Skip to main content
SpringerLink
Log in

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

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

Abstract

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.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Albrecht A, Reise K (1994) Effect of Fucus vesiculosus covering intertidal mussel beds in the Wadden Sea. Helgol Meeresunters 48:243–256

    Article  Google Scholar 

  • Alpert P (2006) The advantages and disadvantages of being introduced. Biol Invasions 8:1523–1534

    Article  Google Scholar 

  • 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 55:170–175

    Article  Google Scholar 

  • 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 9:261–268

    Google Scholar 

  • Barney JN, Whitlow TH (2008) A unifying framework for biological invasions: the state factor model. Biol Invasions 10:259–272

    Article  Google Scholar 

  • 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 284:269–278

    Article  Google Scholar 

  • Beaugrand G, Brander KM, Lindley JA, Souissi S, Reid PC (2003) Plankton effect on cod recruitment in the North Sea. Nature 426:661–664

    Article  CAS  PubMed  Google Scholar 

  • Bishop MWH (1947) Establishment of an immigrant barnacle in British coastal waters. Nature 159:501

    Article  Google Scholar 

  • Bishop MWH (1951) Distribution of barnacles by ships. Nature 167:531

    Article  CAS  PubMed  Google Scholar 

  • 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 2349:39–54

    Google Scholar 

  • Buschbaum C (2002a) Predation on barnacles of intertidal and sub tidal mussel beds in the Wadden Sea. Helgol Mar Res 56:37–43

    Article  Google Scholar 

  • 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 408:143

    Google Scholar 

  • 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 62:23–36

    Article  Google Scholar 

  • Carlton JT (1985) Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanogr Mar Biol Ann Rev 23:313–374

    Google Scholar 

  • Crisp DJ (1958) The spread of Elminius modestus Darwin in North-West-Europe. J Mar Biol Ass UK 37:483–520

    Article  Google Scholar 

  • Crisp DJ (1964) The effects of the winter of 1962/63 on the British marine fauna. Helgol wiss Meeresunters 10:313–327

    Article  Google Scholar 

  • Crooks JA (2005) Lag times and exotic species: the ecology and management of biological invasions in slow-motion. Ecoscience 12(3):316–329

    Article  Google Scholar 

  • 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 103–125

    Google Scholar 

  • 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 684

    Google Scholar 

  • 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 59:97–106

    Article  Google Scholar 

  • Dukes JS, Mooney HA (1999) Does global change increase the success of biological invaders? Trends Ecol Evol 14:135–139

    Article  PubMed  Google Scholar 

  • Foster BA (1971) Desiccation as a factor in the intertidal zonation of barnacles. Mar Biol 8:12–29

    Article  Google Scholar 

  • 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 58:303–310

    Article  Google Scholar 

  • Galil BS (2009) Taking stock: inventory of alien species in the Mediterranean sea. Biol Invasions 11:359–372

    Article  Google Scholar 

  • Gätje C, Reise K (1998) Ökosystem Wattenmeer, Austausch-, Transport- und Stoffumwandlungsprozesse. Springer, Berlin, p 570

    Google Scholar 

  • Görlitz S (2005) Neue Riffe im Wattenmeer: Die Pazifische Auster Crassostrea gigas und ihre assoziierte Lebensgemeinschaft. Diploma thesis, University of Kiel, pp 66

  • Grosholz E (2002) Ecological and evolutionary consequences of coastal invasions. Trends Ecol Evol 17:22–27

    Article  Google Scholar 

  • Harms J (1999) The neozoan Elminius modestus Darwin (Crustacea, Cirripedia): possible explanations for its successful invasion in European water. Helgol Meeresunters 52:337–345

    Article  Google Scholar 

  • Harms J, Anger K (1983) Seasonal, annual, and spatial variation in the development of hard bottom communities. Helgol Meeresunters 36:137–150

    Article  Google Scholar 

  • 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 Ros

    Google Scholar 

  • Kerckhof F, Cattrijsse A (2001) Exotic Cirripedia (Balanomorpha) from buoys off the Belgian coast. Senckenb Marit 31:245–254

    Article  Google Scholar 

  • Kerckhof F, Haelters J, Gollasch S (2007) Alien species in the marine and brackish ecosystem: the situation in Belgian waters. Aquat Invasions 2:243–257

    Article  Google Scholar 

  • 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 330:31–38

    Article  Google Scholar 

  • 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 364:1–10

    Article  Google Scholar 

  • Kühl H (1954) Über das Auftreten von Elminius modestus Darwin in der Elbmündung. Helgol wiss Meeresunters 5:53–56

    Article  Google Scholar 

  • Kühl H (1963) Die Verbreitung von Elminius modestus Darwin (Cirripedia, Thoracica) an der Deutschen Küste. Crustaceana 5:99–111

    Article  Google Scholar 

  • 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 60:729–735

    Article  Google Scholar 

  • Loebl M, van Beusekom JEE, Reise K (2006) Is spread of the neophyte Spartina anglica recently enhanced by increasing temperatures? Aquat Ecol 40:315–324

    Article  Google Scholar 

  • Luther G (1977) Bewuchsuntersuchungen auf Natursteinsubstraten im Gezeitenbereich des Nordsylter Wattenmeeres: sessile und hemisessile Tiere. Helgol wiss Meeresunters 29:375–403

