Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Pacific Conservation Biology Pacific Conservation Biology Society
A journal dedicated to conservation and wildlife management in the Pacific region.
RESEARCH ARTICLE

Marine invasive species: establishing pathways, their presence and potential threats in the Galapagos Marine Reserve

Inti Keith A B E , Terence P. Dawson A , Ken J. Collins C and Marnie L. Campbell D
+ Author Affiliations
- Author Affiliations

A Centre for Environmental Change and Human Resilience, University of Dundee, Dundee, DD1 4HN, UK.

B Charles Darwin Foundation, Marine Science Department, Santa Cruz Island, Galapagos, Ecuador.

C Ocean and Earth Science, University of Southampton, National Oceanography Centre, Southampton SO14 3ZH, UK.

D Environmental Research Institute, University of Waikato, Hamilton, New Zealand.

E Corresponding author. Email: inti.keith@fcdarwin.org.ec

Pacific Conservation Biology 22(4) 377-385 https://doi.org/10.1071/PC15020
Submitted: 25 June 2015  Accepted: 10 June 2016   Published: 17 August 2016

Abstract

Worldwide, marine biological invasions of non-native species have increased significantly in recent years due to a rapid rise in global trade, transport and tourism. Invasions occur when non-native species are transported from one region to another and establish, often resulting in competition displacing native species and changing ecosystems. Historic literature searches were conducted along with dive surveys of the main ports and in sites around the archipelago in order to produce a baseline of which non-native species are present in the Galapagos Marine Reserve at this time. Confounding processes of anthropogenic and natural activities are increasing the potential spread of marine invasive species in the Eastern Tropical Pacific and the Galapagos Marine Reserve. We discuss the potential vectors facilitating marine invasions with the suggestion that marine traffic could be the most influential vector in the transport of marine non-natives to the Galapagos Marine Reserve. The challenge for marine park authorities is to identify those species that are likely to cause negative impacts on native biodiversity and ecosystems before they establish in the Galapagos, and to develop pre-emptive strategies that would likely include prevention as well as risk-based management strategies to remove them or to mitigate their harmful effects.

Additional keywords: bioinvasions, GMR, non-native.


References

Agencia de Regulación y Control de la Bioseguridad y Cuarentena para Galápagos (ABG) (2014). Marine traffic database. ABG, Ministerio del Ambiente, Puerto Ayora, Galapagos, Ecuador.

Agencia de Regulación y Control de la Bioseguridad y Cuarentena para Galápagos (ABG) (2015). Agency for Regulation and Control of Biosecurity and Quarantine for Galapagos. Available at: http://bioseguridadgalapagos.gob.ec [accessed 1 April 2015].

Banks, S. (2002). Ambiente físico. In ‘Reserva Marina de Galápagos. Línea Base de la Biodiversidad’. (Eds E. Danulat, and G. J. Edgar.) pp. 29–42. (Fundación Charles Darwin/Servicio Parque Nacional Galápagos: Santa Cruz, Galápagos, Ecuador.)

Banks, S. A., Acuña, D., Calderón, R., Garske-Garcia, L., Edgar, G. E., Keith, I., Kuhn, A., Pépolas, R., Ruiz, D., Suarez, J., Tirado-Sánchez, N., Vera, M., Vinueza, L., and Wakefield, E. (2014). Manual de Monitoreo Submareal Ecológico para la RMG. Informe Técnico. Fundación Charles Darwin, Puerto Ayora, Galápagos, Ecuador.

Banta, W. C., and Redden, J. C. (1990). A checklist of the Bryozoa of the Galapagos Proceedings of the Biological Society of Washington 103, 789–802.

Brandt, M., and Guarderas, P. (2002). Erizos de Mar. In ‘Reserva Marina de Galápagos. Línea Base de la Biodiversidad’. (Eds E. Danulat, and G. J. Edgar.) pp. 403–425. (Fundación Charles Darwin/Servicio Parque Nacional Galápagos: Santa Cruz, Galápagos, Ecuador.)

Bright, D. (1966). The land crabs of Costa Rica. Biotropica 14, 183–203.

