Abstract
The invasion of the aquarium strain of the green alga Caulerpa taxifolia and subsequent alteration of community structure in the Mediterranean Sea raised awareness of the potential for non-native seaweeds to impact coastal communities. An introduction of C. taxifolia in southern California in 2000, presumably from the release of aquarium specimens, cost ~$7 million for eradication efforts. Besides C. taxifolia, other Caulerpa species being sold for aquarium use also may have the potential to invade southern Californian and U.S. waters. Surveys of the availability of Caulerpa species in southern California aquarium retail stores in 2000–2001 revealed that 26 of 50 stores sold at least one Caulerpa species (52 %) with seven stores selling C. taxifolia. In late 2001, California imposed a ban on the importation, sale, or possession of nine Caulerpa species; the City of San Diego expanded these regulations to include the entire genus. To determine the effectiveness of the California ban, we resurveyed Caulerpa availability at 43 of the 50 previously sampled retail stores in southern California in ~2006, ~4 years following the ban. Of the 43 stores, 23 sold Caulerpa (53 %) with four stores selling C. taxifolia. A χ2 test of frequency of availability before and after the California ban suggests that the ban has not been effective and that the aquarium trade continues to represent a potential vector for distributing Caulerpa specimens, including C. taxifolia. This study underscores the need for increased enforcement and outreach programs to increase awareness among the aquarium industry and aquarium hobbyists.
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References
Abbott IA, Hollenberg GJ (1976) Marine algae of California. Stanford University Press, Stanford
Allen R (2010) International management of tuna fisheries: arrangements, challenges and a way forward. FAO Fisheries and Aquaculture Technical Paper. No. 536
Bax N, Carlton JT, Mathews-Amos A, Haedrich RL, Howarth FG, Purcell JE, Reiser A, Gray A (2001) The control of biological invasions in the world’s oceans. Conservation Biology 15:1234–1246
Bolton TF, Graham WM (2006) Jellyfish on the rocks: bioinvasion threat of the international trade in aquarium live rock. Biological Invasions 8:651–653
Carlton JT (2001) Introduced species in U.S. coastal waters: environmental impacts and management priorities. Pew Oceans Commission, Arlington
Ceccherelli G, Cinelli F (1997) Short-term effects of nutrient enrichment of the sediment and interactions between the seagrass Cymodocea nodosa and the introduced alga Caulerpa taxifolia in a Mediterranean bay. Journal of Experimental Marine Biology and Ecology 217:165–177
Chang AL, Grossman JD, Spezio TS, Weiskel HW, Blum JC, Burt JW, Muir AA, Piovia-Scott J, Veblen KE, Grosholz ED (2009) Tackling aquatic invasions: risks and opportunities for the aquarium fish industry. Biological Invasions 11:773–785
Copp GH, Vilizzi L, Gozlan RE (2010) The demography of introduction pathways, propagule pressure and occurrences of non-native freshwater fish in England. Aquatic Conservation: Marine and Freshwater Ecosystems 20:595–601
Courtenay WR, Robins CR (1973) Exotic aquatic organisms in Florida with emphasis on fishes: a review and recommendations. Transactions of the American Fisheries Society 102:1–12
Courtenay WR, Stauffer JR (1990) The introduced fish problem and the aquarium fish industry. Journal of the World Aquaculture Society 21:145–159
Courtenay WR, Sahiman HF, Miley WW II, Herrema DJ (1974) Exotic fishes in fresh and brackish waters of Florida. Biological Conservation 6:292–302
Cummings DO, Williamson JE (2008) The role of herbivory and fouling on the invasive green alga Caulerpa filiformis in temperate Australian waters. Marine & Freshwater Research 59:279–290
