Assessing biosecurity risk associated with the importation of non-indigenous microalgae

Environmental Research

Volumn 111, Issue 7, 2011, Pages 989-998

  Campbell, Marnie L ^a  

^a CENTRAL QUEENSLAND UNIVERSITY   (Australia)

Author keywords

Aquaculture; Biosecurity; Food security; Introduced marine species; Microalgae

Indexed keywords

AQUACULTURE INDUSTRY; BIODIVERSITY; BIOSAFETY; DATA SET; DECISION MAKING; ENVIRONMENTAL RISK; FOOD SECURITY; IMPORT; INVASIVE SPECIES; MANAGEMENT PRACTICE; MICROALGA; RESEARCH INSTITUTION; RISK ASSESSMENT;

AQUACULTURE; ARTICLE; BIOSAFETY; BIOSECURITY RISK; DECISION TREE; ENVIRONMENT; MICROALGA; NEW ZEALAND; NONHUMAN; PRIORITY JOURNAL; RISK ASSESSMENT;

AQUACULTURE; DECISION MAKING; INTRODUCED SPECIES; MICROALGAE; NEW ZEALAND; RISK ASSESSMENT;

NEW ZEALAND;

EID: 80053220387     PISSN: 00139351     EISSN: 10960953     Source Type: Journal    
DOI: 10.1016/j.envres.2011.02.004     Document Type: Article

References (72)