Bungartz, F., Herrera, H. W., Jaramillo, P., Tirado, N., Jiménez-Uzcátegui, G., Ruiz, D., Guézou, A., and Ziemmeck, F. (Eds.) (2009). Charles Darwin Foundation Galapagos Species Checklist – Lista de Especies de Galápagos de la Fundación Charles Darwin. Charles Darwin Foundation, Puerto Ayora, Galápagos. Available at: http://www.darwinfoundation.org/datazone/checklists/ [accessed13 Apr 2011].

Bustamante, R., Collins, K. J., and Bensted-Smith, R. (2000). Biodiversity conservation in the Galápagos Marine Reserve. In ‘Proccedings of the Symposium, Science for Conservation in Galápagos, 15th April 1998’. Institut Royal des Science Naturelles de Belgique, Brussels Bulletin de l’Institut Royal des Science Naturelles de Belgique 70(supplement), 31–38.

Campbell, M. L., and Hewitt, C. L. (2007). Preliminary assessment of marine biosecurity risks to the Galapagos Islands. National Centre for Marine & Coastal Conservation.

Campbell, M. L., and Hewitt, C. L. (2013). Protecting high-value areas from introduced marine species. Management of Biological Invasions 4, 171–189.
Protecting high-value areas from introduced marine species.Crossref | GoogleScholarGoogle Scholar |

Campbell, M. L., Keith, I., Hewitt, C. L., Dawson, T. P., and Collins, K. (2015). Evolving marine biosecurity in the Galapagos Islands. Management of Biological Invasions 6, 227–230.
Evolving marine biosecurity in the Galapagos Islands.Crossref | GoogleScholarGoogle Scholar |

Carlton, J. T. (1996). Biological invasions and cryptogenic species. Ecology 77, 1653–1655.
Biological invasions and cryptogenic species.Crossref | GoogleScholarGoogle Scholar |

Castilla, J. C., Uribe, M., Bahamonde, N., Clarke, M., Desqueyroux-Faúndez, R., Kong, I., Moyano, H., Rozbaczylo, N., Santelices, B., Valdovinos, C., and Zavala, P. (2005). Down under the Southeastern Pacific: marine non-indigenous species in Chile. Biological Invasions 7, 213–232.
Down under the Southeastern Pacific: marine non-indigenous species in Chile.Crossref | GoogleScholarGoogle Scholar |

Causton, C., Campbell, M., Hewitt, C., and Boada, R. (2008). Riesgos Asociados con las Rutas Marítimas Hacia y Entre Galápagos. Fundación Charles Darwin, Puerto Ayora, Galápagos, Ecuador.

Chan, S. (2012). Japanese tsunami debris and invasive species: lessons being learned in Oregon and applications for the region. Oregon State University, Oregon Sea Grant, National Sea Grant and NOAA.

Charles Darwin Foundation (CDF) and World Wildlife Fund (WWF) (2002). A biodiversity vision for the Galapagos Islands: based on international workshop of conservation biologists in Galapagos in May 1999. World Wildlife Fund.

Chavez, F. P., and Brusca, R. C. (1991). , .
Crossref | GoogleScholarGoogle Scholar |

Chualáin, F. N., Maggs, C. A., Saunders, G. W., and Guiry, M. D. (2004). The invasive genus Asparagopsis (Bonnemaisoniaceae, Rhodophyta): molecular systematics, morphology, and ecophysiology of Falkenbergia isolates. Journal of Phycology 40, 1112–1126.
The invasive genus Asparagopsis (Bonnemaisoniaceae, Rhodophyta): molecular systematics, morphology, and ecophysiology of Falkenbergia isolates.Crossref | GoogleScholarGoogle Scholar |

Cohen-Rengifo, M., Bessudo, S., and Soler, G. (2009). Echinoderms, Malpelo fauna and flora sanctuary, Colombian Pacific: new reports and distributional issues. Check List 5, 702–711.

Danulat, E., and Edgar, G. J. (2002). Reserva Marina de Galápagos. Línea Base de la Biodiversidad. Fundación Charles Darwin/Servicio Parque Nacional Galápagos, Santa Cruz, Galápagos, Ecuador.

