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Influence of non-nutrient environmental factors on Ulva pertusa's inhibitory effects on Heterosigma akashiwo growth

Published online by Cambridge University Press:  15 October 2015

Qiu Jin ,
Han-Gui Wu ,
Xin-Xin Zhang  and
Zhong-Lu Ke
Qiu Jin
Affiliation:
Biopharmaceutical Research and Development Center, Taizhou Vocational and Technical College, Taizhou 318000, China
Han-Gui Wu*
Affiliation:
Biopharmaceutical Research and Development Center, Taizhou Vocational and Technical College, Taizhou 318000, China
Xin-Xin Zhang
Affiliation:
Biopharmaceutical Research and Development Center, Taizhou Vocational and Technical College, Taizhou 318000, China
Zhong-Lu Ke
Affiliation:
Biopharmaceutical Research and Development Center, Taizhou Vocational and Technical College, Taizhou 318000, China
*
Correspondence should be addressed to:H.-G. Wu, Biopharmaceutical Research and Development Center, Taizhou Vocational and Technical College, Taizhou 318000, China email: [email protected]; [email protected]
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Abstract

We studied the effects of four non-nutrient environmental factors (temperature, salinity, irradiance and pH) on the growth inhibition of the macroalgae Ulva pertusa (Chlorophyta) upon the microalgae Heterosigma akashiwo (Rhaphidophyta). Experiments were conducted in single-factor incubation and various two-factor combination experiments in which temperature (10, 15, 25 and 30°C), salinity (10, 20, 30 and 40 g kg−1 water), irradiance (20, 100, 200 and 400 μmol m−2 s−1), and pH (5.5, 7, 8.5 and 10) were varied systematically. The growth rates of U. pertusa and H. akashiwo and the rate of microalgal growth inhibition were altered significantly by changing some of the non-nutrient factors in both the single-factor and the two-factor experiments. The optimal growth conditions for U. pertusa were 20–25°C, salinity of 30 g kg−1, irradiance level of 200–400 μmol m−2 s−1, and pH 8.5–10; optimal conditions for H. akashiwo growth were 25°C, 30 g kg−1, 100 μmol m−2 s−1 and pH 8.5, respectively. The growth inhibitory influence of U. pertusa on H. akashiwo was strongest at 25°C with low salinity (10 g kg−1), high irradiance (400 μmol m−2 s−1) and high alkalinity (pH = 10). The results of this study may be helpful in the development of methods for using green macroalgae to control the proliferation of microalgae in harmful algal blooms (HABs). In particular, these findings provide guidance regarding optimum levels of non-nutrient environmental factors in confined areas, such as aquaculture factories.

Keywords

Mitigation of harmful algal bloomallelopathyUlva pertusaHeterosigma akashiwo
Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 96 , Issue 5 , August 2016 , pp. 1041 - 1052
Copyright
Copyright © Marine Biological Association of the United Kingdom 2015 

