Effects of temperature, salinity, and irradiance on the growth of harmful algal bloom species Phaeocystis globosa Scherffel (Prymnesiophyceae) isolated from the South China Sea

  • Ning Xu (徐宁)
  • Bozhu Huang (黄博珠)
  • Zhangxi Hu (胡章喜)
  • Yingzhong Tang (唐赢中)
  • Shunshan Duan (段舜山)
  • Chengwu Zhang (张成武)
Biology

Abstract

Blooms of Phaeocystis globosa have been frequently reported in Chinese coastal waters, causing serious damage to marine ecosystems. To better understand the ecological characteristics of P. globosa in Chinese coastal waters that facilitate its rapid expansion, the effects of temperature, salinity and irradiance on the growth of P. globosa from the South China Sea were examined in the laboratory. The saturating irradiance for the growth of P. globosa (I s) was 60 μmol/(m2∙s), which was lower than those of other harmful algal species (70–114 μmol/(m2∙s)). A moderate growth rate of 0.22/d was observed at 2 μmol/(m2∙s) (the minimum irradiance in the experiment), and photo-inhibition did not occur at 230 μmol/(m2∙s) (the maximum irradiance in the experiment). Exposed to 42 different combinations of temperatures (10–31°C) and salinities (10–40) under saturating irradiance, P. globosa exhibited its maximum specific growth rate of 0.80/d at the combinations of 24°C and 35, and 27°C and 40. The optimum growth rates (>0.80/d) were observed at temperatures ranging from 24 to 27°C and salinities from 35 to 40. While P. globosa was able to grow well at temperatures from 20°C to 31°C and salinities from 20 to 40, it could not grow at temperatures lower than 15°C or salinities lower than 15. Factorial analysis revealed that temperature and salinity has similar influences on the growth of this species. This strain of P. globosa not only prefers higher temperatures and higher salinity, but also possesses a flexible nutrient competing strategy, adapted to lower irradiance. Therefore, the P. globosa population from South China Sea should belong to a new ecotype. There is also a potentially high risk of blooms developing in this area throughout the year.