Dawson, E. Y. (1963). New records of marine algae from the Galapagos Islands. Pacific Naturalist 4, 1–23.

Dawson, T. P., Jackson, S. T., House, J. I., Prentice, I. C., and Mace, G. M. (2011). Beyond predictions: biodiversity conservation in a changing climate. Science 332, 53–58.
Beyond predictions: biodiversity conservation in a changing climate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXjvVyisbk%3D&md5=9d94b68035a0fd53b8ac4100c70e1555CAS | 21454781PubMed |

Edgar, G. J., Banks, S. A., Brandt, M., Bustamante, R. H., Chiriboga, A., Earle, S. A., Garske, L. E., and Wellington, G. M. (2010). El Niño, grazers and fisheries interact to greatly elevate extinction risk for Galapagos marine species. Global Change Biology 16, 2876–2890.
El Niño, grazers and fisheries interact to greatly elevate extinction risk for Galapagos marine species.Crossref | GoogleScholarGoogle Scholar |

Eldredge, L. G., and Smith, C. M. (2001). A guidebook of introduced marine species in Hawai’’i. Bishop Museum Technical Report 21. Bishop Museum, Honolulu. A1–A54; B1–B60 p.

Elton, C. S. (1958). ‘The Ecology of Invasions by Animals and Plants.’ (Methuen: London.)

Emerton, L., and Howard, G. (2008). A toolkit for the economic analysis of invasive species. Available at: http://www.issg.org/pdf/publications/GISP/Guidelines_Toolkits_BestPractice/Emerton&Howard_2008_EN.pdf [accessed 15 September 2014].

Farlow, W. G. (1902). Algae. In ‘Flora of the Galapagos Islands’. (Ed. B. L. Robinson.) Proceedings of the American Academy of Arts and Sciences 38, 89–99.

Garth, J. S. (1991). Taxonomy, distribution and ecology of Galapagos Brachyura. In ‘Galapagos Marine Invertebrates’. (Ed. M. J. James.) pp. 123–145. (Springer: New York.)

Godwin, L. S. (2003). Hull fouling of maritime vessels as a pathway for marine species invasions to the Hawaiian Islands. Biofouling 19, 123–131.
Hull fouling of maritime vessels as a pathway for marine species invasions to the Hawaiian Islands.Crossref | GoogleScholarGoogle Scholar | 14618713PubMed |

Grenier, C. (2010). La apertura geográfica de Galápagos. In ‘Informe Galápagos 2009–2010’. pp. 123–131. (Puerto Ayora, Galápagos, Ecuador.)

Guiry, M. D., and Guiry, G. M. (2015). AlgaeBase. National University of Ireland, Galway. Available at: http://www.algaebase.org [accessed 30 October 2015].

Hare, J. A., and Whitfield, P. E. (2003). An integrated assessment of the introduction of lionfish (Pterois volitans/miles complex) to the western Atlantic Ocean. NOAA Technical Memorandum NOS NCCOS 2, 1–21.

Hewitt, C. L., and Campbell, M. L. (2013). Facilitated dispersal: overwhelming biogeographic boundaries. Paper presented at 8th International Conference on Marine Bioinvasions. Vancouver, Canada.

Hewitt, C. L., and Hayes, K. R. (2002). Risk assessment of marine biological invasions. In ‘Invasive Aquatic Species of Europe. Distribution, Impacts and Management’. (Eds E. Leppäkoski, S. Gollasch, S. Olenin) pp. 456–466. (Springer: Netherlands.)

Hickman, C. P. (1997). ‘Crustaceans of Galápagos: a Field Guide to the Common Barnacles, Shrimp, Lobsters and Crabs of the Galapagos Islands.’ (Lexington, VA.)

Hickman, C. P. (1998). ‘A Field Guide to Sea Stars and Other Echinoderms of Galápagos.’ (Sugar Spring Press: Lexington, VA.)