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References

REFERENCES

Alamsjah, M.A., Hirao, S., Ishibashi, F. and Fujita, Y. (2005) Isolation and structure determination of algicidal compounds from Ulva fasciata . Bioscience, Biotechnology, and Biochemistry 69, 2186–2192.CrossRefGoogle ScholarPubMed
Alamsjah, M.A., Hirao, S., Ishibashi, F., Oda, T. and Fujita, Y. (2008) Algicidal activity of polyunsaturated fatty acids derived from Ulva fasciata and U. pertusa (Ulvaceae, Chlorophyta) on phytoplankton. Journal of Applied Phycology 20, 713–720.CrossRefGoogle Scholar
Butron, A., Madariaga, I. and Orive, E. (2012) Tolerance to high irradiance levels as a determinant of the bloom-forming Heterosigma akashiwo success in estuarine waters in summer. Estuarine, Coastal and Shelf Science 107, 141–149.Google Scholar
Cade-Menun, B.J. and Paytan, A. (2010) Nutrient temperature and light stress alter phosphorus and carbon forms in culture-grown algae. Marine Chemistry 121, 27–36.Google Scholar
Cohen, R.A. and Fong, P. (2004) Physiological responses of a bloom-forming green macroalga to short-term change in salinity, nutrients, and light help explain its ecological success. Estuaries 27, 209–216.Google Scholar
Engstr, J., Repka, S. and Mikkonen, M. (2011) Interactions between plankton and cyanobacterium Anabaena with focus on salinity, growth and toxin production. Harmful Algae 10, 530–535.Google Scholar
Garry, R.T., Hearing, P. and Cosper, E.M. (1998) Characterization of a lytic virus infectious to the bloom-forming microalga Aureococcus anophagefferens (Pelagophyceae). Journal of Phycology 34, 616–621.Google Scholar
Gross, E.M. (2003) Allelopathy of aquatic autotrophs. Critical Reviews in Plant Sciences 22, 313–339.Google Scholar
Gross, E.M., Hilt, S., Lombardo, P. and Mulderij, G. (2007) Searching for allelopathic effects of submerged macrophytes on phytoplankton – state of the art and open questions. Hydrobiologia 584, 77–88.Google Scholar
Guillard, R.R. and Ryther, J.H. (1962) Studies of marine planktonic diatoms. I. Cyclotella nana (Hustedt), and Detonula confervacea (Cleve). Canadian Journal of Microbiology 8, 229–239.Google Scholar
Guo, Y. (1994) Studies on Heterosigma akashiwo (Hada) Hada in the Dalian Bight, Liaoning, China. Oceanologia et Limnologia Sinica 25, 211–215.Google Scholar
Han, M.S., Kim, Y.P. and Cattolico, R.A. (2002) Heterosigma akashiwo (Raphidophyceae) resting cell formation in batch culture: strain identity versus physiological response. Journal of Phycology 38, 304–317.Google Scholar
Henley, W.J., Lindley, S.T., Levavasseur, G., Osmond, C.B. and Ramus, J. (1992) Photosynthetic response of Ulva rotundata to light and temperature during emersion on an intertidal sand flat. Oecologia 89, 516–523.Google Scholar
Hofmann, G.E., Barry, J.P., Edmunds, P.J., Gates, R.D., Hutchins, D.A., Klinger, T. and Sewell, M.A. (2010) The effect of ocean acidification on calcifying organisms in marine ecosystems: an organism to ecosystem perspective. Annual Review of Ecology, Evolution, and Systematics 41, 127–147.Google Scholar
Hu, H. and Hong, Y. (2008) Algal-bloom control by allelopathy of aquatic macrophytes – a review. Frontiers of Environmental Science & Engineering in China 2, 421–438.Google Scholar
Imai, I., Ishida, Y. and Hata, Y. (1993) Killing of marine phytoplankton by a gliding bacterium Cytophaga sp., isolated from the coastal sea of Japan. Marine Biology 116, 527–532.Google Scholar
Jeong, J.H., JIN, H.J. and Sohn, C.H. (2000) Algicidal activity of the seaweed Corallina pilulifera against red tide microalgae. Journal of Applied Phycology 12, 37–43.CrossRefGoogle Scholar