1. AFS. International Convention on the Control of Harmful Anti-Fouling Systems on Ships. International Maritime Organization, London. 2001. Available at 〈〉 (accessed 01/11/10). http://www.imo.org.
2. Backer, L.C., Fleming, L.E., Rowan, A.D., Baden, D.G., 2001. Epidemiology and public health of human illness associated with harmful marine phytoplankton. WHO/UNESCO HAB Handbook. Available from 〈〉 (accessed 01/11/10). http://www.rsmas.miami.edu/groups/niehs/science/pdf/Epi%20and%20public%20health---marine%20phytoplankton.pdf.
3. Biosecurity Strategy, 2003. Tiakina Aotearoa-Protect New Zealand: The Biosecurity Strategy for New Zealand. Ministry of Agriculture and Forestry (MAF), Wellington. Available from 〈〉 (accessed 01/11/10). http://www.biosecurity.govt.nz/biosec/sys/strategy/biostrategy/biostrategynz.
4. Boalch, G.T., 1994. The introduction of non-indigenous marine species to Europe: Planktonic Species. In: Boudouresque CF, Briand F, Nolan C (Eds.). Introduced Species in European Coastal Waters. European Commission Ecosystems Research Report, vol. 8, pp. 28-31.
5. Boudouresque C.F., Verlaque M. Biological pollution in the Mediterranean Sea: invasive versus introduced macrophytes. Marine Pollution Bulletin 2002, 44(1):32-38.
6. Brown M., Robert R. Preparation and assessment of microalgal concentrates as feeds for larval and juvenile Pacific oyster (Crassostrea gigas). Aquaculture 2002, 207(3-4):289-309.
7. Burkholder J.M., Glasgow H.B., Hobbs C.W. Fish kills linked to a toxic ambush-predator dinoflagellate: distribution and environmental conditions. Marine Ecology Progress Series 1995, 124:43-61.
8. Campbell, M.L.,2006. Risk analysis of microalgae Import Health Standard listed marine species. All Oceans Ecology Report No. 200602. All Oceans Ecology, Melbourne.
9. Campbell M.L. Organism impact assessment: risk analysis for post-incursion management. ICES Journal of Marine Science 2008, 65:795-804.
10. Campbell M.L. An overview of risk assessment in a marine biosecurity context. Biological Invasions in Marine Ecosystems. Ecological, Management, and Geographic Perspectives 2009, 353-373. Springer, Heidelberg, Germany. G. Rilov, J. Crooks (Eds.).
11. Campbell M.L., Gallagher C. Assessing the relative effects of fishing on the New Zealand marine environment through risk assessment. ICES Journal of Marine Science 2007, 64:256-270.
12. Campbell, M.L., Hewitt, C.L., 2008. Introduced marine species risk analysis-aquaculture. FAO Fisheries and Aquaculture Technical Paper 519, Rayong, Thailand.
13. Campbell M.L., Grage A., Mabin C.J.T., Hewitt C.L. Conflict between international treaties: failing to mitigate the effects of introduced marine species. Dialogue 2009, 28(1):46-56.
14. Carlton J.T. Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanography and Marine Biology: An Annual Review 1985, 23:313-371.
15. Carlton J.T., Ruiz G.M. The magnitude and consequence of bioinvasions in marine ecosystems. Implications for conservation biology. Marine Conservation Biology. The Science of Maintaining the Sea's Biodiversity 2005, 123-148. Island Press. E.A. Norse, L.B. Crowder (Eds.).
16. CBD, 1992. Convention on Biological Diversity. Available from 〈〉 (accessed 01/11/10). http://www.cbd.int/convention/convention.shtml.
17. Chandrasekera W.U., Fernando M.A.S.T. Accidental introduction of alien plankton into the Sri Lankan coastal zone through ballast water of cargo ships. Sri Lanka Journal of Aquatic Science 2009, 14:87-103.
18. Chapman J.W., Miller T.W., Coan E.V. Live seafood species as recipes for invasions. Conservation Biology 2003, 17:1386-1395.
19. Crawford C. Qualitative risk assessment of the effects of shellfish farming on the environment in Tasmania, Australia. Ocean and Coastal Management 2003, 46(1-2):47-68.
20. Delabbio J., Murphy B.R., Johnson G.R., McMullin S.L. An assessment of biosecurity utilization in the recirculation sector of finfish aquaculture in the United States and Canada. Aquaculture 2004, 242:165-179.
21. Deeds J.R., Terlizzi D.E., Adolf J.E., Stoeker D.K., Place A.R. Toxic activity from cultures of Karlodinium micrum (=Gyrodinium galatheanum) (Dinophyceae)-a dinoflagellate associated with fish mortalities in an estuarine aquaculture facility. Harmful Algae 2002, 1(2):169-189.
22. Economidis P.S., Dimitriou E., Pagoni R., Michaloudi E., Natsis L. Introduced and translocated fish species in the inland waters of Greece. Fisheries Management and Ecology 2000, 7:239-250.
23. Eno N.C., Clark R.A., Sanderson W.G. Non-native marine species in British waters" a review and directory 1997, Joint Nature Conservation Committee, Peterborough; United Kingdom.
24. FAO, 2003. Health management and biosecurity maintenance in white shrimp (Penaeus vannamei) hatcheries in Latin America. FAO Fisheries Technical Paper 450, Rome FAO.