Keywords

Phaeocystis globosa harmful algal bloom temperature salinity irradiance growth 

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References

  1. Al-Hasan R H, Ali A M, Radwan S S. 1990. Lipids, and their constituent fatty acids, of Phaeocystis sp. from the Arabian Gulf. Mar. Biol., 105 (1): 9–14.CrossRefGoogle Scholar
  2. Anderson D M, Glibert P M, Burkholder J M. 2002. Harmful algal blooms and eutrophication: nutrient sources, composition, and consequences. Estuaries, 25 (4): 04–726.CrossRefGoogle Scholar
  3. Camacho R A, Martin J L, Watson B, Paul M, Zheng L, Stribling J B. 2015. Modeling the factors controlling phytoplankton in the St. Louis Bay estuary, Mississippi and evaluating estuarine responses to nutrient load modifications. Journal of Environmental Engineering, 141 (3), http://dx.doi.org/10. 1061/(ASCE)EE.1943-7870.0000892.Google Scholar
  4. Carstensen J, Henriksen P, Heiskanen A S. 2007. Summer algal blooms in shallow estuaries: definition, mechanisms, and link to eutrophication. Limnology and Ocean ography, 5 2 (1): 70–384.Google Scholar
  5. Chang F H, Vincent W F, Woods P H. 1992. Nitrogen utilization by size-fractionated phytoplankton assemblages associated with an upwelling event off Westland, New Zealand. New Zealand Journal of Marine and Freshwater Research, 26 (3-4): 287–301.CrossRefGoogle Scholar
  6. Chen J F, Xu N, Jiang T J, Wang Y, Wang Z H, Qi Y Z. 1999. A report of Phaeocystis globosa bloom in coastal water of Southeast China. Journal of Ji’nan University (Natural Science & Medicine Edition ), 20 (3): 24–129. (in Chinese with English abstract)Google Scholar
  7. Chen L F, Zhang Q, Luo Y M, Han B P. 2003. Molecular identification of the Hong Kong strain P 2 of Ph o eocystis as Phaeocystis globosa. Ecologic Science, 22 (4): 49–350. (in Chinese with English abstract)Google Scholar
  8. Chen Y Q, Wang N, Zhang P, Zhou H, Qu L H. 2002. Molecular evidence identifies bloom-forming Phaeocystis (Prymnesiophyta) from coastal waters of southeast China as Phaeocystis globosa. Biochemical Systematics and Ecology, 30 (1): 5–22.CrossRefGoogle Scholar
  9. Domingues R B, Anselmo T P, Barbosa A B, Sommer U, Galvão H M. 2011. Light as a driver of phytoplankton growth and production in the freshwater tidal zone of a turbid estuary. Estuarine, Coastal and Shelf Science, 91 (4): 26–535.CrossRefGoogle Scholar
  10. Ellegaard M, Christensen N F, Meostrup A. 1993. Temperature and salinity effects on growth of a non-chain-forming strain of Fymnodinium catenatum (Dinoohyceae) established from a cyst from recent sediments in the Sound (resund), Denmark. J. Phycol., 29 (4): 18–426.CrossRefGoogle Scholar
  11. El-Sayed S Z, Biggs D C, Holm-Hansen O. 1983. Phytoplankton standing crop, primary productivity, and near-surface nitrogenous nutrient fields in the Ross Sea, Antarctica. Deep Sea Res earch Part A. Oceanographic Research Papers, 30 (8): 71–886.Google Scholar
  12. Fu F X, Tatters A O, Hutchins D A. 2012. Global change and the future of harmful algal blooms in the ocean. Marine Ecology Progress Series, 470: 07–233.CrossRefGoogle Scholar
  13. Garrison D L, Buck K R, Fryxell G A. 1987. Algal assemblages in Antarctic pack ice and in ice-edge plankton. J. Phycol., 23 (4): 64–572.Google Scholar
  14. Grimm N, Weisse T. 1985. Die Temperaturabhängigkeit des Wachstums von Phaeocystis pouchetii (Haptophyceae) in Batchkulturen. Helgol ä nder Meeresuntersuchungen, 39 (2): 01–211.Google Scholar
  15. Guillard R R L. 1973. Division rates. In: Stein J R ed. Handbook of Phycological Methods. Culture Methods and Growth Measurements. Cambridge University Press, Cambridge. p.289–311.Google Scholar
  16. Guillard R R L. 1975. Culture of phytoplankton for feeding marine invertebrates. In: Smith W L, Chanley M H eds. Cultures of Marine Invertebrate Animals. Plenum Press, New York. p.29–60.CrossRefGoogle Scholar
  17. Harris G P, Lott J N A. 1973. Light intensity and photosynthetic rates in phytoplankton. Journal of the Fisheries Research Board of Canada, 30 (12): 771–1778.Google Scholar
  18. Harrison P J, Waters R E, Taylor F J R. 1980. A broad spectrum artificial sea water medium for coastal and open ocean phytoplankton 1. Journal of Phycology, 16 (1): 8–35.CrossRefGoogle Scholar