Jin, Q. and Dong, S. (2003) Comparative studies on the allelopathic effects of two different strains of Ulva pertusa on Heterosigma akashiwo and Alexandrium tamarense . Journal of Experimental Marine Biology and Ecology 293, 41–55.Google Scholar
Jin, Q., Dong, S. and Wang, C. (2005) Allelopathic growth inhibition of Prorocentrum micans (Dinophyta) by Ulva pertusa and Ulva linza (Chlorophyta) in laboratory cultures. European Journal of Phycology 40, 31–37.Google Scholar
Kakinuma, M., Coury, D.A., Kuno, Y., Itoh, S., Kozawa, Y., Inagaki, E., Yoshiura, Y. and Amano, H. (2006) Physiological and biochemical responses to thermal and salinity stresses in a sterile mutant of Ulva pertusa (Ulvales, Chlorophyta). Marine Biology 149, 97–106.Google Scholar
Keating, K.I. (1977) Allelopathic influence on blue-green bloom sequence in a eutrophic lake. Science 196, 885–887.Google Scholar
Kim, H., Spivack, A.J. and Menden-Deuer, S. (2013) pH alters the swimming behaviors of the raphidophyte Heterosigma akashiwo: implications for bloom formation in an acidified ocean. Harmful Algae 26, 1–11.Google Scholar
Kim, M.C., Yoshinaga, I., Nagasaki, K., Itakura, S. and Ishida, Y. (1998) A close relationship between algicidal bacteria and termination of Heterosigma akashiwo (Raphidophyceae) bloom in Hiroshima Bay, Japan. Marine Ecology Progress Series 170, 25–32.Google Scholar
Kim, M.J., Choi, J.S., Kang, S.E., Cho, J.Y., Jin, H.J., Chun, B.S. and Hong, Y.K. (2004) Multiple allelopathic activity of the crustose coralline alga Lithophyllum yessoense against settlement and germination of seaweed spores. Journal of Applied Phycology 16, 175–179.CrossRefGoogle Scholar
Lee, S.J., Kim, Y., Kim, H.G., Seo, G.M., Jeong, J.H. and Hong, Y.K. (2000) Algalytic activity of a-mannosidase on harmful marine micoalgae. Journal of Applied Phycology 12, 191–193.Google Scholar
Lobon, N.C., Gallego, J.C.A., Diaz, T.S. and Garcia, J.C.E. (2002) Allelopathic potential of Cistus ladanifer chemicals in response to variations of light and temperature. Chemoecology 12, 139–145.Google Scholar
Lomas, M.W. and Glibert, P.M. (1999) Interactions between NH4 + and NO3 − uptake and assimilation: comparison of diatoms and dinoflagellates at several growth temperatures. Marine Biology 133, 541–551.Google Scholar
Martinez, R., Orive, E., Laza-Martinez, A. and Seoane, S. (2010) Growth response of six strains of Heterosigma akashiwo to varying temperature, salinity and irradiance conditions. Journal of Plankton Research 32, 529–538.Google Scholar
Menéndez, M., Martínez, M. and Comín, F.A. (2001) A comparative study of the effect of pH and inorganic carbon resources on the photosynthesis of three floating macroalgae species of a Mediterranean coastal lagoon. Journal of Experimental Marine Biology and Ecology 256, 123–136.Google Scholar
Molisch, H. (1937) Der Einfluss einer Pflanze aufdie andere-Allelopathie. Jena: Fischer, pp. 158–160.Google Scholar
Na, G.H., Choi, W.J. and Chun, Y.Y. (1996) A study on red tide control with loess suspension. Korean Journal of Aquaculture 9, 239–245.Google Scholar
Nakai, S., Inoue, Y., Hosomi, M. and Murakami, A. (1999) Growth inhibition of blue–green algae by allelopathic effects of macrophytes. Water Science and Technology 39, 47–53.Google Scholar
Nakai, S., Inoue, Y., Hosomi, M. and Murakami, A. (2000) Myriophyllum spicatum-released allelopathic polyphenols inhibiting growth of blue-green algae Microcystis aeruginosa . Water Research 34, 3026–3032.Google Scholar
Nan, C., Zhang, H., Lin, S., Zhao, G. and Liu, X. (2008) Allelopathic effects of Ulva lactuca on selected species of harmful bloom-forming microalgae in laboratory cultures. Aquatic Botany 89, 9–15.CrossRefGoogle Scholar