Hickman, C. P. (2008). ‘A Field Guide to Corals and other Radiates of Galapagos: an Illustrated Guidebook to the Corals, Anemones, Zoanthids, Black Corals, Gorgonians, Sea Pens, and Hydroids of the Galápagos Islands.’ (Sugar Spring Press: Lexington, VA.)

Hickman, C. P. (2009). Evolutionary responses of marine invertebrates to insular isolation in Galapagos. Galapagos Research 66, 32–42.

Hilliard R. (2004). Best practice for the management of introduced marine pests – a review. Global Invasive Species Programme, IUCN.

Hulme, P. E. (2009). Trade, transport and trouble: managing invasive species pathways in an era of globalization. Journal of Applied Ecology 46, 10–18.
Trade, transport and trouble: managing invasive species pathways in an era of globalization.Crossref | GoogleScholarGoogle Scholar |

Inglis, G. J., Hayden, B. J., and Nelson, W. A. (2006). Are the marine biotas of island ecosystems more vulnerable to invasion? In ‘Ecological Studies. Vol. 186’. (Eds R. B. Allen, and W. G. Lee.) pp. 119–135. (Springer-Verlag: Berlin.)

Invasive Species Specialist Group (ISSG) (2015). The Global Invasive Species Database. Version 2015.1.

IPCC (2007). Summary for policymakers. In ‘Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change’. p. 17. (Cambridge University Press: Cambridge.)

IUCN (2011). IUCN Red List of Threatened Species. Version 2012.2. Available at: http://www.iucnredlist.org [accessed 1 April 2013].

Jäger, H., Tye, A., and Kowarik, I. (2007). Tree invasion in naturally treeless environments: impacts of quinine (Cinchona pubescens) trees on native vegetation in Galápagos. Biological Conservation 140, 297–307.
Tree invasion in naturally treeless environments: impacts of quinine (Cinchona pubescens) trees on native vegetation in Galápagos.Crossref | GoogleScholarGoogle Scholar |

Keith, I., and Martinez, P. (2014). Especies Invasoras Marinas – Prevención, detección y manejo. Documento Técnico. Fundación Charles Darwin. Puerto Ayora, Galápagos, Ecuador.

Kolar, C. S., and Lodge, D. M. (2002). Ecological predictions and risk assessment for alien fishes in North America. Science 298, 1233–1236.
Ecological predictions and risk assessment for alien fishes in North America.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XosVerurg%3D&md5=def357236f336061de6e517bc445fc8aCAS | 12424378PubMed |

Loope, L. L., Hamann, O., and Stone, C. P. (1988). Comparative conservation biology of oceanic archipelagoes: Hawaii and the Galapagos. Bioscience 38, 272–282.
Comparative conservation biology of oceanic archipelagoes: Hawaii and the Galapagos.Crossref | GoogleScholarGoogle Scholar |

LOREG (1998). Ley Orgánica de Régimen Especial para la Conservación y el Desarrollo Sustentable de la Provincia de Galápagos. Congreso Nacional. Registro Oficial No 278 del 18 de marzo de 1998. Ecuador.

McBride, G. M. (1918). The Galapagos Islands. Geographical Review 6, 229–239.
The Galapagos Islands.Crossref | GoogleScholarGoogle Scholar |

McCann, L., Keith, I., Carlton, J. T., Ruiz, G. M., Dawson, T. P., and Collins, K. J. (2015). First record of the non-native bryozoan Amathia (=Zoobotryon) verticillata (delle Chiaje, 1822) (Ctenostomata) in the Galapagos Islands. Bioinvasions Records 4, 255–260.
First record of the non-native bryozoan Amathia (=Zoobotryon) verticillata (delle Chiaje, 1822) (Ctenostomata) in the Galapagos Islands.Crossref | GoogleScholarGoogle Scholar |

Molnar, J. L., Gamboa, R. L., Revenga, C., and Spalding, M. D. (2008). Assessing the global threat of invasive species to marine biodiversity. Frontiers in Ecology and the Environment 6, 485–492.
Assessing the global threat of invasive species to marine biodiversity.Crossref | GoogleScholarGoogle Scholar |

Muromtsev, A. M. (1963). ‘The Principal Hydrology Features of the Pacific Ocean.’ (Jerusalem Post Press.)