25. Fletcher W.J. The application of qualitative risk assessment methodology to prioritize issues for fisheries management. ICES Journal of Marine Science 2005, 62:1576-1587.
26. Flewelling L.J., Naar J.P., Abbott J.P., Baden D.G., Barros N.B., Bossart G.D., Bottein M.-Y.D., Hammond D.G., Haubold E.M., Heil C.A., Henry M.S., Jacocks H.M., Leighfield T.A., Pierce R.H., Picthford T.D., Rommel S.A., Scott P.S., Steidinger K.A., Truby E.W., Van Dolah F.M., Landsberg J.H. Brevetoxicosis: Red tides and marine mammal mortalities. Nature 2005, 435:755-756.
27. Flores-Aguilar R.A., Gutierrez A., Ellwanger A., Searcy-Bernal R. Development and current status of abalone aquaculture in Chile. Journal of Shellfish Research 2007, 26:705-711.
28. Fortin D.R., Renton M.S. Consumer acceptance of genetically modified foods in New Zealand. British Food Journal 2003, 105:42-58.
29. Glasgow H.B., Burkholder J.M., Mallin M.A., Deamer-Melia N.J., Reed R.E. Field ecology of toxic Pfiesteria complex species and a conservative analysis of their role in estuarine fish kills. Environ. Health Perspectives 2001, 109(5):715-730.
30. Gleditsch K.S. Expanded trade and GDP data. Journal of Conflict Resolution 2002, 46:712-724.
31. Gollasch S. International collaboration on marine bioinvasions-the ICES response. Marine Pollution Bulletin 2007, 55(7-9):353-359.
32. Goulletquer P., Bachelet G., Sauriau P.G., Noel P. Open Atlantic coast of Europe-a century of introduced species into French waters. Invasive Aquatic Species of Europe 2002, 276-290. Kluwer Academic Publications, Netherlands. E. Leppakoski, S. Gollasch, S. Olenin (Eds.).
33. Haack R.A., Poland T.M. Evolving management strategies for a recently discovered exotic forest pest: the pine shoot beetle, Tomicus piniperda (Coleoptera). Biologial Invasions 2001, 3(3):307-322.
34. Hallegraeff G.M., Bolch C.J. Transport of diatom and dinoflagellate resting spores in ships' ballast water: implications for plankton biogeography and aquaculture. Journal of Plankton Research 1992, 14:1067-1084.
35. Hallegraeff G.M. Transport of toxic dinoflagellates via ships' ballast water: bioeconomic risk assessment and efficacy of possible ballast water management strategies. Marine Ecology Progress Series 1998, 168:297-309.
36. Harvey M., Gilbert M., Gauthier D., Reid D.M. A preliminary assessment of risks for the ballast water-mediated introduction of nonindigenous marine organisms in the estuary and Gulf of St. Lawrence. Canadian Technical Report of Fisheries and Aquatic Sciences 1999, 2268:1-35.
37. Heil C.A., Glibert P.M., Al-Sarawi M., Faraj M., Behbehani M., Husain M. First record of a fish-killing Gynodinium sp. bloom in Kuwait Bay, Arabian Sea: chronology of event and potential causes. Marine Ecology Progress Series 2001, 214:15-23.
38. Hewitt C.L., Campbell M.L. Mechanisms for the prevention of marine bioinvasions for better biosecurity. Marine Pollution Bulletin 2007, 55:395-401.
39. Hewitt C.L., Campbell M.L., Gollasch S. Alien Species in Aquaculture. Considerations for Responsible Use 2006, IUCN, Gland.
40. Hewitt C.L., Everett R.A., Parker N. Examples of Current International, Regional and National Regulatory Frameworks for Preventing and Managing Marine Bioinvasions. Biological Invasions in Marine Ecosystems: Ecology, Conservation and Management Perspectives 2009, 335-349. Springer, Heidelberg, Germany. G. Rilov, J. Crooks, J. (Eds.).
41. Hopkins C.C.E.,2001. Actual and potential effects of introduced marine organisms in Norwegian waters, including Svalbard. Research report, 2001-01. Directorate for Nature Management, Trondheim.
42. HSNO, 1996. Hazardous Substances and New Organisms Act. Available at 〈〉 (accessed 01/11/10). http://www.osh.govt.nz/law/hsno.shtml.
43. ICES, 2005. ICES Code of Practice on the Introductions and Transfers of Marine Organisms. ICES, Denmark. Available from 〈〉 (accessed 01/11/10). http://www.ices.dk/reports/general/2004/ICESCOP2004.pdf.
44. IPPC, 1951. International Plant Protection Convention. Food and Agriculture Organization, Rome. Available from 〈〉 (accessed 01/11/10). https://www.ippc.int/IPP/En/default.jsp.
45. Iwami S., Takeuchi Y., Korobeinikov A., Liu X. Prevention of avian influenza epidemic: what policy should we choose? Journal of Theoretical Biology 2008, 252(4):732-741.
46. Jansson, K.,1994. Alien species in the marine environment. Swedish Environmental Protection Agency Report 4357.
47. Lee J., Igarashi T., Fraga S., Dahl E., Hovgaard P., Yasumoto T. Determination of diarrhetic shellfish toxins in various dinoflagellate species. Journal of Applied Phycology 1989, 1(2):147-152.
48. Alien Species in European Waters 2002, Kluwer Academic Publications, Netherlands. E. Leppakoski, S. Gollasch, S. Olenin (Eds.).
