ALGAE

The Korean Society of Phycology (한국조류학회(藻類))
권호 표지
DOI QR코드

DOI QR Code

Synergistic effects of elevated carbon dioxide and sodium hypochlorite on survival and impairment of three phytoplankton species

  • Kim, Keunyong (Department of Oceanography, College of Natural Sciences, Chonnam National University) ;
  • Kim, Kwang Young (Department of Oceanography, College of Natural Sciences, Chonnam National University) ;
  • Kim, Ju-Hyoung (Department of Oceanography, College of Natural Sciences, Chonnam National University) ;
  • Kang, Eun Ju (Department of Oceanography, College of Natural Sciences, Chonnam National University) ;
  • Jeong, Hae Jin (School of Earth and Environmental Sciences, College of Natural Sciences, Seoul National University) ;
  • Lee, Kitack (School of Environmental Science and Engineering, Pohang University of Science and Technology)
  • Received : 2013.02.27
  • Accepted : 2013.05.21
  • Published : 2013.06.15
Download PDF
⟨ Previous Next ⟩

Abstract

Sodium hypochlorite (NaOCl) is widely used to disinfect seawater in power plant cooling systems in order to reduce biofouling, and in ballast water treatment systems to prevent transport of exotic marine species. While the toxicity of NaOCl is expected to increase by ongoing ocean acidification, and many experimental studies have shown how algal calcification, photosynthesis and growth respond to ocean acidification, no studies have investigated the relationship between NaOCl toxicity and increased $CO_2$. Therefore, we investigated whether the impacts of NaOCl on survival, chlorophyll a (Chl-a), and effective quantum yield in three marine phytoplankton belonging to different taxonomic classes are increased under high $CO_2$ levels. Our results show that all biological parameters of the three species decreased under increasing NaOCl concentration, but increasing $CO_2$ concentration alone (from 450 to 715 ${\mu}atm$) had no effect on any of these parameters in the organisms. However, due to the synergistic effects between NaOCl and $CO_2$, the survival and Chl-a content in two of the species, Thalassiosira eccentrica and Heterosigma akashiwo, were significantly reduced under high $CO_2$ when NaOCl was also elevated. The results show that combined exposure to high $CO_2$ and NaOCl results in increasing toxicity of NaOCl in some marine phytoplankton. Consequently, greater caution with use of NaOCl will be required, as its use is widespread in coastal waters.