Nelson, T.A., Lee, D.J. and Smith, B.C. (2003) Are ‘green tides’ harmful algal blooms? Allelopathic properties of extracts from Ulva fenestrata and Ulvaria obscura . Journal of Phycology 39, 874–879.CrossRefGoogle Scholar
Ray, S. and Bagchi, S.N. (2001) Nutrients and pH regulate algicide accumulation in cultures of the cyanobacterium Oscillatoria laetevirens . New Phytologist 149, 455–460.Google Scholar
Schmidt, L.E. and Hansen, P.J. (2001) Allelopathy in the prymnesiophyte Chrysochromulina polylepis: effect of cell concentration, growth phase and pH. Marine Ecology Progress Series 216, 67–81.Google Scholar
Shikata, T., Nagasoe, S., Matsubara, T., Yamasaki, Y., Shimasaki, Y., Oshima, Y. and Honjo, T. (2007) Effects of temperature and light on cyst germination and germinated cell survival of the noxious raphidophyte Heterosigma akashiwo . Harmful Algae 6, 700–706.Google Scholar
Slattery, M. and Lesser, M.P. (2014) Allelopathy in the tropical alga Lobophora variegata (Phaeophyceae): mechanistic basis for a phase shift on mesophotic coral reefs? Journal of Phycology 50, 493–505.Google Scholar
Smayda, T.J. (1997) Harmful algal blooms: their ecophysiology and general relevance to phytoplankton blooms in the sea. Limnology and Oceanography 42, 1137–1153.Google Scholar
Steidinger, K.A. (1983) A re-evaluation of toxic dinoflagellate biology and ecology. Phycological Research 2, 147–188.Google Scholar
Sun, W., Yu, Z. and Yu, S. (1989) The harness of an eutrophic water body by water-hyacinth. Acta Scientiae Circumstantiae 9, 188–195.Google Scholar
Sun, X., Song, X. and Zhang, B. (1999) A study on the coagulation of clay–MMH system with red tide organisms. Marine Sciences 13, 46–49.Google Scholar
Tang, Y.Z. and Gobler, C.J. (2011) The green macroalga, Ulva lactuca, inhibits the growth of seven common harmful algal bloom species via allelopathy. Harmful Algae 10, 480–488.Google Scholar
Taylor, R., Fletcher, R.L. and Raven, J.A. (2001) Preliminary studies on the growth of selected ‘green tide'algae in laboratory culture: effects of irradiance, temperature, salinity and nutrients on growth rate. Botanica Marina 44, 327–336.CrossRefGoogle Scholar
Valenti, T.W. Jr, James, S.V., Lahousse, M.J., Schug, K.A., Roelke, D.L., Grover, J.P. and Brooks, B.W. (2010) A mechanistic explanation for pH-dependent ambient aquatic toxicity of Prymnesium parvum carter. Toxicon 55, 990–998.Google Scholar
Valenti, T.W. Jr (2010) Influence of pH on amine toxicology and implications for harmful algal bloom ecology. Toxicon 55, 1038–1043.Google Scholar
van Donk, E. and van de Bund, W.J. (2002) Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquatic Botany 72, 261–274.Google Scholar
Wallace, R.B. and Gobler, C.J. (2015) Factors controlling blooms of microalgae and macroalgae (Ulva rigida) in a eutrophic, urban estuary: Jamaica Bay, NY, USA. Estuaries and Coasts 38, 519–533.Google Scholar
Wang, Y., Yu, Z., Song, X., Tang, X. and Zhang, S. (2007) Effects of macroalgae Ulva pertusa (Chlorophyta) and Gracilaria lemaneiformis (Rhodophyta) on growth of four species of bloom-forming dinoflagellates. Aquatic Botany 86, 139–147.Google Scholar
Yan, T., Zhou, M. and Qian, P. (2002) Growth of fish-killing red tide species Raphidophyte Heterosigma akashiwo . Oceanologia et Limnologia Sinica 33, 209–214.Google Scholar
Ye, C., Liao, H. and Yang, Y. (2014) Allelopathic inhibition of photosynthesis in the red tide-causing marine alga, Scrippsiella trochoidea (Pyrrophyta), by the dried macroalga, Gracilaria lemaneiformis (Rhodophyta). Journal of Sea Research 90, 10–15.Google Scholar
Zhou, C., Wang, F. and Yan, X. (2008) Effects of temperature, salinity and irradiance on the cell stability of Heterosigma akashiwo Hada. Marine Environmental Science 27, 17–20.Google Scholar