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Revealing the scale of marine bioinvasions in developing regions: a South African re-assessment

Abstract

As recently as 2009 the number of introductions recorded for South Africa comprised 22 marine and estuarine species. This review aims to reassess the diversity and scale of introduced marine and estuarine species in the region. Accurate taxonomic and systematic work, broad review of historical records and new sampling surveys across selected marine habitats conducted by a team of local and international experts has effectively revealed the presence of previously misidentified, overlooked, or new introductions. A total of 86 introduced and 39 cryptogenic species are recognized, increasing known numbers four and twofold respectively within 1 year, although the current assessment is far from fully comprehensive. Additional species were revealed within the historic literature (76%), from surveys conducted post-2005 (11%) and following taxonomic resolution (13%). Temporal analyses confirmed discovery rates were increasing over time. Ship fouling and ballast water were the dominant vector pathways, accounting for 48 and 38% respectively. Spatial analyses revealed patterns of bioinvasion to be significantly higher on the west coast compared to the other coastal regions. Overall, 53% of introductions were concentrated within harbour areas with only 4 open-coast invaders detected at present. Introduced species found in the cool and warm-temperate provinces of the west and south coast mainly originated from the northern hemisphere (65%). In contrast, introductions located in the sub-tropical and tropical provinces of the east coast mainly originated from the southern hemisphere (18%), with the remaining 17% of introduced species being of unknown origin. The research approach described has proven pivotal, contributing massively toward revealing the true scale and patterns of bioinvasion for a developing region within a relatively short period of time.

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References

  • Barnes DKA, Milner P (2005) Drifting plastic and its consequences for sessile organism dispersal in the Atlantic Ocean. Mar Biol 146:815–825

    Article  Google Scholar 

  • Bax N, Williamson A, Aguero M, Gonzalez E, Geeves W (2004) Marine invasive alien species: a threat to global biodiversity. Mar Policy 27:313–323

    Article  Google Scholar 

  • Bownes SJ, McQuaid CD (2009) Mechanisms of habitat segregation between an invasive and an indigenous mussel: settlement, post-settlement mortality and recruitment. Mar Biol 156:991–1006

    Article  Google Scholar 

  • Branch GM, Steffani CN (2004) Can we predict the effects of alien species? A case history of the invasion of South Africa by Mytilus galloprovincialis Lamarck. J Exp Mar Biol Ecol 300:189–215

    Google Scholar 

  • Branch GM, Odendaal F, Robinson TB (2010) Competition and facilitation between the alien mussel Mytilus galloprovincialis and indigenous species: moderation by wave action. J Exp Mar Biol Ecol 383:65–78

    Article  Google Scholar 

  • Bustamante RH, Branch GM (1996) Large scale patterns and trophic structure of Southern African rocky shores: the roles of geographic variation and wave exposure. J Biogeogr 23:339–351

    Article  Google Scholar 

  • Byers JE (2009) Competition in marine invasions. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 245–260

    Chapter  Google Scholar 

  • Carlton JT (1987) Patterns of transoceanic marine biological invasions in the Pacific. Ocean Bull Mar Sci 41:452–465

    Google Scholar 

  • Carlton JT (1996) Pattern, process and prediction in marine invasion ecology. Biol Conserv 78:96–106

    Article  Google Scholar 

  • Carlton JT (2003) Community assembly and historical biogeography in the North Atlantic Ocean: the potential role of human-mediated dispersal vectors. Hydrobiologia 503:1–8

    Article  Google Scholar 

  • Carlton JT (2009) Deep invasion ecology and the assembly of communities in historical time. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 13–56

    Chapter  Google Scholar 

  • Carlton JT, Cohen AN (2003) Episodic global dispersal in shallow water marine organisms. The case history of the European shore crabs Carcinus maenus and C. aestuarii. J Biogeogr 30:1809–1820

    Article  Google Scholar 

  • Carlton JT, Eldredge LG (2009) Marine bioinvasions of Hawai’i. The introduced and cryptogenic marine and estuarine animals and plants of the Hawaiian Archipelago. Bishop Museum Bulletins in Cultural and Environmental Studies 4. Bishop Museum Press, Honolulu, 202 pp

  • Carlton JT, Hodder J (1995) Biogeography and dispersal of coastal marine organisms: experimental studies on a replica of a 16th century sailing vessel. Mar Biol 121:721–730

    Article  Google Scholar 

  • Castilla JC, Neill PE (2009) Marine bioinvasions in the southeastern Pacific: status, ecology, economic impacts, conservation, and management. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 439–457

