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Marine and Freshwater Research Marine and Freshwater Research Society
Advances in the aquatic sciences
RESEARCH ARTICLE

Potential invasions of phytoplankton in ship ballast water at South Korean ports

Bonggil Hyun A , Kyoungsoon Shin A , Min-Chul Jang A , Pung-Guk Jang A , Woo-Jin Lee A , Chul Park B and Keun-Hyung Choi A B C
+ Author Affiliations
- Author Affiliations

A Ballast Water Research Center, Korea Institute of Ocean Science and Technology, Geoje, 656-830, Republic of Korea.

B Department of Oceanography and Ocean Environmental Sciences, Chungnam National University, 99 Daehak-ro, Yuseong-gu, Daejeon 305-764, Republic of Korea.

C Corresponding author. Email: keunhchoi@cnu.ac.kr

Marine and Freshwater Research 67(12) 1906-1917 https://doi.org/10.1071/MF15170
Submitted: 28 April 2015  Accepted: 24 September 2015   Published: 10 December 2015

Abstract

We studied the phytoplankton communities in ballast water in ships that arrived at two South Korean ports. We determined the potential for phytoplankton in the ballast water to invade the South Korean marine environment, given the specific growth rates of the phytoplankton, the delay before the phytoplankton started growing, and the rate at which the phytoplankton would initially disperse in ports and bays. Most of the phytoplankton in the ballast water samples originated in countries such as China and Japan that are adjacent to South Korea, and diatoms dominated these phytoplankton communities. The abundance of phytoplankton in a sample did not appear to be related to any particular environmental parameter, including the voyage duration. However, the number of phytoplankton taxa in a sample decreased as the voyage duration increased. The survival and growth of phytoplankton communities in the South Korean marine environment were assessed, and we found that most invasions failed at the initial dispersal phase, especially when a community was introduced to pier-side seawater. However, some members of phytoplankton communities, if they were dispersed and where conditions were highly eutrophic, could grow fast enough to overcome the initial dispersal phase in South Korean ports and bays.

Additional keywords: dispersal, specific growth rate, survival, time delay.


References

Baars, J. W. M. (1979). Autecological investigations on marine diatoms. I. Experimental results in biogeographical studies. Hydrological Bulletin 13, 123–137.
Autecological investigations on marine diatoms. I. Experimental results in biogeographical studies.Crossref | GoogleScholarGoogle Scholar |

Baek, S., Shimode, S., and Kikuchi, T. (2007). Reproductive ecology of the dominant dinoflagellate, Ceratium fusus, in coastal area of Sagami Bay, Japan. Journal of Oceanography 63, 35–45.
Reproductive ecology of the dominant dinoflagellate, Ceratium fusus, in coastal area of Sagami Bay, Japan.Crossref | GoogleScholarGoogle Scholar |

Baek, S. H., Shimode, S., and Kikuchi, T. (2008). Growth of dinoflagellates, Ceratium furca and Ceratium fusus in Sagami Bay, Japan: the role of temperature, light intensity and photoperiod. Harmful Algae 7, 163–173.
Growth of dinoflagellates, Ceratium furca and Ceratium fusus in Sagami Bay, Japan: the role of temperature, light intensity and photoperiod.Crossref | GoogleScholarGoogle Scholar |

Baek, S. H., Jung, S. W., and Shin, K. (2011). Effects of temperature and salinity on growth of Thalassiosira pseudonana (Bacillariophyceae) isolated from ballast water. Journal of Freshwater Ecology 26, 547–552.
| 1:CAS:528:DC%2BC3MXhsFantL7O&md5=7b7f192bdf624d07f4ffb338aa913bc3CAS |

Baek, S. H., Jung, S. W., Jang, M. C., Hyun, B., and Shin, K. (2012). Survival potential of autotrophic phytoplankton species collected from ballast water in international commercial ships. New Zealand Journal of Marine and Freshwater Research 46, 125–136.
Survival potential of autotrophic phytoplankton species collected from ballast water in international commercial ships.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XktFWgtL4%3D&md5=de59f3e655f238ce30eb464c81773ec8CAS |

