Assessment of phytoplankton invasion risks in the ballast water of international ships in different growth conditions
Keywords:
dilution rates, regrowth, nutrient, water temperature, salinityAbstract
The possibility of successful invasion by phytoplankton assemblages in the ballast water of twelve international commercial ships was investigated. Various scenarios of port water dilution rates with a time delay for the exponential growth of the plankton were considered. Most of the phytoplankton in the ballast water samples originated in countries such as Japan and China, and diatoms dominated (>90% abundance) these phytoplankton communities. To assess their survival after discharge in seawater under various conditions, the phytoplankton were reintroduced into ballast water, pier-side water, and nutrient-enriched f/2 medium and incubated at various water temperatures and salinities for 2 weeks. The growth of the invading phytoplankton was influenced by the time delay for regrowth when introduced in the new seawater conditions. The results also suggest that once introduced by ballast water, the growth of a phytoplankton community may depend more on the nutrient levels and the water temperature and less on the salinity. Although we did not consider parameters such as competition with native species and predation, both high nutrient concentrations and water temperatures may significantly shorten the period before exponential growth occurs, which increases the invasion potential.
References
Baars, J.W.M., 1979. Autecological investigations on marine diatoms. I. Experimental results in biogeographical studies. Hydrobiol. Bull. 13, 123–137.
Baek, S.-H., Jang, M.-C., Jang, P.-G., Shin, K.-S., 2011a. Ballast-water Microphytoplankton Diversity and Survivability from International Ships Berthed at Ulsan and Pyeongtaek Ports, Korea. Ocean Polar Res. 33, 113–125.
Baek, S.-H., Jang, M.-C., Shin, K.-S., 2011b. Regrowth Ability and Species Composition of Phytoplankton in International Commercial Ship's Ballast Water Berthed at Pusan and Daesan Ports. The Sea 16, 106–115.
Baek, S., Jung, S., Jang, M., Hyun, B., Shin, K., 2012. Survival potential of autotrophic phytoplankton species collected from ballast water in international commercial ships. N. Z. J. Mar. Freshwater Res. 46, 125–136.
Bate, G., Crafford, S.D., 1985. Inhibition of phytoplankton photosynthesis by the WSF of used lubricating oil. Mar. Pollut. Bull. 16, 401–404.
Bertrand, E.M., McCrow, J.P., Moustafa, A., Zheng, H., McQuaid, J.B., Delmont, T.O., Post, A.F., Sipler, R.E., Spackeen, J.L., Xu, K., 2015. Phytoplankton–bacterial interactions mediate micronutrient colimitation at the coastal Antarctic sea ice edge. Proceedings of the National Academy of Sciences 112, 9938–9943.
Carlton, J.T., Geller, J.B., 1991. Ecological roulette: the global transport of nonindigenous marine organisms. Chem. Phys. Lett. 179, 53.
Carney, K., Delany, J., Sawant, S., Mesbahi, E., 2011. The effects of prolonged darkness on temperate and tropical marine phytoplankton, and their implications for ballast water risk management. Mar. Pollut. Bull. 62, 1233–1244.
Chen, C.Y., Folt, C.L., 2005. High plankton densities reduce mercury biomagnification. Environ. Sci. Technol. 39, 115–121.
Choi, K.-H., 2009. Risk assessment of ballast water-mediated invasions of phytoplankton: A modeling study. Ocean Sci. J. 44, 221–226.
Choi, K.-H., Kimmerer, W., 2009. Mating success and its consequences for population growth in an estuarine copepod. Mar. Ecol. Prog. Ser. 377, 183–191.
Collos, Y., 1986. Time-lag algal growth dynamics: biological constraints on primary production in aquatic environments. Mar. Ecol. Prog. Ser. 33, 193–206.
Cullen, J.J., MacIntyre, H.L., 2016. On the use of the serial dilution culture method to enumerate viable phytoplankton in natural communities of plankton subjected to ballast water treatment. J. Appl Phycol. 28, 279–298.
Davidson, K., Cunningham, A., 1996. Accounting for nutrient processing time in mathematical models of phytoplankton growth. Limnol Oceanogr. 41, 779–783.
DeRivera, C.E., Ruiz, G.M., Hines, A.H., Jivoff, P., 2005. Biotic resistance to invasion: native predator limits abundance and distribution of an introduced crab. Ecology 86, 3364–3376.