  19. He J W, Shi Z X, Zhang Y H, Liu Y D, Jiang T J, Yin Y W, Qi Y Z. 1999. Morphological characteristics and toxins of Phaeocystis cf. pouchetii (prymnesiophyceae). Oceanologia et Limnologia Sinica, 30 (2): 72–179. (in Chinese with English abstract)Google Scholar
  20. Heisler J, Glibert P M, Burkholder J M, Anderson D M, Cochlan W, Dennison W C, Dortch Q, Gobler C J, Heil C A, Humphries E, Lewitus A, Magnien R, Marshallm H G, Sellner K, Stockwell D A, Stoecker D K, Suddleson M. 2008. Eutrophication and harmful algal blooms: a scientific consensus. Harmful A lgae, 8 (1): 3–13.CrossRefGoogle Scholar
  21. Howarth R, Chan F, Conley D J, Garnier J, Doney S C, Marino R, Billen G. 2011. Coupled biogeochemical cycles: eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems. Frontiers in Ecology and the Environment, 9 (1): 8–26.CrossRefGoogle Scholar
  22. Hu Z X, Xu N, Duan S S, Li A, Zhang C W. 2010. Effects of urea on the growth of Phaeocystis globosa, Scrippsiella trochoidea, Skeletonema costatum. Acta Scientiae Circumstantiae, 30 (6): 265–1270. (in Chinese with English abstract)Google Scholar
  23. Jahnke J, Baumann M E M. 1987. Differentiation between Phaeocystis pouchetii (Har.) Lagerheim and Phaeocystis globosa Scherffel I. Colony shapes and temperature tolerance. Hydrobiol. Bull., 21 (2): 41–147.CrossRefGoogle Scholar
  24. Jahnke J. 1989. The light and temperature dependence of growth rate and elemental composition of Phaeocystis globosa scherffel and 1 (Har.) Lagerh. in batch cultures. Neth. J. Sea Res., 23 (1): 5–21.CrossRefGoogle Scholar
  25. Kim D I, Matsuyama Y, Nagasoe S, Yamaguchi M, Yoon Y H, Oshima Y, Imada N, Honjo T. 2004. Effects of temperature, salinity and irradiance on the growth of the harmful red tide dinoflagellate Cochlodinium polykri koides Margalef (Dinophyceae). J. Plankton. Res., 26 (1): 1–66.CrossRefGoogle Scholar
  26. Lancelot C, Billen G, Sournia A, Weisse T, Colijn F, Veldhuis M J W, Davies A, Wassmann P. 1987. Phaeocystis blooms and nutrient enrichment in the continental coastal zones of the North Sea. Ambio, 16 (1): 8–46.Google Scholar
  27. Lancelot C, Veth C, Mthot S. 1991. Modelling ice-edge phytoplankton bloom in the Scotia-Weddell sea sector of the Southern Ocean during spring 1988. Journal of Marine Systems, 2 (3-4): 333–346.CrossRefGoogle Scholar
  28. Lederman T C, Tett P. 1981. Problems in modelling the photosynthesis-light relationship for phytoplankton. Bot. Mar., 24 (3): 25–134.CrossRefGoogle Scholar
  29. Liu J S, van Rijssel M, Yang W D, Peng X C, Lu S H, Wang Y, Chen J F, Wang Z H, Qi Y Z. 2010. Negative effects of Phaeocystis globosa on microalgae. Chinese Journal of Oceanology and Limnology, 28 (4): 11–916.Google Scholar
  30. Matsubara T, Nagasoe S, Yamasaki Y, Shikata T, Shimasaki Y, Oshima Y, Honjo T. 2007. effects of temperature, salinity, and irradiance on the growth of the dinoflagellate Akashiwo sanguinea. Journal of Experimental Marine Biology and Ecology, 342 (2): 26–230.CrossRefGoogle Scholar
  31. Medlin L K, Lange M, Baumann M E M. 1994. Genetic differentiation among three colony-forming species of Phaeocystis: further evidence for the phylogeny of the Prymnesiophyta. Phycologia, 33 (3): 99–212.CrossRefGoogle Scholar
  32. Nagasoe S, Kim D I, Shimasaki Y, Oshima Y, Yamaguchi M, Honjo T. 2006. Effects of temperature, salinity and irradiance on the growth of the red tide dinoflagellate Gyrodinium instriatum Freudenthal et Lee. Harmful Algae, 5 (1): 0–25.CrossRefGoogle Scholar
  33. Nixon S W. 1995. Coastal marine eutrophication: a definition, social causes, and future concerns. Ophelia, 41 (1): 99–219.CrossRefGoogle Scholar
  34. Paerl H W. 1997. Coastal eutrophication and harmful algal blooms: importance of atmospheric deposition and groundwater as ‘new’ nitrogen and other nutrient sources. Limnology and Oceanography, 42 (5 Part 2): 1154–1165.CrossRefGoogle Scholar
  35. Palmisano A C, Sullivan C W. 1985. Pathways of photosynthetic carbon assimilation in sea-ice microalgae from McMurdo Sound, Antarctica. Limnology and Oceanography, 30 (3): 74–678.CrossRefGoogle Scholar