    Chapter  Google Scholar 

  • Chapman JW (1988) Invasions of the northeast Pacific by Asian and Atlantic gammaridean amphipod crustaceans, including a new species of Corophium. J Crustac Biol 8:364–382

    Article  Google Scholar 

  • Chapman JW, Carlton JT (1991) A test of criteria for introduced species: the global invasion by the isopod Synidotea laevidorsalis (Miers, 1881). J Crustac Biol 11:386–400

    Article  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Coles SL, DeFelice RC, Eldredge LC, Carlton JT (1999) Historical and recent introductions of nonindigenous marine species into Pearl Harbor, Oahu, Hawaiian Islands. Mar Biol 135:147–158

    Article  Google Scholar 

  • Cranfield HJ, Gordon DP, Willan RC, Marshall BA, Battershill CN, Francis NP, Nelson WA, Glasby CJ, Read JB (1998) Adventive marine species in New Zealand. NIWA Technical Report 34, 48 pp

  • DeFelice RC, Eldredge LG, Carlton JT (2001) Non-indigenous marine invertebrates. In: Eldredge LG, Smith CM (eds) A guidebook of introduced marine species in Hawaii. Bishop Museum Technical Report 21, 70 pp

  • Emanuel BP, Bustamante RH, Branch GM, Eekhout S, Odendaal SJ (1992) A zoogeographic and functional approach to the selection of marine reserves on the west coast of South Africa. S Afr J Mar Sci 12:341–354

    Article  Google Scholar 

  • Ferreira CEL, de Oliveira Ribeiro Junqueira A, Villac MC, Lopes RM (2009) Marine bioinvasions in the Brazilian coast: brief report on history of events, vectors, ecology, impacts, and management of non-indigenous species. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 459–477

    Chapter  Google Scholar 

  • Florence WK, Hayward PJ, Gibbons MJ (2008) Taxonomy of shallow-water Bryozoa from the west coast of South Africa. Afr Nat Hist 3:1–58

    Google Scholar 

  • Fofonoff PW, Ruiz GM, Hines AH, Steves BD, Carlton JT (2009) Four centuries of biological invasions in tidal waters of the Chesapeake Bay region. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 479–506

    Chapter  Google Scholar 

  • Galil BS, Zenetos A (2002) A sea change—exotics in the eastern Mediterranean. In: Leppakoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe: distributions, impacts and management. Kluwer, Dordrecht, pp 325–336

    Google Scholar 

  • Gibbons MJ, Abiahy BB, Angel M, Assuncao CML, Bartsch I, Best P, Biseswar RJ, Bradford-Grieve JM, Branch W, Burreson E, Cannon L, Casanova JP, Channing A, Child CA, Compagno L, Cornelius RFS, Dadon JR, David JHM, Day J, Della-Croce N, Emschermann P, Erseus C, Esnal G, Gibson R, Griffiths CL et al (1999) The taxonomic richness of South Africa’s marine fauna: a crisis at hand. S Afr J Sci 95:8–12

    Google Scholar 

  • Gollasch S, Nehring S (2006) National checklist for aquatic alien species in Germany. Aquat Invasions 1:245–269

    Article  Google Scholar 

  • Griffiths CL (2000) Overview of current problems and future risks. In: Preston G, Brown G, van Wyk E (eds) Best management practices for preventing and controlling invasive alien species. Working for Water Programme, Cape Town, pp 235–241

    Google Scholar 

  • Griffiths CL, Branch GM (1991) The macrofauna of rocky shores in False Bay. Trans R Soc S Afr 47:575–594

    Google Scholar 

  • Griffiths CL, Hockey PAR, Van Erkom Schurink C, Le Roux PJ (1992) Marine invasive aliens on South African shores—implications for community structure and trophic functioning. S Afr J Mar Sci 12:713–722

    Article  Google Scholar 

  • Griffiths CL, Robinson TB, Mead A (2009) The status and distribution of marine alien species in South Africa. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 393–408

    Chapter  Google Scholar 

  • Hampton S, Griffiths CL (2007) Why Carcinus maenas cannot get a grip on South Africa’s wave exposed coastline. Afr J Mar Sci 9:123–126

    Article  Google Scholar 

  • Hayden BJ, Inglis GJ, Schiel DR (2009) Marine invasions in New Zealand: a history of complex supply-side dynamics. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 409–424

    Chapter  Google Scholar 

  • Hewitt CL, Campbell ML, Thresher RE, Martin RB, Boyd S (2004) Introduced and cryptogenic species in Port Phillip Bay, Victoria, Australia. Mar Biol 144:183–202