Burkholder, J. M., Hallegraeff, G. M., Melia, G., Cohen, A., Bowers, H. A., Oldach, D. W., Parrow, M. W., Sullivan, M. J., Zimba, P. V., Allen, E. H., Kinder, C. A., and Mallin, M. A. (2007). Phytoplankton and bacterial assemblages in ballast water of US military ships as a function of port of origin, voyage time, and ocean exchange practices. Harmful Algae 6, 486–518.
Phytoplankton and bacterial assemblages in ballast water of US military ships as a function of port of origin, voyage time, and ocean exchange practices.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsVGmtLk%3D&md5=69f26eb67555142cc2b789ebbb430a7bCAS |

Carlton, J. T. (1985). Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanography and Marine Biology – an Annual Review 23, 313–371.

Carlton, J. T. (1999). The scale and ecological consequences of biological invasions in the world’s oceans. In ‘Invasive Species and Biodiversity Management’. (Eds O. T. Sandlund, P. J. Schei and A. Viken.) pp. 195–212. (Kluwer Academic Press: Dordrecht, Netherlands.)

Carney, K. J., Delany, J. E., Sawant, S., and Mesbahi, E. (2011). The effects of prolonged darkness on temperate and tropical marine phytoplankton, and their implications for ballast water risk management. Marine Pollution Bulletin 62, 1233–1244.
The effects of prolonged darkness on temperate and tropical marine phytoplankton, and their implications for ballast water risk management.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVCntrY%3D&md5=ae237d7fa7fe01477da1af3f366d9c3aCAS | 21489565PubMed |

Casas-Monroy, O., Roy, S., and Rochon, A. (2011). Ballast sediment-mediated transport of non-indigenous species of dinoflagellates on the east coast of Canada. Aquatic Invasions 6, 231–248.
Ballast sediment-mediated transport of non-indigenous species of dinoflagellates on the east coast of Canada.Crossref | GoogleScholarGoogle Scholar |

Chavanich, S., Tan, L. T., Vallejo, B., and Viyakarn, V. (2010). Report on the current status of marine non-indigenous species in the Western Pacific region. Intergovernmental Oceanographic Commission Sub-commission for the Western Pacific (IOC/WESTPAC), Bangkok, Thailand.

Chen, S. L., Zhang, G. A., Yang, S.-L., and Shi, J. Z. (2006). Temporal variations of fine suspended sediment concentration in the Changjiang River estuary and adjacent coastal waters, China. Journal of Hydrology 331, 137–145.
Temporal variations of fine suspended sediment concentration in the Changjiang River estuary and adjacent coastal waters, China.Crossref | GoogleScholarGoogle Scholar |

Choi, K.-H. (2009). Risk assessment of ballast water-mediated invasions of phytoplankton: a modeling study. Ocean Science Journal 44, 221–226.
Risk assessment of ballast water-mediated invasions of phytoplankton: a modeling study.Crossref | GoogleScholarGoogle Scholar |

Choi, K.-H., and Kimmerer, W. J. (2008). Mate limitation in an estuarine population of copepods. Limnology and Oceanography 53, 1656–1664.
Mate limitation in an estuarine population of copepods.Crossref | GoogleScholarGoogle Scholar |

Choi, K. H., Kimmerer, W., Smith, G., Ruiz, G. M., and Lion, K. (2005). Post-exchange zooplankton in ballast water of ships entering the San Francisco Estuary. Journal of Plankton Research 27, 707–714.
Post-exchange zooplankton in ballast water of ships entering the San Francisco Estuary.Crossref | GoogleScholarGoogle Scholar |

