Skip to main content
Log in

Effect of temperature, salinity and irradiance on growth and photosynthesis of Ulva prolifera

  • Published:
Acta Oceanologica Sinica Aims and scope Submit manuscript

Abstract

Intensive Pyropia aquaculture in the coast of southwestern Yellow Sea and its subsequent waste, including disposed Ulva prolifera, was speculated to be one of the major sources for the large-scale green tide proceeding in the Yellow Sea since 2007. It was, however, unclear how the detached U. prolifera responded and resumed growing after they detached from its original habitat. In this study, we investigated the growth and photosynthetic response of the detached U. prolifera to various temperature, salinity and irradiance in the laboratory. The photosynthetic rate of the detached U. prolifera was significantly higher at moderate temperature levels (14–27°C) and high salinity (26–32), with optimum at 23°C and 32. Both low (<14°C) and highest temperature (40°C), as well as low salinity (8) had adverse effects on the photosynthesis. Compared with the other Ulva species, U. prolifera showed higher saturated irradiance and no significant photoinhibition at high irradiance, indicating the great tolerance of U. prolifera to the high irradiance. The dense branch and complex structure of floating mats could help protect the thalli and reduce photoinhibition in field. Furthermore, temperature exerted a stronger influence on the growth rate of the detached U. prolifera compared to salinity. Overall, the high growth rate of this detached U. prolifera (10.6%–16.7% d–1) at a wide range of temperature (5–32°C) and salinity (14–32) implied its blooming tendency with fluctuated salinity and temperature during floating. The environmental parameters in the southwestern Yellow Sea at the beginning of green tide were coincident with the optimal conditions for the detached U. prolifera.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Ale M T, Mikkelsen J D, Meyer A S. 2011. Differential growth response of Ulva lactuca to ammonium and nitrate assimilation. J Appl Phycol, 23(3): 345–351

    Article  Google Scholar 

  • Arnold K E, Murray S N. 1980. Relationships between irradiance and photosynthesis for marine benthic green algae (Chlorophyta) of differing morphologies. J Exp Mar Bio Ecol, 43(2): 183–192

    Article  Google Scholar 

  • Baly E C C. 1935. The kinetics of photosynthesis. Proc Roy Soc B Biol Sci, 117(804): 218–239

    Article  Google Scholar 

  • Binzer T, Middelboe A L. 2005. From thallus to communities: scale effects and photosynthetic performance in macroalgae communities. Mar Ecol Prog Ser, 287: 65–75

    Article  Google Scholar 

  • Bold H C, Wynne M J. 1978. Introduction to the Algae: Structure and Reproduction. New Jersey: Prentice Hall limited Company, 77–130

    Google Scholar 

  • Brinkhuis B H. 1985. Growth patterns and rates. In: Littler M M, Littler D S, eds. Handbook of Phycological Methods, Ecological Field Methods: Macroalgae. Cambridge: Cambridge University Press, 461–477

    Google Scholar 

  • Choi T S, Kang E J, Kim J H, et al. 2010. Effect of salinity on growth and nutrient uptake of Ulva pertusa (Chlorophyta) from an eelgrass bed. Algae, 25(1): 17–26

    Article  Google Scholar 

  • de Paula Silva P H, McBride S, de Nys R, et al. 2008. Integrating filamentous ‘green tide’ algae into tropical pond-based aquaculture. Aquaculture, 284(1–4): 74–80

    Article  Google Scholar 

  • Ding Lanping, Luan Rixiao. 2009. The taxonomy, habit, and distribution of a green alga Enteromorpha prolifera (Ulvales, Chlorophyta). Oceanol Limnol Sin (in Chinese), 40(1): 68–71

    Google Scholar 

  • Fan Shiliang, Fu Mingzhu, Wang Zongling, et al. 2015. Temporal variation of green macroalgal assemblage on Porphyra aquaculture rafts in the Subei Shoal, China. Estuar Coast Shelf Sci, 163: 23–28

    Article  Google Scholar 

  • Fong P, Boyer K E, Desmond J S, et al. 1996. Salinity stress, nitrogen competition, and facilitation: what controls seasonal succession of two opportunistic green macroalgae?. J Exp Mar Bio Ecol, 206(1–2): 203–221

    Article  Google Scholar 

  • Fu Gang, Yao Jianting, Liu Fuli, et al. 2008. Effect of temperature and irradiance on the growth and reproduction of Enteromorpha prolifera J. Ag. (Chlorophycophyta, Chlorophyceae). Chin J Oceanol Limnol, 26(4): 357–362

    Article  Google Scholar 

  • Gao Shan, Chen Xiaoyuan, Yi Qianqian, et al. 2010. A strategy for the proliferation of Ulva prolifera, main causative species of green tides, with formation of sporangia by fragmentation. PLoS One, 5(1): e8571

    Article  Google Scholar 

  • Gao Bingbing, Zheng Chunfang, Xu Juntian, et al. 2012. Physiological responses of Enteromorpha linza and Enteromorpha prolifera to seawater salinity stress. Chin J Appl Ecol (in Chinese), 23(7): 1913–1920

    Google Scholar 

  • Hayden H S, Blomster J, Maggs C A, et al. 2003. Linnaeus was right all along: Ulva and Enteromorpha are not distinct genera. Eur J Phycol, 38(3): 277–294