    Article  Google Scholar 

  • Hewitt CL, Gollasch S, Minchin D (2009) The vessel as a vector—Biofouling, ballast water and sediments. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 117–132

    Chapter  Google Scholar 

  • Jenner HA, Rajagopal S, Van der Velde G, Duad MS (2003) Perforation of ABS pipes by boring bivalve Martesia striata: a case study. Int Biodeterior Biodegrad 52:229–232

    Article  CAS  Google Scholar 

  • Jensen K, Knudsen J (2005) A summary of alien marine benthic invertebrates in Danish waters. Oceanol Hydrobiol Stud 34:137–162

    Google Scholar 

  • Kolar CS, Lodge DM (2001) Progress in invasion biology: predicting invaders. Trends Ecol Evol 16(4):199–204

    PubMed  Article  Google Scholar 

  • Le Roux PJ, Branch GM, Joska MAP (1990) On the distribution, diet and possible impact of the invasive European shore crab Carcinus maenas (L.) along the South African coast. S Afr J Mar Sci 9:85–93

    Article  Google Scholar 

  • Leppakoski 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 

  • Leppakoski E, Shiganova T, Alexandrov B (2009) European enclosed and semi-enclosed seas. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 529–547

    Chapter  Google Scholar 

  • Levings CD, Kieser D, Jamieson GS, Dudas S (2002) Marine and estuarine alien species in the Strait of Georgia, British Columbia. In: Claudia R, Nantel P, Muckle-Jeffs E (eds) Alien invaders in Canada’s waters, wetlands and forests. Natural Resources Canada, Canadian Forest Service, Ottawa, pp 111–131

    Google Scholar 

  • Lombard AT (2004) Marine component of the National Spatial Biodiversity Assessment for the development of South Africa’s National Biodiversity Strategic and Action Plan. National Botanical Institute, p 101

  • Lonhart SI (2009) Natural and climate change mediated invasions. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 57–70

    Chapter  Google Scholar 

  • Mead A, Carlton JT, Griffiths CL, Rius M (2011) Introduced and cryptogenic marine and estuarine species in South Africa. J Nat Hist (in press)

  • Miller AW, Ruiz GM (2009) Differentiating successful and failed invaders: Species pools and the importance of defining vector, source and recipient regions. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 353–374

    Google Scholar 

  • Minchin D, Gollasch S, Cohen AN, Hewitt CL, Olenin S (2009) Characterizing vectors of marine invasions. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 109–116

    Chapter  Google Scholar 

  • Molnar JL, Gamboa RL, Revenga C, Spalding MD (2008) Assessing the global threat of invasive species to marine biodiversity. Front Ecol Env 6:485–492

    Article  Google Scholar 

  • Nuñez MA, Pauchard A (2010) Biological invasions in developing and developed countries: does one model fit all? Biol Invasions 12:707–714

    Article  Google Scholar 

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

    PubMed  Article  CAS  Google Scholar 

  • Occhipinti-Ambrogi A, Savini D (2003) Biological invasions as a component of global change in stressed marine ecosystems. Mar Pollut Bull 46:542–551

    PubMed  Article  CAS  Google Scholar 

  • Olyarnik SV, Bracken MES, Byrnes JE, Randall Hughes A, Hultgren KM, Stachowicz JJ (2009) Ecological factors affecting community invasibility. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 215–240

    Chapter  Google Scholar 

  • Orensanz JM, Schwindt E, Pastorino G, Bortulus A, Casas G, Darrigran G et al (2002) No longer the pristine confines of the world’s ocean: a survey of exotic marine species in the southwestern Atlantic. Biol Invasions 4:115–143

    Article  Google Scholar 

  • Otani M (2004) Introduced marine organisms in Japanese coastal waters and processes involved in their entry. Jpn J Bentho 59:45–57 (note English translation available from author)

    Google Scholar 

  • Rilov G, Galil B (2009) Marine bioinvasions in the Mediterranean Sea—history, distribution and ecology. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 549–576

    Chapter  Google Scholar 

  • Rius M, McQuaid CD (2009) Facilitation and competition between invasive and indigenous mussels over a gradient of physical stress. Basic Appl Ecol 10:607–613

    Article  Google Scholar 

  • Robinson TA, Griffiths CL, McQuaid CD, Rius M (2005) Marine alien species of South Africa—status and impacts. Afr J Mar Sci 27:297–306