Chu, K. H. E., Tam, P., Fung, C. H., and Chen, Q. C. (1997). A biological survey of ballast water in container ships entering Hong Kong. Hydrobiologia 352, 201–206.
A biological survey of ballast water in container ships entering Hong Kong.Crossref | GoogleScholarGoogle Scholar |

Cloern, J. E. (1987). Turbidity as a control on phytoplankton biomass and productivity in estuaries. Continental Shelf Research 7, 1367–1381.
Turbidity as a control on phytoplankton biomass and productivity in estuaries.Crossref | GoogleScholarGoogle Scholar |

David, M., Gollasch, S., Cabrini, M., Perkovič, M., Bošnjak, D., and Virgilio, D. (2007). Results from the first ballast water sampling study in the Mediterranean Sea: the port of Koper study. Marine Pollution Bulletin 54, 53–65.
Results from the first ballast water sampling study in the Mediterranean Sea: the port of Koper study.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXntl2htA%3D%3D&md5=3e5e0211f4aa685db96a1dac1d1aa334CAS | 17049948PubMed |

De Stasio, B. T., Schrimpf, M. B., and Cornwell, H. (2014). Phytoplankton communities in Green Bay, Lake Michigan, after invasion by deissenid mussels: increased dominance by Cyanobacteria. Diversity 6, 681–704.
Phytoplankton communities in Green Bay, Lake Michigan, after invasion by deissenid mussels: increased dominance by Cyanobacteria.Crossref | GoogleScholarGoogle Scholar |

Dickman, M., and Zhang, F. Z. (1999). Mid-ocean exchange of container vessel ballast water. 2: effects of vessel type in the transport of diatoms and dinoflagellates from Manzanillo, Mexico, to Hong Kong, China. Marine Ecology Progress Series 176, 253–262.
Mid-ocean exchange of container vessel ballast water. 2: effects of vessel type in the transport of diatoms and dinoflagellates from Manzanillo, Mexico, to Hong Kong, China.Crossref | GoogleScholarGoogle Scholar |

Doblin, M. A., Coyne, K. J., Rinta-Kanto, J. M., Wilhelm, S. W., and Dobbs, F. C. (2007). Dynamics and short-term survival of toxic cyanobacteria species in ballast water from NOBOB vessels transiting the Great Lake: implications for HAB invasions. Harmful Algae 6, 519–530.
Dynamics and short-term survival of toxic cyanobacteria species in ballast water from NOBOB vessels transiting the Great Lake: implications for HAB invasions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsVGmtLY%3D&md5=72edf47c47254810432711037b2561e3CAS |

Drake, L. A., Meyer, A. E., Forsberg, R. L., Baier, R. E., Doblin, M. A., Heinemann, S., Johnson, W. P., Koch, M., Rublee, P. A., and Dobbs, F. C. (2005). Potential invasion of microorganisms and pathogens via interior hull fouling: biofilms inside ballast-water tanks. Biological Invasions 7, 969–982.
Potential invasion of microorganisms and pathogens via interior hull fouling: biofilms inside ballast-water tanks.Crossref | GoogleScholarGoogle Scholar |

Elser, J. J., Stabler, L. B., and Hassett, R. P. (1995). Nutrient limitation of bacterial growth and rates of bacterivory in lakes and oceans: a comparative study. Aquatic Microbial Ecology 9, 105–110.
Nutrient limitation of bacterial growth and rates of bacterivory in lakes and oceans: a comparative study.Crossref | GoogleScholarGoogle Scholar |

Goldman, J. C. (1977). Steady state growth of phytoplankton in continuous culture: comparison of internal and external nutrient equations. Journal of Phycology 13, 251–258.

Guillard, R. L. L. (1975). Culture of phytoplankton for feeding marine invertebrates. In ‘Culture of Marine Invertebrates Animals’. (Eds W. L. Smith and M. H. Chanley.) pp. 29–60. (Plenum Press: New York.)