Pagad, S., Hayes, K., Katsanevakis, S., and Costello, M. J. (2015). World Register of Introduced Marine Species (WRIMS). Available at: http://www.marinespecies.org/introduced (accessed 30 October 2015.)

Paris, C. B., Helgers, J., Van Sebille, E., and Srinivasan, A. (2013). Connectivity Modeling System: a probabilistic modelling tool for the multi-scale tracking of biotic and abiotic variability in the ocean. Environmental Modelling & Software 42, 47–54.
Connectivity Modeling System: a probabilistic modelling tool for the multi-scale tracking of biotic and abiotic variability in the ocean.Crossref | GoogleScholarGoogle Scholar |

Parra, D. M., Andrés, M., Jiménez, J., Banks, S., and Muñoz, J. P. (2013). Evaluación de la incidencia de impacto de embarcaciones y distribución de la tortuga verde (Chelonia mydas) en Galápagos. Documento Técnico. Fundación Charles Darwin. Puerto Ayora, Galápagos, Ecuador.

Perry, A. L., Low, P. J., Ellis, J. R., and Reynolds, J. D. (2005). Climate change and distribution shifts in marine fishes. Science 308, 1912–1915.
Climate change and distribution shifts in marine fishes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXlsVWmtbg%3D&md5=188655b8a809aef6b70c1ee10e14863dCAS | 15890845PubMed |

Pineda, J., Hare, J. A., and Sponaungle, S. (2007). Larval transport and dispersal in the coastal ocean and consequences for population connectivity. Oceanography 20, 22–39.
Larval transport and dispersal in the coastal ocean and consequences for population connectivity.Crossref | GoogleScholarGoogle Scholar |

Piu, M., and Muñoz, E. (2008). General characteristics of the tourist fleet in Galapagos and its compliance with environmental standards. In ‘Galapagos Report 2007–2008’. Puerto Ayora, Galapagos, Ecuador.

Rahel, F. J. (2002). Using current biogeographic limits to predict fish distributions following climate change. In ‘Fisheries in a Changing Climate, American Fisheries Society Symposium 32’. (Ed. Nature A. McGinn) pp. 99–112. (American Fisheries Society.)

Ruiz, D., and Ziemmeck, F. (2011). CDF Checklist of Galápagos Green Algae – FCD Lista de especies de Algas verdes de Galápagos. In ‘Charles Darwin Foundation Galapagos Species Checklist – Lista de Especies de Galápagos de la Fundación Charles Darwin’. (Eds F. Bungartz, H. Herrera, P. Jaramillo, N. Tirado, G. Jímenez-Uzcategui, D. Ruiz, A. Guézou, and F. Ziemmeck.) (Charles Darwin Foundation/ Fundación Charles Darwin, Puerto Ayora, Galápagos.) Available at: http://www.darwinfoundation.org/datazone/checklists/algae/chlorophyta/ [accessed 13 April 2011].

Ryland, J. S., Bishop, J. D. D., De Blauwe, H., El Nagar, E., Minchin, D., Wood, C. A., and Yunnie, A. L. E. (2011). Alien species of Bugula (Bryozoa) along the Atlantic coasts of Europe Aquatic Invasions 6, 17–31.
Alien species of Bugula (Bryozoa) along the Atlantic coasts of EuropeCrossref | GoogleScholarGoogle Scholar |

Sachs, J., and Ladd, N. (2010). Climate and oceanography of the Galápagos in the 21st Century: expected changes and research needs. Galapagos Research 67, 50–54.

Sánchez, J. A., Gómez, C. E., Escobar, D., and Dueñas, L. F. (2011). Diversidad, abundancia y amenazas de los octocorales de la isla Malpelo, Pacífico Oriental Tropical, Colombia. Boletín Investigaciones Marinas y Costeras 40, 139–154.