    Article  Google Scholar 

  • Ruiz GM, Hewitt CL (2002) Toward understanding patterns of coastal marine invasions: a prospectus. In: Leppäkoski E, Gollasch S, Olenin S (eds) Invasive aquatic species of Europe. Distribution, impacts, and management. Kluwer, Dordrecht, pp 529–547

    Google Scholar 

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

    Google Scholar 

  • Ruiz GM, Fofonoff P, Hines AH, Grosholz ED (1999) Non-inidgenous species as stressors in estuarine and marine communities: assessing invasion impacts and interactions. Limnol Oceanogr 44:950–972

    Article  Google Scholar 

  • Ruiz GM, Fofonoff PW, Carlton JT, Wonham MJ, Hines AJ (2000) Invasion of coastal marine communities in North America: apparent patterns, processes and biases. Annu Rev Ecol Syst 31:481–531

    Article  Google Scholar 

  • Sala OE, Chapin FS, Armesto JJ, Berlow E et al (2000) Global biodiversity scenarios for the year 2100. Science 287:1770–1774

    PubMed  Article  CAS  Google Scholar 

  • Seo KS, Lee Y (2009) A first assessment of invasive marine species on Chinese and Korean coasts. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 577–585

    Chapter  Google Scholar 

  • Sink KJ, Branch GM (2005) Biogeographic patterns in rocky intertidal communities in KwaZulu-Natal, South Africa. Afr J Mar Sci 27:81–96

    Article  Google Scholar 

  • Sliwa C, Migus S, McEnnulty F, Hayes KR (2009) Marine bioinvasions in Australia. In: Rilov G, Crooks JA (eds) Biological invasions in marine ecosystems. Springer, Berlin, pp 425–437

    Chapter  Google Scholar 

  • Solow AR, Costello CJ (2004) Estimating the rate of species introductions from the discovery record. Ecology 85:1822–1825

    Article  Google Scholar 

  • Stegenga H, Bolton JJ, Anderson RJ (1997) Seaweeds of the South African west coast. Contrib Bolus Herb 18:3–637

    Google Scholar 

  • Wells MJ, Poynton RJ, Balsinhas AA, Musil KJ, Joffe H, van Hoepen E, Abbot SK (1986) The history of the introduction of invasive alien plants to Southern Africa. In: Macdonald IAW, Kruger FJ, Ferrar AA (eds) The ecology and management of biological invasions in southern Africa. Oxford University Press, Cape Town, pp 21–35

    Google Scholar 

  • Wilson JRU, Dormontt EE, Prentis PJ, Lowe AJ, Richardson DM (2009) Something in the way you move: dispersal pathways affect invasion success. Trends Ecol Evol 24:136–144

    PubMed  Article  Google Scholar 

  • Winston JE (1982) Drift plastic: an expanding niche for a marine invertebrate? Mar Pollut Bull 13:348–351

    Article  Google Scholar 

  • Wonham MJ, Carlton JT (2005) Trends in marine biological invasions at local and regional scales: the Northeast Pacific Ocean as a model system. Biol Invasions 7:369–392

    Article  Google Scholar 

  • Wonham MJ, Pachepsky E (2006) A null model of temporal trends in biological invasion records. Ecol Lett 9(6):663–672

    PubMed  Article  Google Scholar 

  • Wonham MJ, Carlton JT, Ruiz GM, Smith LD (2000) Fish and ships: relating dispersal frequency to success in biological invasions. Mar Biol 136:1111–1121

    Article  Google Scholar 

  • Zar JH (2004) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle River, p 663

    Google Scholar 

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Acknowledgments

We are grateful to a large number of colleagues (cited in Mead et al. 2011) who generously provided unpublished records, museum data, systematic expertise, identified specimens or gave valuable advice. This research was conducted with support from History of the Near-shore (HNS) and the South African Environmental Observation Node (SAEON) to AM, and a grant from the Department of Science and Technology/National Research Foundation Centre of Excellence for Invasion Biology to CLG, MR and JTC. MR was supported by the ‘Agencia Española de Cooperación Internacional para el Desarrolló from the Spanish ‘Ministerio de Asuntos Exteriores y de Cooperación’.

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Mead, A., Carlton, J.T., Griffiths, C.L. et al. Revealing the scale of marine bioinvasions in developing regions: a South African re-assessment. Biol Invasions 13, 1991–2008 (2011). https://doi.org/10.1007/s10530-011-0016-9

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Keywords

  • Ballast
  • Bioinvasions
  • Cryptogenic
  • Fouling
  • Vectors
  • South Africa