Hallegraeff, G. M. (1993). Review of harmful algal blooms and their apparent global increase. Phycologia 32, 79–99.
Review of harmful algal blooms and their apparent global increase.Crossref | GoogleScholarGoogle Scholar |

Hallegraeff, G. M. (1998). Transport of toxic dinoflagellates via ship’s ballast water: bioeconomic risk assessment and efficacy of possible ballast water management strategies. Marine Ecology Progress Series 168, 297–309.
Transport of toxic dinoflagellates via ship’s ballast water: bioeconomic risk assessment and efficacy of possible ballast water management strategies.Crossref | GoogleScholarGoogle Scholar |

Hallegraeff, G. M., and Bolch, C. J. (1992). Transport of diatom and dinoflagellate resting spores in ships ballast water: implications for plankton biogeography and aquaculture. Journal of Plankton Research 14, 1067–1084.
Transport of diatom and dinoflagellate resting spores in ships ballast water: implications for plankton biogeography and aquaculture.Crossref | GoogleScholarGoogle Scholar |

IMO (2008). Harmful aquatic organisms in ballast water. In ‘Marine Environment Protection Committee 58th Session Agenda Item 2’. (IMO: London, UK.)

Kang, J.-H., Hyun, B.-G., and Shin, K. (2010). Phytoplankton viability in ballast water from international commercial ships berthed at ports in Korea. Marine Pollution Bulletin 60, 230–237.
Phytoplankton viability in ballast water from international commercial ships berthed at ports in Korea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhvFKitr8%3D&md5=3d0c02cfb91984a1a43a450c547e88d9CAS | 19857877PubMed |

Ketchum, B. T. (1954). Relation between circulation and plankton populations in estuaries. Ecology 35, 191–200.
Relation between circulation and plankton populations in estuaries.Crossref | GoogleScholarGoogle Scholar |

Klein, G., MacIntosh, K., Kaczmarska, I., and Ehrman, J. M. (2010). Diatom survivorship in ballast water during trans-Pacific crossings. Biological Invasions 12, 1031–1044.
Diatom survivorship in ballast water during trans-Pacific crossings.Crossref | GoogleScholarGoogle Scholar |

Korea Ocean Research and Development Institute (2008). ‘Development of Port Environmental Risk Assessment Technology. BSPE 00700-2044-7’. (Kordi Press: Ansan, South Korea.)

Liebich, V., Stehouwer, P. P., and Veldhuis, M. (2012). Re-growth of potential invasive phytoplankton following UV-based ballast water treatment. Aquatic Invasion 7, 29–36.
Re-growth of potential invasive phytoplankton following UV-based ballast water treatment.Crossref | GoogleScholarGoogle Scholar |

McCarthy, H. P., and Crowder, L. B. (2000). An overlooked scale of global transport: phytoplankton species richness in ships’ ballast water. Biological Invasions 2, 321–322.
An overlooked scale of global transport: phytoplankton species richness in ships’ ballast water.Crossref | GoogleScholarGoogle Scholar |

Ohtsuka, S., Horiguchi, T., Lopes, R. M., Choi, K. H., and Iwasaki, K. (2004). Plankton introduction via ship ballast water: a review. Bulletin of the Plankton Society of Japan 51, 101–118.

Parsons, T. R., Maita, Y., and Lalli, C. M. (1984). ‘A Manual of Chemical and Biological Methods for Seawater Analysis.’ 1st edn. (New York Pergamon Press: Oxford, UK.)

