Journal of Oceanology and Limnology

, Volume 37, Issue 2, pp 580–588 | Cite as

Survivorship characteristics and adaptive mechanisms of phytoplankton assemblages in ballast water

  • Huixian Wu
  • Chen Shen
  • Qiong Wang
  • Richard B. Aronson
  • Chen Chen
  • Junzeng XueEmail author


Phytoplankton diversity and abundance were determined in ballast water from 26 vessels in the Shanghai Yangshan Deep-Water Port from April 2015 to January 2016. In total, 84 species of phytoplankton were identified, belonging to 43 genera and 5 phyla. Bacillariophyta (75.0%, including 30 genera and 63 species) were the dominant algae in the ballast water. Their density ranged from (5.55±9.62) SD to (1.878±0.872)×10 3 cells/L, with a mean of 410.1 cells/L. Nine potentially harmful phytoplankton taxa were detected: Ceratium furca, Ce. marcroceros, Leptocylindrus danicus, Coscinodiscus radiatus, Co. granii, Prorocentrum micans, Melosira sulcata, Meuniera membranacea and Skeletonema costatum. Our survey and identification results showed that Microcystis aeruginosa, Ankistrodesmus falcatus and Scenedesmus survived in the high-salinity ballast water, even though they are freshwater species. We identified the common features of surviving phytoplankton and impacts on the phytoplankton assemblage of ballast water age and source. Our goal was to understand the adaptative mechanisms of phytoplankton in ballast water, providing statistical and theoretical support for future ballast water research and suggesting a scientific basis of ballast water management and inspection of vessels entering the port.


diversity abundances Yangshan Port dominant algae ballast water age source 


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We are very grateful to the Shanghai Entry-Exit Inspection and Quarantine Bureau, as well as to the officers and crew of all the vessels that were boarded and sampled. The comments and suggestions of the reviewers are greatly appreciated.