Davis AR, Roberts DE, Cummins SP (1997) Rapid invasion of a sponge-dominated deep-reef by Caulerpa scalpelliformis (Chlorophyta) in Botany Bay, New South Wales. Australian Journal of Ecology 22:146–150
de Villèle X, Verlaque M (1995) Changes and degradation in a Posidonia oceanica bed invaded by the introduced tropical alga Caulerpa taxifolia in the north western Mediterranean. Botanica Marina 38:79–87
Eldredge LG, Carlton JT (2002) Hawaiian marine bioinvasions: a preliminary assessment. Pacific Science 56:211–212
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
Fuller PL, Nico LG, Williams JD (1999) Nonindigenous fishes introduced into inland waters of the United States. American Fisheries Society Special Publication 27
Gambell R (1993) International management of whales and whaling: an historical review of the regulation of commercial and aboriginal subsistence whaling. Arctic 46:97–107
Gray DK, Johengen TH, Reid DF, MacIsaac HJ (2007) Efficacy of open-ocean ballast water exchange as a means of preventing invertebrate invasions between freshwater ports. Limnology and Oceanography 52:2386–2397
Guidetti P, Milazzo M, Bussotti S, Molinari A, Murenu M, Pais A, Spanò N, Balzano R, Agardy T, Boero F, Carrada G, Cattaneo-Vietti R, Cau A, Chemello R, Greco S, Manganaro A, Notarbartolo di Sciara G, Russo GF, Tunesi L (2008) Italian marine reserve effectiveness: Does enforcement mater? Biological Conservation 141:699–709
Halpern B (2003) The impact of marine reserves: Do reserves work and does reserve size matter? Ecological Applications 13:S117–S137
Hardin, S (2007) Managing non-native wildlife in Florida: state perspective, policy and practice. In: Witmer GW, Pitt WC, Fagerston KA (eds) Managing vertebrate invasive species: proceedings of an international symposium. National Wildlife Research Center, Fort Collins
Hardin S, Watson C, Zajicek P (2008) Pathway risk analysis for exotic ornamental marine and estuarine species. Technical Report for the Florida Department of Agriculture and Consumer Services
Hare JA, Whitfield PE (2003) An integrated assessment of the introduction of lionfish (Pterois volitans/miles complex) to the western Atlantic Ocean. NOAA Technical Memorandum NOS NCCOS 2
Harlioglu MM, Harlioglu AG (2006) Threat of non-native crayfish introductions in Turkey: global lessons. Reviews in Fish Biology and Fisheries 16:171–181
Hayes KA, Joshi RC, Thiengo SC, Cowie RH (2008) Out of South America: multiple origins of non-native apple snails in Asia. Diversity and Distributions 14:701–712
Higgins A, Serbesoff-King K, King M, O’Reilly-Doyle K (2007) The power of partnerships: landscape scale conservation through public/private collaboration. Natural Areas Journal 27:236–250
Hockings M, Stolton S, Leverington F, Dudley N, Courrau J (2006) Evaluating effectiveness: a framework for assessing management effectiveness of protected areas, 2nd edn. IUCN, Gland, Switzerland/Cambridge, p 105
Jacoby C, Lapointe B, Creswell L (2004) Are native and nonindigenous seaweeds overgrowing Florida’s east coast reefs? Florida Sea Grant College Program
Jousson O, Pawlowski J, Zaninetti L, Zechman FW, Dini F, Di Guiseppe G, Woodfield R, Millar A, Meinez A (2000) Invasive alga reaches California. Nature 408:157–158
Kay SH, Hoyle ST (2007) Mail order, the internet and invasive aquatic weeds. Journal of Aquatic Plant Management 39:88–91
Levi F, Francour P (2004) Behavioral response of Mullus surmuletus to habitat modification by the invasive macroalga Caulerpa taxifolia. Journal of Fish Biology 64:55–64
Magalhães ALB, Jacobi CM (2010) E-commerce of freshwater aquarium fishes: potential disseminator of exotic species in Brazil. Acta Scientiarum Biological Sciences 32:243–248
Maki K, Galatowitsch S (2004) Movement of invasive aquatic plants into Minnesota (USA) through horticulture trade. Biological Conservation 118:389–396
