TY - JOUR
T1 - 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
AU - Burkholder, Jo Ann M.
AU - Hallegraeff, Gustaaf M.
AU - Melia, Gregory
AU - Cohen, Andrew
AU - Bowers, Holly A.
AU - Oldach, David W.
AU - Parrow, Matthew W.
AU - Sullivan, Michael J.
AU - Zimba, Paul V.
AU - Allen, Elle H.
AU - Kinder, Carol A.
AU - Mallin, Michael A.
N1 - Funding Information:
Funding for this research was provided by the Strategic Environmental Research and Development Program (SERDP)—Sustainable Infrastructure (J. Burkholder, CP-1244). We thank R. Holst and the SERDP staff for their counsel and encouragement. We are grateful to E. Holm for his counsel and assistance throughout this project. E. Holm, E. Haslbeck, and the research group at the Naval Surface Warfare Center, Carderock division, and G. Rosen, J. Grovhoug, and staff of the Space and Naval Warfare Systems Center, San Diego, CA assisted in sampling. T. Dodgshun of the Cawthron Institute, New Zealand, provided counsel on ballast water sampling. The research was also done in collaboration with B. Legge and staff of the U.S. Army Tank-Automotive and Armaments Command; and G. Ruiz, G. Smith and staff of the Smithsonian Environmental Research Center. This work would not have been possible without the cooperation of the personnel of the Military Sealift Command and U.S. Army. We thank J. Austin, F. Shukis, D. Cook, and K. Pope of the Military Sealift Command for aiding us, through Eric Holm and his project team, in developing a viable process for interfacing with the fleet and accessing the vessels; D. Cooke, J. Burkhardt, and M. Ragonese for helping us to understand fleet oiler operations; R. Caldwell, P. O’Donnell, Lt. E. Gonzaga, and T. Howser for providing scheduling and access information for vessel arrivals on the East Coast; and R. Appling, T. Brown, G. Talbott, L. Carley, N. Smith, S. Busby, and R. Pleas for arranging vessel access on the West Coast. J. Austin provided insights about the differences between MSC and MARAD vessels from a management operations standpoint. J. Darnell, A. Biondolillo, and P. Pope from the U.S. Army Tank-Automotive and Armaments Command, and SFC R. Crum from the U.S. Army Marine Maintenance Office, 7th Transportation Group. E. Fensin of the North Carolina. Department of Environment and Natural Resources assisted in phytoplankton analysis by light microscopy; L. Barnes assisted in flow cytometry; J. James and N. Rosen conducted nutrient analyses; N. Deamer managed algal cultures and contributed to data summarization and analysis; and H. Glasgow provided other general counsel. T. Tengs provided assistance in the phylogenetic studies, and F. Diaz-Mendez performed PCR and sequencing of clones. C. Brownie, D. Dickey, and J. Smith of the NCSU Department of Statistics provided counsel on statistics. We are grateful to Larry Holland for his organization of the large database for this project, and for his many contributions to an accompanying phytoplankton atlas. We are also grateful to the captains and crews of the vessels that were boarded and sampled; the vessels that were contacted but not included in the study; and the port facilities personnel with whom our project team and research partners interacted. All gave freely of their time and experience.
PY - 2007/8
Y1 - 2007/8
N2 - We characterized the physical/chemical conditions and the algal and bacterial assemblages in ballast water from 62 ballast tanks aboard 28 ships operated by the U.S. Military Sealift Command and the Maritime Administration, sampled at 9 ports on the U.S. West Coast and 4 ports on the U.S. East Coast. The ballast tank waters had been held for 2-176 days, and 90% of the tanks had undergone ballast exchange with open ocean waters. Phytoplankton abundance was highly variable (grand mean for all tanks, 3.21 × 104 viable cells m-3; median, 7.9 × 103 cells m-3) and was unrelated to physical/chemical parameters, except for a positive relationship between centric diatom abundance and nitrate concentration. A total of 100 phytoplankton species were identified from the ballast tanks, including 23 potentially harmful taxa (e.g. Chaetoceros concavicornis, Dinophysis acuminata, Gambierdiscus toxicus, Heterosigma akashiwo, Karlodinium veneficum, Prorocentrum minimum, Pseudo-nitzschia multiseries). Assemblages were dominated by chain-forming diatoms and dinoflagellates, and viable organisms comprised about half of the total cells. Species richness was higher in ballast tanks with coastal water, and in tanks containing Atlantic or Pacific Ocean source waters rather than Indian Ocean water. Total and viable phytoplankton numbers decreased with age of water in the tanks. Diversity also generally decreased with water age, and tanks with ballast water age >33 days did not produce culturable phytoplankton. Abundance was significantly higher in tanks with recently added coastal water than in tanks without coastal sources, but highly variable in waters held less than 30 days. Bacterial abundance was significantly lower in ballast tanks with Atlantic than Pacific Ocean source water, but otherwise was surprisingly consistent among ballast tanks (overall mean across all tanks, 3.13 ± 1.27 × 1011 cells m-3; median, 2.79 × 1011 cells m-3) and was unrelated to vessel type, exchange status, age of water, environmental conditions measured, or phytoplankton abundance. At least one of four pathogenic eubacteria (Listeria monocytogenes, Escherichia coli, Mycobacterium spp., Pseudomonas aeruginosa) was detected in 48% of the ballast tanks, but toxigenic strains of Vibrio cholerae were not detected. For ships with tanks of similar ballasting history, the largest source of variation in phytoplankton and bacteria abundance was among ships; for ships with tanks of differing ballasting histories, and for all ships/tanks considered collectively, the largest source of variation was within ships. Significant differences in phytoplankton abundance, but not bacterial abundance, sometimes occurred between paired tanks with similar ballasting history; hence, for regulatory purposes phytoplankton abundance cannot be estimated from single tanks only. Most tanks (94%) had adequate records to determine the source locations and age of the ballast water and, as mentioned, 90% had had ballast exchange with open-ocean waters. Although additional data are needed from sediments that can accumulate at the bottom of ballast tanks, the data from this water-column study indicate that in general, U.S. Department of Defense (DoD) ships are well managed to minimize the risk for introduction of harmful microbiota. Nevertheless, abundances of viable phytoplankton with maximum dimension >50 μm exceeded proposed International Maritime Organization standards in 47% of the ballast tanks sampled. The data suggest that further treatment technologies and/or alternative management strategies will be necessary to enable DoD vessels to comply with proposed standards.