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  1. Antonella P, Luca G. 2013. The quantitative real–time PCR applications in the monitoring of marine harmful algal bloom (HAB) species. Environmental Science and Pollution Research, 20 (10): 6 851–6 862.CrossRefGoogle Scholar
  2. 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, Mallin M A. 2007. Phytoplankton and bacterial assemblages in ballast water of U.S. military ships as a function of port of origin, voyage time, and ocean exchange practices. Harmful Algae, 6 (4): 486–518.CrossRefGoogle Scholar
  3. Carlton J T, Geller J B. 1993. Ecological roulette: the global transport of nonindigenous marine organisms. Science, 261 (5117): 78–82.CrossRefGoogle Scholar
  4. Carlton J T. 1985. Transoceanic and interoceanic dispersal of coastal marine organisms: the biology of ballast water. Oceanography and Marine Biology, 23 (4): 313–371.Google Scholar
  5. Casas–Monroy O, Linley R D, Adams J K, Chan F T, Drake D A R, Bailey S A. 2015. Relative invasion risk for plankton across marine and freshwater systems: examining efficacy of proposed international ballast water discharge standards. PLoS One, 10 (3): e0118267.CrossRefGoogle Scholar
  6. Casas–Monroy O, Parenteau M, Drake D A R, Roy S, Rochon A. 2016. Absolute estimates of the propagule pressure of viable dinofagellates across Canadian coasts: the variable infuence of ballast water exchange. Marine Biology, 163:174.CrossRefGoogle Scholar
  7. Casas–Monroy O, Roy S, Andre R. 2011. Ballast sedimentmediated transport of non–indigenous species of dinoflagellates on the East Coast of Canada. Aquatic Invasions, 6 (3): 231–248.CrossRefGoogle Scholar
  8. Chen X F, Zhou Q J, Duan W J, Zhou C X, Duan L J, Zhang H L, Sun A L, Yan X J, Chen J. 2016. Development and evaluation of a DNA microarray assay for the simultaneous detection of nine harmful algal species in ship ballast and seaport waters. Chinese Journal of Oceanology and Limnology, 34 (1): 86–101.CrossRefGoogle Scholar
  9. Chu K H, Tam P F, Fung C H, Chen Q C. 1997. A biological survey of ballast water in container ships entering Hong Kong. Hydrobiologia, 352 (1–3): 201–206.CrossRefGoogle Scholar
  10. David M, Gollasch S, Cabrini M, Perkovič M, Bošnjak D, Virgilio D. 2007. Results from the first ballast water sampling study in the Mediterranean Sea—the Port of Koper study. Marine Pollution Bulletin, 54 (1): 53–65.CrossRefGoogle Scholar
  11. David M, Gollasch S, Leppäkoski E, Hewitt C. 2015. Risk assessment in ballast water management. In: David M, Gollasch S eds. Global Maritime Transport and Ballast water Management. Springer, Netherland. p.133–169.Google Scholar
  12. Dickman M, 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, 176: 253–262.CrossRefGoogle Scholar
  13. Fahnenstiel G, Hong Y, Millie D, Doblin M A, Johengen T, Reid D. 2009. Marine dinoflagellate cysts in the ballast tank sediments of ships entering the Laurentian Great Lakes. Transport Engineering in Australia, 30 (6): 353–355.Google Scholar
  14. Feng D L, Xu S H, Liu G. 2015. Application of immobilized TiO 2 photocatalysis to improve the inactivation of heterosigma akashiwo in ballast water by intense pulsed light. Chemosphere, 125: 102–107.CrossRefGoogle Scholar
  15. Galluzzi L, Cegna A, Casabianca S, Penna A, Saunders N, Magnani M. 2011. Development of an oligonucleotide microarray for the detection and monitoring of marine dinoflagellates. Journal of Microbiological Methods, 84 (2): 234–242.CrossRefGoogle Scholar
  16. Gollasch S, Lenz J, Dammer M, Andres H G. 2000. Survival of tropical ballast water organisms during a cruise from the Indian Ocean to the North Sea. Journal of Plankton Research, 22 (5): 923–937.CrossRefGoogle Scholar
  17. Guo Y G, Qian S D. 2003. China Seaweed. Science Press, Beijing, China. (in Chinese)Google Scholar
  18. Hallegraeff G M, Bolch D J. 1991. Transport of toxic dinoflagellate cysts via ships’ ballast water. Marine Pollution Bulletin, 22 (1): 27–30.CrossRefGoogle Scholar
  19. Hamer J P, Lucas I A N, McCollln T A. 2001. Harmful dinoflagellate resting cysts in ships' ballast tank sediments: potential for introduction into English and Welsh waters. Phycologia, 40 (3): 246–255.CrossRefGoogle Scholar