McMurray CA (2009) Wildlife trafficking: U.S. efforts to tackle a global crisis. Natural Resources and Environment 23:16–18
McNeely JA (2005) Human dimensions of invasive alien species. In: Mooney HA, Mack RN, McNeely JA, Neville LE, Schei PJ, Waage JK (eds) Invasive alien species. Island Press, WA, pp 285–309
Meinesz A, Hesse B (1991) Introduction et invasion de l’algue tropicale Caulerpa taxifolia en Méditerranée Nord-occidentale. Oceanologica Acta 14:415–426
Meinesz A, Belsher T, Thibaut T, Antolic B, Ben Mustapha K, Chiaverini D, Cinelli F, Cotallorda J, Djellouli A, El Abed A, Orestano C, Grau A, Ivesa L, Jaklin A, Langar H, Massuti-Pascual E, Peirano A, Tunesi L, De Vaugelas J, Zavodnik N, Zuljevic A (2001) The introduced green alga Caulerpa taxifolia continues to spread in the Mediterranean. Biological Invasions 3:201–210
Merkel and Associates, Inc. (2006) Final Report on the eradication of the invasive seaweed Caulerpa taxifolia from Agua Hedionda lagoon and Huntington harbour, California. Technical report prepared for Steering Committee of the Southern California Caulerpa Action Team
Mullin BH, Anderson LW, Ditomaso JM, Eplee RE, Getsinger KD (2000) Invasive plant species. Council for Agricultural Science and Technology, Issue Paper 13
Murray SN (1998) Effectiveness of marine life refuges on southern California shores. In: Magoon OT, Converse H, Baird B, Miller-Henson M (eds) California and the world ocean ‘97. Taking a look at California’s ocean resources: an agenda for the future. American Society of Civil Engineers, Reston, pp 1453–1465
Murray SN, Fernandez L, Zertuche-Gonzalez JA (2007) Status, environmental threats, and policy considerations for invasive seaweeds for the Pacific Coast of North America. Commission on Environmental Cooperation, Montreal
Padilla DK, Williams SL (2004) Beyond ballast water: aquarium and ornamental trades as sources of invasive species in aquatic ecosystems. Frontiers in Ecology and the Environment 2:131–138
Pimentel D, Lach L, Zuniga R, Morrison D (2000) Environmental and economic costs of nonindigenous species in the United States. BioScience 50:53–65
Ribera Siguan MA (2003) Pathways of biological invasions of marine plants. In: Ruiz GM, Carlton J (eds) Invasive Species: vectors and management strategies. Island Press, Washington, DC, pp 183–226
Ruitton S, Javel F, Culioli J, Meinesz A, Pergent G, Verlaque M (2005) First assessment of the Caulerpa racemosa (Caulerpales, Chlorophyta) invasion along the French Mediterranean coast. Marine Pollution Bulletin 50:1061–1068
Ruiz GM, Carlton JT, Grosholz ED, Hines AH (1997) Global invasions of marine and estuarine habitats by non-indigenous species: mechanism, extent, and consequences. American Zoologist 37:621–632
Ruiz GM, Fofonoff PW, Carlton JT, Wonham MJ, Hines AH (2000) Invasion of coastal marine communities in North America: apparent patterns, processes, and biases. Annual Review of Ecology and Systematics 31:481–531
Ruiz GM, Reid DF (2007) Current state of understanding about the effectiveness of ballast water exchange (BWE) in reducing aquatic nonindigenous species (ANS) introductions to the Great Lakes Basin and Chesapeake Bay, USA: synthesis and analysis of existing information. National Ocean and Atmospheric Administration Technical Memorandum
Schaffelke B, Murphy N, Uthicke S (2002) Using genetic techniques to investigate the sources of the invasive alga Caulerpa taxifolia in three new locations in Australia. Marine Pollution Bulletin 44:204–210
Semmens BX, Buhle ER, Salomon AK, Pattengill-Semmens CV (2004) A hotspot of non-native marine fishes: evidence for the aquarium trade as an invasion pathway. Marine Ecology Progress Series 266:239–244