49. Leppakoski E., Olenin S. Non-native species and rates of spread: lessons from the brackish Baltic Sea. Biological Invasions 2000, 2:151-163.
50. Minchin D. The transport and spread of living aquatic species. The Ecology of Transportation: Managing Mobility for the Environment 2006, 77-97. Springer, Germany. J. Davenport, J.L. Davenport (Eds.).
51. Minchin D. A checklist of alien and cryptogenic aquatic species in Ireland. Aquatic Invasions 2007, 2(4):341-366.
52. Ribera M.A., Boudouresque C.-F. Introduced plants, with special reference to macroalgae: mechanisms and impact. Progress in Phycological Research 1995, 11:217-268.
53. Rigby G.R., Hallegraeff G.M., Sutton C. Novel ballast water heating technique offers cost-effective treatment to reduce the risk of global transport of harmful marine organisms. Marine Ecology Progress Series 1999, 191:289-293.
54. Rue E., Bruland K. Domoic acid binds iron and copper: a possible role for the toxin produced by the marine diatom Pseudo-nitzschia. Marine Chemistry 2001, 76:127-134.
55. Ruiz G.M., Fofonoff P., Carlton J.T., Wonham M.J., Hines A.H. Invasion of coastal marine communities in North America: apparent patterns, processes and biases. Annual Review of Ecology and Systematics 2000, 31:481-531.
56. Saunders C., Cagatay S. Commercial release of first-generation genetically modified food products in New Zealand: using a partial equilibrium trade model to assess the impact on producer returns in New Zealand. The Australian Journal of Agriculture and Resource Economics 2003, 47:233-259.
57. Scholin C., Gulland F., Doucette G.J., Benson S., Busman M., Chavez F.P., Cordaro J., DeLong R., De Voeglaere A., Harvey J., Haulena M., Lefebvre K., Lipscomb T., Loscutoff S., Lowenstine L.J., Marin R., Miller P.E., McLellan W.A., PDR Moeller, Powell C.L., Rowles T., Silvagni P., Silver M., Spraker T., Trainer V., Van Dolah F. Mortality of sea lions along the central California coast linked to a toxic diatom bloom. Nature 2000, 403:80-84.
58. Schwindt E., Bortolus A., Iribarne O.O. Invasion of a reef-builder polychaete: direct and indirect impacts on the native benthic community structure. Biological Invasions 2001, 3(2):137-149.
59. Sierra-Beltran A.P., Cruz A., Nunez E., Del Villar L.M., Cerecero J., Ochoa J.L. An overview of the marine food poisoning in Mexico. Toxicon 1998, 36(1):1493-1502.
60. Simons, S.A., de Poorter, M., (Eds.), 2009. Best practices in pre-import risk screening for species of live animals in international trade. In: Proceedings of an Expert Workshop on Preventing Biological Invasions, University of Notre Dame, Indiana, USA, 9-11 April 2008. Global Invasive Species Programme, Nairobi, Kenya.
61. Standards Australia, 2000. Australian and New Zealand Standard. Risk Management. Standards Australia, Sydney.
62. Standards Australia, 2004. Australian and New Zealand Standard. Risk Management. Standards Australia, Sydney.
63. Streftaris N., Zenetos A., Papthanassiou E. Globalisation in marine ecosystems: the story of non-indigenous marine species across European Seas. Oceaongraphy and Marine Biology: An Annual Review 2005, 43:419-453.
64. Taylor F.J.R., Haigh R. Spatial and temporal distributions of microplankton during the summers of 1992-1993 in Barkley Sound, British Columbia, with emphasis on harmful species. Canadian Journal of Fisheries and Aquatic Sciences 1995, 53:2310-2322.
65. Tlusty M. The benefits and risks of aquacultural production for the aquarium trade. Aquaculture 2002, 205:203-219.
66. UNCLOS, 1982. United Nations Convention on the Law of the Sea. Available from 〈〉 (accessed 01/11/10). http://www.un.org/Depts/los/index.htm.
67. Whittington R.J., Chong R. Global trend in ornamental fish from an Australian perspective: the case for revised import risk analysis and management strategies. Preventative Veterinary Medicine 2007, 81(1-3):92-116.
68. Work T.T., McCullough D.G., Cavey J.F., Komsa R. Arrival rate of nonindigenous insect species into the United States through foreign trade. Biological Invasions 2005, 7(2):323-332.
69. World Heritage, 1972. Available from 〈〉 (accessed 01/11/10). http://whc.unesco.org/archive/convention-en.pdf.
70. 2001, Turkish Marine Research Foundation, Istanbul, Turkey. Y. Zaitsev, B. Orturk (Eds.).
71. Zhang F., Dickman M. Mid-ocean exchange of container vessel ballast water. 1: seasonal factors affecting the transport of harmful diatoms and dinoflagellates. Marine Ecology Progress Series 1999, 176:243-251.
72. Zhang F., Dickman M. Mid-ocean exchange of container vessel ballast water. 2: effects if vessel type in the transport of diatoms and dinoflagellates from Manzillo, Mexico, to Hong Kong, China. Marine Ecology Progress Series 1999, 176:253-262.