  20. Handy S M, Demir E, Hutchins D A, Portune K J, Whereat E B, Hare C E, Rose J M, Warner M, Farestad M, Cary S C, Coyne K J. 2008. Using quantitative real–time PCR to study competition and community dynamics among Delaware Inland Bays harmful algae in field and laboratory studies. Harmful Algae, 7 (5): 599–613.CrossRefGoogle Scholar
  21. Hu H J, Wei Y X. 2006. The Freshwater Algae of China–Systematics, Taxonomy and Ecology. Science Press, Beijing, China. (in Chinese)Google Scholar
  22. IMI (International Maritime Information Website). 2018. Shanghai port’s news. APL launches premium Shanghai–LA service to help airfreight shippers. 2018–03–07 08:33:58 View: 39, php?lan=en&id=368&flag=cnports&pname=shanghai.Google Scholar
  23. IMO (International Maritime Organization). 2004. International Convention for the Controland Management of Ships' Ballast Water and Sediments. London, England: International Maritime Organization.Google Scholar
  24. IMO. 2008. IMO. Accessed on 2008–04–24.Google Scholar
  25. Jin D X, Chen J H, Huang K G. 1965. Chinese Marine Planktonic Diatoms. Shanghai Science and Technology Press, Shanghai, China. (in Chinese)Google Scholar
  26. Jin D X, Cheng Z, Lin J. 1982. China Ocean Bottom Handle Diatoms. Ocean Press, Beijing, China. (in Chinese)Google Scholar
  27. Jin D X, Cheng Z, Liu S C. 1991. China Marine Benthic Diatoms. Ocean Press, Beijing, China. (in Chinese)Google Scholar
  28. John P H, McCollin T A, Lucas I A N. 2000. Dinoflagellate cysts in ballast tank sediments: between tank variability. Marine Pollution Bulletin, 40 (9): 731–733.CrossRefGoogle Scholar
  29. Klein G, Macintosh K, Kaczmarska I, Ehrman J M. 2010. Diatom survivorship in ballast water during trans–pacific crossings. Biological Invasions, 12 (5): 1 031–1 044.CrossRefGoogle Scholar
  30. Liebich V, Stehouwer P P, Veldhuis M. 2012. Re–growth of potential invasive phytoplankton following UV–based ballast water treatment. Aquatic Invasions, 7 (1): 29–36.CrossRefGoogle Scholar
  31. Liu K. 2005. Science and technology in Foreign countries. Marine Invasion, (5): 26–28.Google Scholar
  32. Liu Y, Wang S, Wang Q, Li Y, Wang H X, Guan Y Y. 2011. Notice of retraction investigation of plankton in ballast water of two Chinese domestic voyages. In: Proceedings of 2011 5th International Conference on Bioinformatics and Biomedical Engineering. IEEE, Wuhan, China. p.78–82.Google Scholar
  33. Mackenzie M. 1999. Alien invaders. New Scientist, 162 (2183): 18–19.Google Scholar
  34. McCarthy H P, Crowder L B. 2000. An overlooked scale of global transport: phytoplankton species richness in ships' ballast water. Biological Invasions, 2 (4): 321–322.CrossRefGoogle Scholar
  35. McCoy G R, Touzet N, Fleming G T A, Raine R. 2013. An evaluation of the applicability of microarrays for monitoring toxic algae in Irish coastal waters. Environmental Science and Pollution Research, 20 (10): 6 751–6 764.CrossRefGoogle Scholar
  36. McQuoid M R, Hobson L A. 1996. Diatom resting stages. Journal of Phycology, 32: 889–902.CrossRefGoogle Scholar
  37. Medcof J C. 1975. Living marine animals in a ships’ ballast water. Proceedings of the National Shellfisheries Association, 65: 11–12.Google Scholar
  38. Olenin S, Gollasch S, Jonušas S, Rimkutė I. 2000. En–route investigations of plankton in ballast water on a ship’s voyage from the Baltic Sea to the open Atlantic coast of Europe. International Review of Hydrobiology, 85 (5–6): 577–596.CrossRefGoogle Scholar
  39. Pam E D, Li K X, Wall A, Yang Z, Wang J. 2013. A subjective approach for ballast water risk estimation. Ocean Engineering, 61: 66–76.CrossRefGoogle Scholar
  40. Round F E, Crawford R M, Mann D G. 1990. The Diatoms: Biology and Morphology of the Genera. Cambridge University Press, Cambridge.Google Scholar
  41. Ruiz G M, Carlton J T, Grosholz E D, Hines A H. 1997. Global invasions of marine and estuarine habitats by nonindigenous species: mechanisms, extent, and consequences. American Zoologist, 37 (6): 621–632.CrossRefGoogle Scholar
  42. Ruiz G M, Rawlings T K, Dobbs F C, Drake L A, Mullady T, Huq A, Colwell R R. 2000. Global spread of microorganisms by ships. Nature, 408 (6808): 49–50.CrossRefGoogle Scholar