Smith JR, Fong P, Ambrose RF (2008) The impact of human visitation on mussel bed communities along the California coast: Are regulatory marine reserves effective in protecting these communities? Environmental Management 41:599–612
Stam WT, Olsen JL, Zaleski SF, Murray SN, Brown KR, Walters LJ (2006) A forensic and phylogenetic survey of Caulerpa species (Caulerpales, Chlorophyta) from the Florida coast, local aquarium shops, and e-commerce: establishing a proactive baseline for early detection. Journal of Phycology 42:1113–1124
Strayer DL (2009) Twenty years of zebra mussels: lessons from the mollusk that made headlines. Frontiers in Ecology and the Environment 7:135–141
Strecker AL, Campbell PM, Olden JD (2011) The aquarium trade as an invasion pathway in the Pacific Northwest. Fisheries 36:74–85
Szaro RC, Sexton WT, Malone CR (1998) The emergence of ecosystem management as a tool for meeting people’s needs and sustaining ecosystems. Landscape and Urban Planning 40:1–7
Verlaque M, Fritayre P (1994) Modifications des communautés algales méditerranéennes en presence de l’algue envahissante Caulerpa taxifolia (Vahl) C. Agardth. Oceanologica Acta 17:659–672
Verlaque M, Durand C, Huisman JM, Boudouresque CF, le Parco Y (2003) On the identity and the origin of the Mediterranean invasive Caulerpa racemosa (Caulerpales, Chlorophyta). European Journal of Phycology 38:325–339
Verlaque M, Afonso-Carillo J, Gil-Rodríguez MC, Durand C, Boudouresque CF, Le Parco Y (2004) Blitzkrieg in a marine invasion: Caulerpa racemosa var. cylindracea (Bryopsidales, Chlorophyta) reaches the Canary Islands (north-east Atlantic). Biological Invasions 6:269–281
Wabinitz C, Taylor M, Green E, Razak T (2003) From ocean to aquarium. UNEP WCMC, Cambridge
Walters LJ, Brown KB, Stam WT, Olsen JL (2006) E-commerce and Caulerpa: unregulated dispersal of invasive species. Frontiers in Ecology and the Environment 4:75–79
Walters LJ, Odom R, Zaleski S (2011) The aquarium hobby industry and invasive species: Has anything changed? Frontiers in Ecology and the Environment 9:206–207
Whitfield PE, Gardner T, Vives SP, Gilligan MR, Courtenay WR Jr, Ray GC, Hare JA (2002) Biological invasion of the Indo-Pacific lionfish Pterois volitans along the Atlantic coast of North America. Marine Ecology Progress Series 235:289–297
Wilcove DS, Rothstein D, Dubow J, Phillips A, Losos E (1998) Quantifying threats to imperiled species in the United States. BioScience 48:607–614
Zaleski SF, Murray SN (2006) Taxonomic diversity and geographic distributions of aquarium traded species of Caulerpa (Cholorphyta: Caulerpaceae) in southern California, USA. Marine Ecology Progress Series 314:97–108
Acknowledgments
This study was funded by (a) National Science Foundation (UMEB 0102614 and 0602922) under the California State University, Fullerton Southern California Ecosystems Research Program (SCERP); (b) University of Southern California Sea Grant; and (c) Pacific States Marine Fisheries Commission. The authors are also grateful for support provided by: (a) the Pacific Outer Continental Shelf Region, Bureau of Ocean Energy Management (BOEM), U.S. Department of the Interior; (b) the California State University, Fullerton (CSUF) Department of Biological Science; and (c) the CSUF Departmental Associated Council. The views expressed herein do not necessarily reflect the views of the funding agencies, or any of its subagencies. The authors’ would like to thank the editor and three reviewers for constructive criticism.
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Diaz, S., Smith, J.R., Zaleski, S.F. et al. Effectiveness of the California State Ban on the Sale of Caulerpa Species in Aquarium Retail Stores in Southern California. Environmental Management 50, 89–96 (2012). https://doi.org/10.1007/s00267-012-9860-3
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DOI: https://doi.org/10.1007/s00267-012-9860-3