Schlöder, C., Canning-Clode, J., Saltonstall, K., Strong, E. E., Ruiz, G. M., and Torchin, M. E. (2013). The Pacific bivalve Anomia peruviana in the Atlantic: a recent invasion across the Panama Canal. Aquatic Invasions 8, 443–448.
The Pacific bivalve Anomia peruviana in the Atlantic: a recent invasion across the Panama Canal.Crossref | GoogleScholarGoogle Scholar |

Seebens, H., Gastner, M., and Blasius, B. (2013). The risk of marine bioinvasion caused by global shipping. Ecology Letters 16, 782–790.
The risk of marine bioinvasion caused by global shipping.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3srns1Oruw%3D%3D&md5=4d04858a932a035f84a302cb8672f246CAS | 23611311PubMed |

Semtner, A. J. (1995). Modeling ocean circulation. Science 269, 1379–1384.
Modeling ocean circulation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXnvFClu7c%3D&md5=1add204bcfe7a0fcfb2c2e854b47637eCAS | 17731147PubMed |

Simberloff, D. (1995). Why do introduced species appear to devastate islands more than mainland areas? Pacific Science 49, 87–97.

Taylor, W. R. (1945). Pacific marine algae of the Allan Hancock Expeditions to the Galápagos Islands. Allan Hancock Pacific Expeditions 12, 1–528.

Vegter, A. C., Barletta, M., Beck, C., Borrero, J., Burton, H., Campbell, M. L., Eriksen, M., Eriksson, C., Estrades, A., Gilardi, K. V. K., Hardesty, B. D., Assuncao, J., do Sul, I., Lavers, J. L., Lazar, B., Lebreton, L., Nichols, W. J., Ribic, C. A., Ryan, P. G., Schuyler, Q. A., Smith, S. D. A., Takada, H., Townsend, K., Wabnitz, C. C. C., Wilcox, C., Young, L. C., and Hamann, M. (2014). Global research priorities to mitigate plastic pollution impacts on marine wildlife. Endangered Species Research 25, 225–247.
Global research priorities to mitigate plastic pollution impacts on marine wildlife.Crossref | GoogleScholarGoogle Scholar |

Vieira, L. M., Winston, J. E., and Fehlauer-Ale, K. H. (2012). Nine new species of Bugula Oken (Bryozoa: Cheilostomata) in Brazilian shallow waters. PLoS One 7, e40492.
Nine new species of Bugula Oken (Bryozoa: Cheilostomata) in Brazilian shallow waters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhtVOnsLfN&md5=a1fbe60540eaf81da546d5546393423bCAS | 22808173PubMed |

Vitousek, P. M., D’Antonio, C. M., Loope, L. L., Rejmanek, M., and Westbrooks, R. (1997). Introduced species: a significant component of human-caused global change. New Zealand Journal of Ecology 21, 1–16.

Vogler, C., Benzie, J., Lessios, H., Barber, P., and Wörheide, G. (2008). A threat to coral reefs multiplied? Four species of crown-of-thorns starfish. Biology Letters 4, 696–699.
A threat to coral reefs multiplied? Four species of crown-of-thorns starfish.Crossref | GoogleScholarGoogle Scholar | 18832058PubMed |

Wonham, M. J., Carlton, J. T., Ruiz, G. M., and Smith, L. D. (2000). Fish and ships: relating dispersal frequency to success in biological invasions. Marine Biology 136, 1111–1121.
Fish and ships: relating dispersal frequency to success in biological invasions.Crossref | GoogleScholarGoogle Scholar |

Wonham, M. J., Walton, W. C., Ruiz, G. M., Frese, A. M., and Galil, B. S. (2001). Going to the source: role of the invasion pathway in determining potential invaders. Marine Ecology Progress Series 215, 1–12.
Going to the source: role of the invasion pathway in determining potential invaders.Crossref | GoogleScholarGoogle Scholar |

WoRMS Editorial Board (2015). World Register of Marine Species. Available at: http://www.marinespecies.org [accessed 2 November 2015].

Zapata, C. (2006). Evaluación de la eficiencia técnica-operativa del Sistema de Inspección y Cuarentena para Galápagos (SICGAL). Charles Darwin Foundation, Puerto Ayora, Galápagos.