Keywords

References

  1. Allonier, A. -S., Khalanski, M., Camel, V. & Bermond, A. 1999. Characterization of chlorination by-products in cooling effluents of coastal nuclear power stations. Mar. Pollut. Bull. 38:1232-1241. https://doi.org/10.1016/S0025-326X(99)00168-X
  2. Anasco, N. C., Koyama, J., Imai, S. & Nakamura, K. 2008. Toxicity of residual chlorines from hypochlorite-treated seawater to marine amphipod Hyale barbicornis and estuarine fish Oryzias javanicus. Water Air Soil Pollut. 195:129-136. https://doi.org/10.1007/s11270-008-9732-x
  3. Arar, E. J. & Collins, G. B. 1997. Method 445.0, in vitro determination of chlorophyll a and pheophytin a in marine and freshwater algae by fluorescence. National Exposure Research Laboratory, Office of Research and Development, U.S. Environmental Protection Agency, Cincinnati, OH, 22 pp.
  4. Booth, J. A. T., McPhee-Shaw, E. E., Chua, P., Kingsley, E., Denny, M., Phillips, R., Bograd, S. J., Zeidberg, L. D. & Gilly, W. F. 2012. Natural intrusions of hypoxic, low pH water into nearshore marine environments on the California coast. Cont. Shelf Res. 45:108-115. https://doi.org/10.1016/j.csr.2012.06.009
  5. Branco, D., Lima, A., Almeida, S. F. P. & Figueira, E. 2010. Sensitivity of biochemical markers to evaluate cadmium stress in the freshwater diatom Nitzschia palea (Kutzing) W. Smith. Aquat. Toxicol. 99:109-117. https://doi.org/10.1016/j.aquatox.2010.04.010
  6. Caldeira, K. & Wickett, M. E. 2003. Anthropogenic carbon and ocean pH. Nature 425:365. https://doi.org/10.1038/425365a
  7. Clesceri, L. S., Greenberg, A. E. & Eaton, A. D. 1999. Standard methods for the examination of water and wastewater. 20th ed. American Public Health Association, Washington DC, 1325 pp.
  8. Doropoulos, C. & Diaz-Pulido, G. 2013. High $CO_2$ reduces the settlement of a spawning coral on three common species of crustose coralline algae. Mar. Ecol. Prog. Ser. 475:93-99. https://doi.org/10.3354/meps10096
  9. Echeveste, P., Agusti, S. & Dachs, J. 2010. Cell size dependent toxicity thresholds of polycyclic aromatic hydrocarbons to natural and cultured phytoplankton populations. Environ. Pollut. 158:299-307. https://doi.org/10.1016/j.envpol.2009.07.006
  10. Endo, H., Yoshimura, T., Kataoka, T. & Suzuki, K. 2013. Effects of $CO_2$ and iron availability on phytoplankton and eubacterial community compositions in the northwest subarctic Pacific. J. Exp. Mar. Biol. Ecol. 439:160-175. https://doi.org/10.1016/j.jembe.2012.11.003
  11. Endresen, O., Behrens, H. L., Brynestad, S., Andersen, A. B. & Skjong. R. 2004. Challenges in global ballast water management. Mar. Pollut. Bull. 48:615-623. https://doi.org/10.1016/j.marpolbul.2004.01.016
  12. Finney, D. J. 1971. Probit analysis. 3rd ed. Cambridge University Press, Cambridge, 333 pp.
  13. Franklin, D. J., Choi, C. J., Hughes, C., Malin, G. & Berges, J. A. 2009. Effect of dead phytoplankton cells on the appearent efficiency of photosystem II. Mar. Ecol. Prog. Ser. 382:35-40. https://doi.org/10.3354/meps07967
  14. Franklin, N. M., Stauber, J. L., Apte, S. C. & Lim, R. P. 2002. Effect of initial cell density on the bioavailability and toxicity of copper in microalgal bioassays. Environ. Toxicol. Chem. 21:742-751. https://doi.org/10.1002/etc.5620210409
  15. Gao, K., Helbling, E. W., Hader, D. -P. & Hutchins, D. A. 2012a. Responses of marine primary producers to interactions between ocean acidification, solar radiation, and warming. Mar. Ecol. Prog. Ser. 470:167-189. https://doi.org/10.3354/meps10043
  16. Gao, K., Xu, J., Gao, G., Li, Y., Hutchins, D. A., Huang, B., Wang, L., Zheng, Y., Jin, P., Cai, X., Hader, D. -P., Li, W., Xu, K., Liu, N. & Riebesell, U. 2012b. Rising $CO_2$ and increased light exposure synergistically reduce marine primary productivity. Nat. Clim. Change 2:519-523.
  17. Gray, D. K., Duggan, I. C. & MacIsaac, H. J. 2006. Can sodium hypochlorite reduce the risk of species introductions from diapausing invertebrate eggs in non-ballasted ships? Mar. Pollut. Bull. 52:689-695. https://doi.org/10.1016/j.marpolbul.2005.11.001
  18. Gregg, M. D. & Hallegraeff, G. M. 2007. Efficacy of three commercially available ballast water biocides against vegetative microalgae, dinoflagellate cysts and bacteria. Harmful Algae 6:567-584. https://doi.org/10.1016/j.hal.2006.08.009
  19. Hernandez-Ayon, J. M., Belli, S. L. & Zirino, A. 1999. pH, alkalinity and total $CO_2$ in coastal seawater by potentiometric titration with a difference derivative readout. Anal. Chim. Acta 394:101-108. https://doi.org/10.1016/S0003-2670(99)00207-X
  20. Hinga, K. R. 2002. Effects of pH on coastal marine phytoplankton. Mar. Ecol. Prog. Ser. 238:281-300. https://doi.org/10.3354/meps238281
  21. Hofmann, G. E., Smith, J. E., Johnson, K. S., Send, U., Levin, L. A., Micheli, F., Paytan, A., Price, N. N., Peterson, B., Takeshita, Y., Matson, P. G., Crook, E. D., Kroeker, K. J., Gambi, M. C., Rivest, E. B., Frieder, C. A., Yu, P. C. & Martz, T. R. 2011. High-frequency dynamics of ocean pH: a multi-ecosystem comparison. PLoS ONE 6:e28983. https://doi.org/10.1371/journal.pone.0028983