  43. Sarinas B G S, Gellada L D, Magramo M M, Baria LO, Tirazona D B, Sorio L R D, Tornalejo J A. 2014. Plankton diversity in ballast water of an inter–island passengercargo ship calling the Philippine ports. Asian Journal of Biodiversity, 5 (1): 78–91.CrossRefGoogle Scholar
  44. Satir T. 2008. Ship's ballast water and marine pollution. In: Coskun H G, Cigizoglu H K, Maktav M D eds. Integration of Information for Environmental Security. Springer, Netherlands. p.453–463.Google Scholar
  45. Satir T. 2014. Ballast water treatment systems: design, regulations, and selection under the choice varying priorities. Environmental Science and Pollution Research, 21 (18): 10 686–10 695.CrossRefGoogle Scholar
  46. Sicko–Goad L, Stoermer E F, Kociolek J P. 1989. Diatom resting cell rejuvenation and formation: time course, species records and distribution. Journal of Plankton Research, 11 (2): 375–389.CrossRefGoogle Scholar
  47. Stan L C, Sabau A, Buzbuchi N. 2013. Ballast water treating by advanced oxidation technology. Annals of the University Dunarea De Jos of Galati: Fascicle II, 36 (2): 287–291.Google Scholar
  48. Stehouwer P P, Buma A, Peperzak L. 2015. A comparison of six different ballast water treatment systems based on UV radiation, electrochlorination and chlorine dioxide. Environmental Technology, 36 (13–16): 2 094–2 104.CrossRefGoogle Scholar
  49. Steichen J L, Denby A, Windham R, Brinkmeyer R, Quigg A. 2015. A Tale of Two Ports: Dinoflagellate and Diatom Communities Found in the High Ship Traffic Region of Galveston Bay, Texas (USA). Journal of Coastal Research, 31 (2): 407–416.CrossRefGoogle Scholar
  50. The General Administration of Quality Supervision, Inspection and Quarantine of the People’s Republic of China and the National Standardization Administration of China. 2007a. GB 17378.4–200. The Specification for Marine Monitoring—Part 4: Seawater Analysis. China Standard Press, Beijing, China. (in Chinese)Google Scholar
  51. The General Administration of Quality Supervision, Inspection and Quarantine of the People’s Republic of China and the National Standardization Administration of China. 2007b. GB 17378.7–200. The Specification for Marine Monitoring—Part 7: Ecological Survey for Offshore Pollution and Biological Monitoring. China Standard Press, Beijing, China. (in Chinese)Google Scholar
  52. Wang C C, Niu Z G, Zhang Y. 2013. Health risk assessment of inhalation exposure of irrigation workers and the public to trihalomethanes from reclaimed water in landscape irrigation in Tianjin, north China. Journal of Hazardous Materials, 262: 179–188.CrossRefGoogle Scholar
  53. Wang G. 2014. The international shipping situation and the development Suggestions of Yangshan deep–water port. Transportation Enterprise Management, 29 (8): 11–14. (in Chinese)Google Scholar
  54. Xue J Z, Liu Y, Wang J H, Xing X L, Xu L P, Feng D L, Wu H X. 2011. A biological survey of zooplankton taken from ballast water of the international navigation ships entering the Shanghai Yangshan Deep–water Port in China. Acta Oceanologica Sinica, 33 (1): 138–145. (in Chinese with English abstract)Google Scholar
  55. Xue J Z, Xiao N Y, Wang Q, Wu H X. 2016. Seasonal variation of bacterial community diversity in Yangshan Por. Acta Ecologica Sinica, 36 (23): 7 758–7 767. (in Chinese with English abstract)Google Scholar
  56. Yang S M, Dong S. 2006. Common Planktonic Diatoms in China Sea Map. China Ocean University Press, Qingdao, China. (in Chinese)Google Scholar
  57. Yuan J, Mi T Z, Zhen Y, Yu Z G. 2012. Development of a rapid detection and quantification method of Karenia mikimotoi by real–time quantitative PCR. Harmful Algae, 17: 83–91.CrossRefGoogle Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  • Huixian Wu
    • 1
    • 2
  • Chen Shen
    • 1
    • 2
  • Qiong Wang
    • 1
    • 2
  • Richard B. Aronson
    • 3
  • Chen Chen
    • 1
    • 2
  • Junzeng Xue
    • 1
    • 2
    • 3
    Email author
  1. 1.College of Marine Ecology and EnvironmentShanghai Ocean UniversityShanghaiChina
  2. 2.Ballast Water Detecting LabShanghai Ocean UniversityShanghaiChina
  3. 3.Department of Biological SciencesFlorida Institute of TechnologyMelbourneUSA

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