Pertola, S., Kuosa, H., and Olsonen, R. (2005). Is the invasion of Prorocentrum minimum (Dinophyceae) related to the nitrogen enrichment of the Baltic Sea? Harmful Algae 4, 481–492.
Is the invasion of Prorocentrum minimum (Dinophyceae) related to the nitrogen enrichment of the Baltic Sea?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivVCmtLg%3D&md5=5765c3cd4114dedde343d1d1b6110705CAS |

Pertola, S., Faust, M. A., and Kuosa, H. (2006). Survey on germination and species composition of dinoflagellates from ballast tanks and recent sediments in ports on the south coast of Finland, north-eastern Baltic Sea. Marine Pollution Bulletin 52, 900–911.
Survey on germination and species composition of dinoflagellates from ballast tanks and recent sediments in ports on the south coast of Finland, north-eastern Baltic Sea.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XptValsrs%3D&md5=887a93a9383049f500f521d519a8ce2cCAS | 16442131PubMed |

Ricciardi, A., and MacIsaac, H. J. (2000). Recent mass invasion of the North American Great Lakes by Ponto-Caspian species. Trends in Ecology & Evolution 15, 62–65.
Recent mass invasion of the North American Great Lakes by Ponto-Caspian species.Crossref | GoogleScholarGoogle Scholar |

Rigby, G. R., Hallegraeff, G. M., and Sutton, C. (1999). Novel ballast water heating technique offers cost-effective treatment to reduce the risk of global transport of harmful marine organisms. Marine Ecology Progress Series 191, 289–293.
Novel ballast water heating technique offers cost-effective treatment to reduce the risk of global transport of harmful marine organisms.Crossref | GoogleScholarGoogle Scholar |

Rines, J. E. B., and Hargraves, P. E. (1988). ‘The Chaetoceros Ehrenberg (Bacillariophyceae) Flora of Narragansett Bay, Rhode Island, USA.’ (J. Cramer Press: Berlin.)

Roy, S., Parenteau, M., Casas-Monroy, O., and Rochon, A. (2012). Coastal ship traffic: a significant introduction vector for potentially harmful dinoflagellates in eastern Canada. Canadian Journal of Fisheries and Aquatic Sciences 69, 627–644.
Coastal ship traffic: a significant introduction vector for potentially harmful dinoflagellates in eastern Canada.Crossref | GoogleScholarGoogle Scholar |

Ruiz, G. M., Rawlings, T. K., Dobbs, F. C., Drake, L. A., Mullady, T., Huq, A., and Colwell, R. R. (2000). Global spread of microorganisms by ships. Nature 408, 49–50.
Global spread of microorganisms by ships.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotValu74%3D&md5=f48ce66a37656bbdf955c4e899241b05CAS | 11081499PubMed |

Shapoori, M., and Gholami, M. (2014). Effect of a ballast water treatment system on survivorship of natural populations of marine plankton in Persian Gulf, Iran. Marketing Science 4, 44–48.

Shim, J.-H. (1994). ‘Illustrated Encyclopaedia of Fauna & Flora of Korea. 34. Marine Phytoplankton.’ (Ministry of Education: Seoul.)

Smith, L. D., Wonham, M. J., Mccann, L. D., Ruiz, G. M., Hines, A. H., and Carlton, J. T. (1999). Invasion pressure to a ballast-flooded estuary and an assessment of inoculant survival. Biological Invasions 1, 67–87.
Invasion pressure to a ballast-flooded estuary and an assessment of inoculant survival.Crossref | GoogleScholarGoogle Scholar |

Sournia, A. (1978). ‘Phytoplankton Manual.’ (UNESCO: Paris.)

Steichen, J., Windham, R., Brinkmeyer, R., and Quigg, A. (2012). Ecosystem under pressure: Ballast water discharge into Galveston Bay, Texas (USA) from 2005 to 2010. Marine Pollution Bulletin 64, 779–789.
Ecosystem under pressure: Ballast water discharge into Galveston Bay, Texas (USA) from 2005 to 2010.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XkvFaiu7Y%3D&md5=d9c83c163bc77aa22c40b1cc9e07b0b7CAS | 22336093PubMed |