    Article  Google Scholar 

  • Luther G (1987) Seepocken der deutschen Küstengewässer. Helgol Meeresunters 41:1–43

    Article  Google Scholar 

  • MacKenzie BR, Schiedek D (2007) Daily ocean monitoring since the 1860 s shows record warming of northern European seas. Global Change Biology 13:1335–1347

    Article  Google Scholar 

  • Martens P, van Beusekom JEE (2008) Zooplankton response to a warmer northern Wadden Sea. Helgol Mar Res 62:67–75

    Article  Google Scholar 

  • 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 555:241–251

    Article  Google Scholar 

  • Nehls G, Büttger H (2006) Miesmuschelmonitoring 1998–2005 im Nationalpark Schleswig-Holsteinisches Wattenmeer. Landesamt für den Nationalpark, Schleswig-Holsteinisches Wattenmeer, p 165

    Google Scholar 

  • 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 60:135–143

    Article  Google Scholar 

  • O’Riordan RM, Muphy O (2000) Variation in the reproductive cycle of Elminius modestus in southern Ireland. J Mar Biol Ass UK 80:607–616

    Article  Google Scholar 

  • 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 2:1–4

    Article  Google Scholar 

  • Occhipinti-Ambrogi A (2007) Global change and marine communities: alien species and climate change. Mar Pollut Bull 55:342–352

    Article  CAS  PubMed  Google Scholar 

  • Parmesan C, Yohe G (2003) A globally coherent fingerprint of climate change impacts across natural systems. Nature 421:37–42

    Article  CAS  PubMed  Google Scholar 

  • Perry AL, Low PJ, Ellis JR, Reynolds JD (2005) Climate change and distribution shifts in marine fishes. Science 308:1912–1915

    Article  CAS  PubMed  Google Scholar 

  • Pörtner HO, Knust R (2007) Climate change affects marine fishes through the oxygen limitation of thermal tolerance. Science 315:95–97

    Article  PubMed  Google Scholar 

  • Rainbow PS (1984) An introduction to the biology of British littoral barnacles. Field Stud 6:1–51

    Google Scholar 

  • 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 60:213–223

    Article  Google Scholar 

  • Reise K (1998) Pacific oysters invade mussel beds in the European Wadden Sea. Senckenb Marit 28:167–175

    Article  Google Scholar 

  • Reise K, van Beusekom JEE (2008) Interactive effects of global and regional change on a coastal ecosystem. Helgol Mar Res 62:85–91

    Article  Google Scholar 

  • Reise K, Olenin S, Thieltges DW (2006) Are aliens threatening European aquatic coastal ecosystems? Helgol Mar Res 60:77–83

    Article  Google Scholar 

  • Sax DF, Stachowicz JJ, Brown JH et al (2007) Ecological and evolutionary insights from species invasions. Trends Ecol Evol 22:465–471

    Article  PubMed  Google Scholar 

  • 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 20:127–155

    Article  Google Scholar 

  • 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 311:375–391

    Article  Google Scholar 

  • 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

  • Underwood AJ (1997) Experiments in ecology. Cambridge University Press, Cambridge, p 504

    Google Scholar 

  • 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 62:49–57

    Article  Google Scholar 

  • 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 61:26–33

    Article  Google Scholar 

  • 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 416:389–395

    Article  CAS  PubMed  Google Scholar 

  • 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 63:119–131

    Article  Google Scholar 

  • Westphal MI, Browne M, MacKinnon K, Noble I (2008) The link between international trade and the global distribution of invasive species. Biol Invasions 10:391–398

    Article  Google Scholar 

  • Wethey DS, Woodin SA (2008) Ecological hind casting of biogeographic responses to climate change in the European intertidal zone. Hydrobiologia 606:139–151

    Article  Google Scholar 

  • Wiegemann M (2008) Wild cyprids metamorphosing in vitro reveal the presence of Balanus amphitrite Darwin, 1854 in the German Bight basin. Aquat Invasions 3:235–238

    Article  Google Scholar 

  • Wiltshire KH, Manly BFJ (2004) The warming trend at Helgoland roads, North Sea: phytoplankton responses. Helgol Mar Res 58:269–273

    Article  Google Scholar 

  • 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 193–205

    Google Scholar 

Download references

Acknowledgments

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.

Author information

Authors and Affiliations

  1. Alfred Wegener Institute for Polar and Marine Research, Wadden Sea Station Sylt, 25992, List, Germany

    Christian Buschbaum, Justus E. E. van Beusekom & Karsten Reise

  2. BioConsult SH, Brinckmannstr. 31, 25813, Husum, Germany

    Sophia Witte

Authors
  1. Sophia Witte
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christian Buschbaum
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Justus E. E. van Beusekom
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Karsten Reise
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Karsten Reise.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Witte, S., Buschbaum, C., van Beusekom, J.E.E. et al. Does climatic warming explain why an introduced barnacle finally takes over after a lag of more than 50 years?. Biol Invasions 12, 3579–3589 (2010). https://doi.org/10.1007/s10530-010-9752-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10530-010-9752-5

Keywords

Search

Navigation