Drake, L.A., Choi, K.-H., Ruiz, G.M., Dobbs, F.C., 2001. Global redistribution of bacterioplankton and virioplankton communities. Biol. Invasions 3, 193–199.
Fog, G., 1957. Relationships between metabolism and growth in plankton algae. J. gen. Microbiol. 16, 294–297.
Frey, B.E., Small, L.F., 1980. Effects of micro-nutrients and major nutrients on natural phytoplankton populations. J. Plankton Res. 2, 1–22.
Hallegraeff, G.M., 1993. A review of harmful algal blooms and their apparent global increase. Phycologia 32, 79–99.
Hyun, B., Shin, K., Jang, M.-C., Jang, P.-G., Lee, W.-J., Park, C., Choi, K.-H., 2016. Potential invasions of phytoplankton in ship ballast water at South Korean ports. Mar. Freshwater Res. 67, 1906–1917.
Kang, J.-H., Hyun, B.-G., Shin, K., 2010. Phytoplankton viability in ballast water from international commercial ships berthed at ports in Korea. Mar. Pollut. Bull. 60, 230–237.
Klein, G., MacIntosh, K., Kaczmarska, I., Ehrman, J.M., 2010. Diatom survivorship in ballast water during trans-Pacific crossings. Biol. Invasions 12, 1031–1044.
Lewis, J., Harris, A., Jones, K., Edmonds, R., 1999. Long-term survival of marine planktonic diatoms and dinoflagellates in stored sediment samples. J. Plankton Res. 21, 343–354.
Massana, R., Terrado, R., Forn, I., Lovejoy, C., Pedrós‐Alió, C., 2006. Distribution and abundance of uncultured heterotrophic flagellates in the world oceans. Environ. Microbiol. 8, 1515–1522.
McCarthy, H.P., Crowder, L.B., 2000. An overlooked scale of global transport: phytoplankton species richness in ships' ballast water. Biol Invasions 2, 321–322.
Miller, A., Lion, K., Minton, M., Ruiz, G., 2007. Status and trends of ballast water management in the United States. Third Biennial Report of the National Ballast Information Clearinghouse.(January 2004 to December 2005). Smithsonian Environmental Research Center.
Olenina, I., Wasmund, N., Hajdu, S., Jurgensone, I., Gromisz, S., Kownacka, J., Toming, K., Vaiciūtė, D., Olenin, S., 2010. Assessing impacts of invasive phytoplankton: The Baltic Sea case. Mar. Pollut. Bull. 60, 1691–1700.
Pertola, S., Kuosa, H., Olsonen, R., 2005. Is the invasion of Prorocentrum minimum (Dinophyceae) related to the nitrogen enrichment of the Baltic Sea? Harmful Algae 4, 481–492.
Rines, J.E., Hargraves, P.E., 1988. The Chaetoceros Ehrenberg (Bacillariophyceae) flora of Narragansett Bay. Rhode Island, USA.
Shi, X.L., Marie, D., Jardillier, L., Scanlan, D.J., Vaulot, D., 2009. Groups without Cultured Representatives Dominate Eukaryotic Picophytoplankton in the Oligotrophic South East Pacific Ocean. PLoS ONE 4, e7657.
Shim, J., 1994. Illustrated encyclopedia of fauna and flora of Korea, vol. 34 Marine phytoplankton. Ministry of Education, Seoul, 1–487.
Team, R.C., 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. 2013. ISBN 3-900051-07-0.
Tomas, C.R., 1997. Identifying marine phytoplankton. Academic Press, Massachusetts.
Venables, W.N., Ripley, B.D., 2013. Modern applied statistics with S-PLUS. Springer Science & Business Media, Germany.
Verling, E., Ruiz, G.M., Smith, L.D., Galil, B., Miller, A.W., Murphy, K.R., 2005. Supply-side invasion ecology: characterizing propagule pressure in coastal ecosystems. Proceedings of the Royal Society of London B: Biological Sciences 272, 1249–1257.
Wells, M.G., Bailey, S.A., Ruddick, B., 2011. The dilution and dispersion of ballast water discharged into Goderich Harbor. Mar. Pollut. Bull. 62, 1288–1296.
Wonham, M.J., Lewis, M.A., MacIsaac, H.J., 2005. Minimizing invasion risk by reducing propagule pressure: a model for ballast-water exchange. Front. Ecol. Environ. 3, 473–478.
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