  22. Jeong, H. J., Kim, H. R., Kim, K. I., Kim, K. Y., Park, K. H., Kim, S. T., Yoo, Y. D., Song, J. Y., Kim, J. S., Seong, K. A., Yih, W. H., Pae, S. J., Lee, C. H., Huh, M. D. & Lee, S. H. 2002. NaOCl produced by electrolysis of natural seawater as a potential method to control marine red-tide dinoflagellates. Phycologia 41:643-656. https://doi.org/10.2216/i0031-8884-41-6-643.1
  23. Kester, D. R. 1986. Equilibrium models in seawater: applications and limitations. In Bernhard, M., Brinckman, F. E. & Sadler, P. J. (Eds.) The Importances of Chemical "Speciation" in Environmental Processes. Springer Verlag, Berlin, pp. 337-363.
  24. Kroeker, K. J., Kordas, R. L., Crim, R., Hendriks, I. E., Ramajo, L., Singh, G. S., Duarte, C. M. & Gattuso, J. -P. 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Glob. Change Biol. 19:1884-1896. https://doi.org/10.1111/gcb.12179
  25. Lewis, E. & Wallace, D. W. R. 1998. Program developed for $CO_2$ system calculation. ORNL/CDIAC-105. Carbon Dioxide Information Analysis Center, Oak Ridge National Laboratory, Department of Energy, Oak Ridge, TN, 74 pp.
  26. Lumsden, B. R. & Florence, T. M. 1983. A new algal assay procedure for the determination of the toxicity of copper species in seawater. Environ. Technol. Lett. 4:271-276. https://doi.org/10.1080/09593338309384205
  27. McCarthy, A., Rogers, S. P., Duffy, S. J. & Campbell, D. A. 2012. Elevated carbon dioxide differentially alters the photophysiology of Thalassiosira pseudonana (Bacillariophyceae) and Emiliania huxleyi (Haptophyta). J. Phycol. 48:635-646. https://doi.org/10.1111/j.1529-8817.2012.01171.x
  28. Millero, F. J., Zhang, J. -Z., Lee, K. & Campbell, D. M. 1993. Titration alkalinity of seawater. Mar. Chem. 44:153-165. https://doi.org/10.1016/0304-4203(93)90200-8
  29. Orr, J. C., Fabry, V. J., Aumont, O., Bopp, L., Doney, S. C., Feely, R. A., Gnanadesikan, A., Gruber, N., Ishida, A., Joos, F., Key, R. M., Lindsay, K., Maier-Reimer, E., Matear, R., Monfray, P., Mouchet, A., Najjar, R. G., Plattner, G. -K., Rodgers, K. B., Sabine, C. L., Sarmiento, J. L., Schlitzer, R., Slater, R. D., Totterdell, I. J., Weirig, M. -F., Yamanaka, Y. & Yool, A. 2005. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 437:681-686. https://doi.org/10.1038/nature04095
  30. Polman, H., Verhaart, F. & Bruijs, M. 2013. Impact of biofouling in intake pipes on the hydraulics and efficiency of pumping capacity. Desalination Water Treat. 51:997-1003. https://doi.org/10.1080/19443994.2012.707371
  31. Rajamohan, R., Vinnitha, E., Venugopalan, V. P. & Narasimhan, S. V. 2007. Chlorination by-products and their discharge from the cooling water system of a coastal electric plant. Curr. Sci. 93:1608-1612.
  32. Saleem, M., Chakrabarti, M. H., Hasan, D. B., Islam, M. S., Yussof, R., Hajimolana, S. A., Hussain, M. A., Khan, G. M. A. & Ali, B. S. 2012. On site electrochemical production of sodium hypochlorite disinfectant for a power plant utilizing seawater. Int. J. Electrochem. Sci. 7:3929-3938.
  33. Sanchez-Marin, P., Slaveykova, V. I. & Beiras, R. 2010. Cu and Pb accumulation by the marine diatom Thalassiosira weissflogii in the presence of humic acids. Environ. Chem. 7:309-317. https://doi.org/10.1071/EN10015
  34. Sarbatly, R. H. J. & Krishnaiah, D. 2007. Free chlorine residual content within the drinking water distribution system. Int. J. Phys. Sci. 2:196-201.
  35. Schippers, P., Lurling, M. & Scheffer, M. 2004. Increase of atmospheric $CO_2$ promotes phytoplankton productivity. Ecol. Lett. 7:446-451. https://doi.org/10.1111/j.1461-0248.2004.00597.x
  36. Schreiber, U., Bilger, W. & Neubauer, C. 1994. Chlorophyll fluorescence as a non-instructive indicator for rapid assessment of in vivo photosynthesis. In Schulze, E. D. & Caldwell, M. M. (Eds.) Ecophysiology of Photosynthesis. Springer, Berlin, pp. 49-70.
  37. Smayda, T. J. 2007. Reflections on the ballast water dispersal: harmful algal bloom paradigm. Harmful Algae 6:601-622. https://doi.org/10.1016/j.hal.2007.02.003
  38. Sugam, R. & Helz, G. R. 1976. Apparent ionization constant of hypochlorous acid in sea water. Environ. Sci. Technol. 10:384-386. https://doi.org/10.1021/es60115a012
  39. Taylor, C. J. L. 2006. The effects of biological fouling control at coastal and estuarine power stations. Mar. Pollut. Bull. 53:30-48. https://doi.org/10.1016/j.marpolbul.2006.01.004
  40. White, G. C. 1992. Handbook of chlorination and alternative disinfectants. 3rd ed. Van Nostrand Reinhold, Toronto, ON, 1308 pp.

Cited by

  1. Environmental risks associated with ballast water management systems that create disinfection by-products (DBPs) vol.105, 2015, https://doi.org/10.1016/j.ocecoaman.2015.01.004
  2. Enhancing the efficacy of electrolytic chlorination for ballast water treatment by adding carbon dioxide vol.95, pp.1, 2015, https://doi.org/10.1016/j.marpolbul.2015.03.025
  3. Adaptations of a green tide formingUlva linza(Ulvophyceae, Chlorophyta) to selected salinity and nutrients conditions mimicking representative environments in the Yellow Sea vol.55, pp.2, 2016, https://doi.org/10.2216/15-67.1
  4. Enhancement of photosynthetic carbon assimilation efficiency by phytoplankton in the future coastal ocean vol.10, pp.11, 2013, https://doi.org/10.5194/bg-10-7525-2013