  36. Qi Y Z, Chen J F, Wang Z H, Xu N, Wang Y, Shen P P, Lu S H, Hodgkiss I J. 2004. Some observations on harmful algal bloom (HAB) events along the coast of Guangdong, southern China in 1998. Hydrobiologia, 512 (1-3): 209–214.CrossRefGoogle Scholar
  37. Riegman R, Van Boekel W. 1996. The ecophysiology of Phaeocystis globosa: a review. Journal of Sea Research, 35 (4): 35–242.CrossRefGoogle Scholar
  38. Schoemann V, Becquevort S, Stefels J, Rousseau V, Lancelot C. 2005. Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J. Sea Res., 53 (1): 3–66.Google Scholar
  39. Shen P P, Wang Y, Qi Y Z, Xie L C, Lü S H, Hodgkiss I J. 2000. Growth characteristics and life cycle of Phaeocystis globosa Scherffel. Acta Hydrobiologica Sinica, 24 (6): 35–643. (in Chinese with English abstract)Google Scholar
  40. SooHoo J B, Palmisano A C, Kottmeier S T, Lizotte M P, SooHoo S L, Sullivan C W. 1987. Spectral light absorption and quantum yield of photosynthesis in sea ice microalgae and a bloom of Phaeocystis pouchetii from McMurdo Sound, Antarctica. Mar. Ecol. Prog. Ser., 39: 75–189.CrossRefGoogle Scholar
  41. Sunda W G, Graneli E, Gobler C J. 2006. Positive feedback and the development and persistence of ecosystem disruptive algal blooms. Journal of P hycology, 42 (5): 63–974.Google Scholar
  42. Wang N, Chen Y Q, Qu L H, Li T H, Qi Y Z. 2000. Analysis of 18S rDNA gene from a “red tide” related Phaeocystis species in South China Sea. Acta Scientiarum Naturalium Universitatis Sunyatseni, 39 (1): 27–128. (in Chinese with English abstract)Google Scholar
  43. Wang Y, Qi Y Z, Li S S. 2007. Nutritional requirements for the growth of Phaeocystis globosa Scherffel. Acta Hydrobiologica Sinica, 31 (1): 4–29. (in Chinese with English abstract)Google Scholar
  44. Xu N, Duan S S, Li A F, Zhang C W, Cai Z P, Hu Z X. 2010. effects of temperature, salinity and irradiance on the growth of the harmful dinoflagellate Prorocentrum donghaiense Lu. Harmful A lgae, 9 (1): 3–17.Google Scholar
  45. Xu N, Qi Y Z, Chen J F, Huang W J, Lu S H, Wang Y. 2003. Analysis on the cause of Phaeocystis globosa Scherffel red tide. Acta Scientiae Circumstantiae, 23 (1): 13–118. (in Chinese with English abstract)Google Scholar
  46. Yamaguchi M, Honjo T. 1989. effects of temperature, salinity and irradiance on the growth of the noxious red tide flagellate Gymnodinium nagasakiense (Dinophyceae). Nippon Suisan Gakkaishi, 55 (11): 029–2036. (in Japanese with English abstract)CrossRefGoogle Scholar
  47. Yamaguchi M, Imai I, Honjo T. 1991. Effects of temperature, salinity and irradiance on the growth rates of the noxious red tide flagellates Chattonella antiqu a and C. marina (Rhaphidophyceae). Nippon Suisan Gakkaishi, 57 (7): 277–1284. (in Japanese with English abstract)CrossRefGoogle Scholar
  48. Yamaguchi M, Shigeru I, Nagasaki K, Matsuyama Y, Uchida T, Imai I. 1997. effects of temperature and salinity on the growth of the red tide flagellates Heterocapsa circularisquama (Dinophyceae) and Chattonella verruculosa (Raphidophyceae). J. Plankton Res., 19 (8): 167–1174.CrossRefGoogle Scholar
  49. Yamamoto T, Tarutani K. 1997. effect of temperature, salinity and irradiance on the growth of toxic dinoflagellate Alexandrium tamarense isolated from Hiroshima Bay, Japan. Jpn. J. Phycol. (Sorui), 45: 5–101. (in Japanese with English abstract)Google Scholar
  50. Zhou M J, Yan T, Zou J Z. 2003. Preliminary analysis of the characteristics of red tide areas in Changjiang River estuary and its adjacent sea. Chinese Journal of Applied Ecology, 14 (7): 031–1038. (in Chinese with English abstract)Google Scholar

Copyright information

© Chinese Society for Oceanology and Limnology, Science Press and Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  • Ning Xu (徐宁)
    • 1
  • Bozhu Huang (黄博珠)
    • 1
  • Zhangxi Hu (胡章喜)
    • 2
  • Yingzhong Tang (唐赢中)
    • 2
  • Shunshan Duan (段舜山)
    • 1
  • Chengwu Zhang (张成武)
    • 1
  1. 1.Institute of HydrobiologyJinan UniversityGuangzhouChina
  2. 2.Key Laboratory of Ecology and Environmental Sciences, Institute of OceanologyChinese Academy of SciencesQingdaoChina

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