossRefGoogle Scholar
  57. Sax DF, Stachowicz JJ, Brown JH et al (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22:465–471CrossRefPubMedGoogle Scholar
  58. Southward AJ, Hawkins SJ, Burrows MT (2005) Seventy years’ observations of changes in distribution and abundance of zooplankton and intertidal organisms in the western English Channel in relation to rising sea temperature. J Therm Biol 20:127–155CrossRefGoogle Scholar
  59. Thieltges DW, Strasser M, van Beusekom JEE, Reise K (2004) Too cold to prosper–winter mortality prevents population increase of the introduced American slipper limpet Crepidula fornicata in northern Europe. J Exp Mar Biol Ecol 311:375–391CrossRefGoogle Scholar
  60. Thieltges DW, Prinz K, Reise K, Jensen KT (2009) Invaders interfere with native parasite-host interactions. Biol Invasions. doi: 10.1007/s10530-008-9350-y
  61. Underwood AJ (1997) Experiments in ecology. Cambridge University Press, Cambridge, p 504Google Scholar
  62. van Beusekom JEE, Weigelt-Krenz S, Martens P (2008) Long-term variability of winter nitrate concentrations in the Northern Wadden Sea driven by freshwater discharge, decreasing riverine loads and denitrification. Helgol Mar Res 62:49–57CrossRefGoogle Scholar
  63. van Beusekom JEE, Loebl M, Martens P (2009) Distant riverine nutrient supply and local temperature drive the long-term phytoplankton development in a temperate coastal basin. J Sea Res 61:26–33CrossRefGoogle Scholar
  64. Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416:389–395CrossRefPubMedGoogle Scholar
  65. Watson DI, O’Riordan RM, Barnes DKA, Cross T (2005) Temporal and spatial variability in the recruitment of barnacles and the local dominance of Elminius modestus Darwin in SW Ireland. Est Coast Shelf Sci 63:119–131CrossRefGoogle Scholar
  66. Westphal MI, Browne M, MacKinnon K, Noble I (2008) The link between international trade and the global distribution of invasive species. Biol Invasions 10:391–398CrossRefGoogle Scholar
  67. Wethey DS, Woodin SA (2008) Ecological hind casting of biogeographic responses to climate change in the European intertidal zone. Hydrobiologia 606:139–151CrossRefGoogle Scholar
  68. Wiegemann M (2008) Wild cyprids metamorphosing in vitro reveal the presence of Balanus amphitrite Darwin, 1854 in the German Bight basin. Aquat Invasions 3:235–238CrossRefGoogle Scholar
  69. Wiltshire KH, Manly BFJ (2004) The warming trend at Helgoland roads, North Sea: phytoplankton responses. Helgol Mar Res 58:269–273CrossRefGoogle Scholar
  70. Wolff WJ, Reise K (2002) Oyster imports as a vector for the introduction of alien species into northern and western European coastal waters. In: Leppäkoski E et al (eds) Invasive aquatic species of Europe. Kluwer Acad Press, Netherlands, pp 193–205Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Sophia Witte
    • 2
  • Christian Buschbaum
    • 1
  • Justus E. E. van Beusekom
    • 1
  • Karsten Reise
    • 1
    Email author
  1. 1.Alfred Wegener Institute for Polar and Marine ResearchListGermany
  2. 2.BioConsult SHHusumGermany

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