AB - We characterized the physical/chemical conditions and the algal and bacterial assemblages in ballast water from 62 ballast tanks aboard 28 ships operated by the U.S. Military Sealift Command and the Maritime Administration, sampled at 9 ports on the U.S. West Coast and 4 ports on the U.S. East Coast. The ballast tank waters had been held for 2-176 days, and 90% of the tanks had undergone ballast exchange with open ocean waters. Phytoplankton abundance was highly variable (grand mean for all tanks, 3.21 × 104 viable cells m-3; median, 7.9 × 103 cells m-3) and was unrelated to physical/chemical parameters, except for a positive relationship between centric diatom abundance and nitrate concentration. A total of 100 phytoplankton species were identified from the ballast tanks, including 23 potentially harmful taxa (e.g. Chaetoceros concavicornis, Dinophysis acuminata, Gambierdiscus toxicus, Heterosigma akashiwo, Karlodinium veneficum, Prorocentrum minimum, Pseudo-nitzschia multiseries). Assemblages were dominated by chain-forming diatoms and dinoflagellates, and viable organisms comprised about half of the total cells. Species richness was higher in ballast tanks with coastal water, and in tanks containing Atlantic or Pacific Ocean source waters rather than Indian Ocean water. Total and viable phytoplankton numbers decreased with age of water in the tanks. Diversity also generally decreased with water age, and tanks with ballast water age >33 days did not produce culturable phytoplankton. Abundance was significantly higher in tanks with recently added coastal water than in tanks without coastal sources, but highly variable in waters held less than 30 days. Bacterial abundance was significantly lower in ballast tanks with Atlantic than Pacific Ocean source water, but otherwise was surprisingly consistent among ballast tanks (overall mean across all tanks, 3.13 ± 1.27 × 1011 cells m-3; median, 2.79 × 1011 cells m-3) and was unrelated to vessel type, exchange status, age of water, environmental conditions measured, or phytoplankton abundance. At least one of four pathogenic eubacteria (Listeria monocytogenes, Escherichia coli, Mycobacterium spp., Pseudomonas aeruginosa) was detected in 48% of the ballast tanks, but toxigenic strains of Vibrio cholerae were not detected. For ships with tanks of similar ballasting history, the largest source of variation in phytoplankton and bacteria abundance was among ships; for ships with tanks of differing ballasting histories, and for all ships/tanks considered collectively, the largest source of variation was within ships. Significant differences in phytoplankton abundance, but not bacterial abundance, sometimes occurred between paired tanks with similar ballasting history; hence, for regulatory purposes phytoplankton abundance cannot be estimated from single tanks only. Most tanks (94%) had adequate records to determine the source locations and age of the ballast water and, as mentioned, 90% had had ballast exchange with open-ocean waters. Although additional data are needed from sediments that can accumulate at the bottom of ballast tanks, the data from this water-column study indicate that in general, U.S. Department of Defense (DoD) ships are well managed to minimize the risk for introduction of harmful microbiota. Nevertheless, abundances of viable phytoplankton with maximum dimension >50 μm exceeded proposed International Maritime Organization standards in 47% of the ballast tanks sampled. The data suggest that further treatment technologies and/or alternative management strategies will be necessary to enable DoD vessels to comply with proposed standards.
KW - Bacteria
KW - Ballast water exchange
KW - Harmful algae
KW - Phytoplankton
KW - Ship
KW - Transport
UR - http://www.scopus.com/inward/record.url?scp=34247120031&partnerID=8YFLogxK
U2 - 10.1016/j.hal.2006.11.006
DO - 10.1016/j.hal.2006.11.006
M3 - Article
AN - SCOPUS:34247120031
SN - 1568-9883
VL - 6
SP - 486
EP - 518
JO - Harmful Algae
JF - Harmful Algae
IS - 4
ER -