Stolte, W., Mccollin, T., Noordellos, A. A. M., and Riegman, R. (1994). Effect of nitrogen source on the size distribution within marine phytoplankton population. Journal of Experimental Marine Biology and Ecology 184, 83–97.
Effect of nitrogen source on the size distribution within marine phytoplankton population.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjs1Siurs%3D&md5=2f3ec4b2aa4adc31a0a691386034b488CAS |

Strayer, D. L. (2009). Twenty years of zebra mussels: lessons from the mollusk that made headlines. Frontiers in Ecology and the Environment 7, 135–141.
Twenty years of zebra mussels: lessons from the mollusk that made headlines.Crossref | GoogleScholarGoogle Scholar |

Takabayashi, M., Lew, K., Johnson, A., Marchi, A., Dugdale, R., and Wilkerson, F. P. (2006). The effect of nutrient availability and temperature on chain length of the diatom, Skeletonema costatum. Journal of Plankton Research 28, 831–840.
The effect of nutrient availability and temperature on chain length of the diatom, Skeletonema costatum.Crossref | GoogleScholarGoogle Scholar |

Takano, K., Ishikawa, Y., Mikami, H., Ban, S., Yoshida, T., Aono, T., Imada, K., Yasutomi, R., Takeuchi, K., and Hino, S. (2001). Analysis of the change in dominant phytoplankton species in unstratified Lake Oshima-Ohnuma estimated by a bottle incubation experiment. Limnology 2, 29–35.
Analysis of the change in dominant phytoplankton species in unstratified Lake Oshima-Ohnuma estimated by a bottle incubation experiment.Crossref | GoogleScholarGoogle Scholar |

Tomas, C. R. (1997). ‘Identifying Marine Phytoplankton.’ (Academic Press: San Diego, CA.)

Van Overdijk, C. D. A., Grigorovich, I. A., Mabee, T., Ray, W. J., Ciborowski, J. J. H., and MacIsaac, H. J. (2003). Microhabitat selection by the invasive amphipod Echinogammarus ischnus and native Gammarus fasciatus in laboratory experiment and in Lake Erie. Freshwater Biology 48, 567–578.
Microhabitat selection by the invasive amphipod Echinogammarus ischnus and native Gammarus fasciatus in laboratory experiment and in Lake Erie.Crossref | GoogleScholarGoogle Scholar |

Wang, Z.-H., Qi, Y.-Z., and Yang, Y.-F. (2007). Cyst formation: an important mechanism for the termination of Scrippsiella trochoidea (Dinophyceae) bloom. Journal of Plankton Research 29, 209–218.
Cyst formation: an important mechanism for the termination of Scrippsiella trochoidea (Dinophyceae) bloom.Crossref | GoogleScholarGoogle Scholar |

Wells, M. G., Bailey, S. A., and Ruddick, B. (2011). The dilution and dispersion of ballast water discharged into Goderich Harbor. Marine Pollution Bulletin 62, 1288–1296.
The dilution and dispersion of ballast water discharged into Goderich Harbor.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXnsVCnt7o%3D&md5=4d82281e8f95d2af6341c927722328e2CAS | 21440268PubMed |

Wonham, M. J., Walton, W. D., 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 |

Yoshida, M., Fukuyo, Y., Murase, T., and Ikegami, T. (1996). On-board observations of phytoplankton viability in ships’ ballast tanks under critical light and temperature conditions. In ‘Harmful and Toxic Algal Blooms’. (Eds T. Yasumoto, Y. Oshima and Y. Fukuyo.) pp. 205–208. (Intergovernmental Oceanographic Commission of UNESCO: Paris.)

Zhang, F., and Dickman, M. (1999). Mid-ocean exchange of container vessel ballast water. 1: seasonal factors affecting the transport of harmful diatoms and dinoflagellates. Marine Ecology Progress Series 176, 243–251.
Mid-ocean exchange of container vessel ballast water. 1: seasonal factors affecting the transport of harmful diatoms and dinoflagellates.Crossref | GoogleScholarGoogle Scholar |