    Article  Google Scholar 

  • Hayden H S, Waaland J R. 2002. Phylogenetic systematics of the Ulvaceae (Ulvales, Ulvophyceae) using chloroplast and nuclear DNA sequences. J Phycol, 38(6): 1200–1212

    Article  Google Scholar 

  • Hiraoka M, Oka N. 2008. Tank cultivation of Ulva prolifera in deep seawater using a new “germling cluster” method. J Appl Phycol, 20(1): 97–102

    Article  Google Scholar 

  • Hiraoka M, Ichihara K, Zhu Wenrong, et al. 2011. Culture and hybridization experiments on an Ulva clade including the Qingdao strain blooming in the Yellow Sea. PLoS One, 6(5): e19371

    Article  Google Scholar 

  • Hu Chuanmin, Li Daqiu, Chen Changsheng, et al. 2010. On the recurrent Ulva prolifera blooms in the Yellow Sea and East China Sea. J Geophys Res, 115(C5): C05017

    Article  Google Scholar 

  • Huo Yuanzi, Zhang Jianheng, Chen Liping, et al. 2013. Green algae blooms caused by Ulva prolifera in the southern Yellow Sea: identification of the original bloom location and evaluation of biological processes occurring during the early northward floating period. Limnol Oceanogr, 58(6): 2206–2218

    Article  Google Scholar 

  • Kang E J, Kim J H, Kim K, et al. 2014. Re-evaluation of green tideforming species in the Yellow Sea. Algae, 29(4): 267–277

    Article  Google Scholar 

  • Keesing J K, Liu Dongyan, Fearns P, et al. 2011. Inter-and intra-annual patterns of Ulva prolifera green tides in the Yellow Sea during 2007–2009, their origin and relationship to the expansion of coastal seaweed aquaculture in China. Mar Pollut Bull, 62(6): 1169–1182

    Article  Google Scholar 

  • Kim J H, Kang E J, Park M G, et al. 2011. Effects of temperature and irradiance on photosynthesis and growth of a green-tide-forming species (Ulva linza) in the Yellow Sea. J Appl Phycol, 23(3): 421–432

    Article  Google Scholar 

  • Leliaert F, Zhang Xiaowen, Ye Naihao, et al. 2009. Identity of the Qingdao algal bloom. Phycol Res, 57(2): 147–151

    Article  Google Scholar 

  • Li Ruixiang, Wu Xiaowen, Wei Qinsheng, et al. 2009. Growth of Enteromorpha prolifera under different uutrient conditions. Adv Marine Sci (in Chinese), 27(2): 211–216

    Google Scholar 

  • Lin Apeng, Shen Songdong, Wang Jianwei, et al. 2008. Reproduction diversity of Enteromorpha prolifera. J Integr Plant Biol, 50(5): 622–629

    Article  Google Scholar 

  • Lin Apeng, Shen Songdong, Wang Guangce, et al. 2011. Comparison of chlorophyll and photosynthesis parameters of floating and attached Ulva prolifera. J Integr Plant Biol, 53(1): 25–34

    Article  Google Scholar 

  • Lin Apeng, Wang Chao, Qiao Hongjin, et al. 2009. Study on the photosynthetic performances of Enteromorpha prolifera collected from the surface and bottom of the sea of Qingdao sea area. Chin Sci Bull, 54(3): 399–404

    Google Scholar 

  • Liu Jingwen, Dong Shuanglin. 2001. Nutrient metabolism and the major nutrient uptake kinetics of seaweeds. Plant Physiol Commun (in Chinese), 37(4): 325–330

    Google Scholar 

  • Liu Dongyan, Keesing J K, Dong Zhijun, et al. 2010a. Recurrence of the world’s largest green-tide in 2009 in Yellow Sea, China: Porphyra yezoensis aquaculture rafts confirmed as nursery for macroalgal blooms. Mar Pollut Bull, 60(9): 1423–1432

    Article  Google Scholar 

  • Liu Dongyan, Keesing J K, He Peimin, et al. 2013a. The world’s largest macroalgal bloom in the Yellow Sea, China: formation and implications. Estuar Coast Shelf Sci, 129: 2–10

    Article  Google Scholar 

  • Liu Feng, Pang Shaojun, Chopin T, et al. 2010b. The dominant Ulva strain of the 2008 green algal bloom in the Yellow Sea was not detected in the coastal waters of Qingdao in the following winter. J Appl Phycol, 22(5): 531–540

    Article  Google Scholar 

  • Liu Feng, Pang Shaojun, Chopin T, et al. 2013b. Understanding the recurrent large-scale green tide in the Yellow Sea: temporal and spatial correlations between multiple geographical, aquacultural and biological factors. Mar Environ Res, 83: 38–47

    Article  Google Scholar 

  • Liu Feng, Pang Shaojun, Xu Na, et al. 2010c. Ulva diversity in the Yellow Sea during the large-scale green algal blooms in 2008–2009. Phycol Res, 58(4): 270–279

    Article  Google Scholar 

  • Liu Feng, Pang Shaojun, Zhao Xiaobo, et al. 2012. Quantitative, molecular and growth analyses of Ulva microscopic propagules in the coastal sediment of Jiangsu province where green tides initially occurred. Mar Environ Res, 74: 56–63

    Article  Google Scholar 

  • Lüning K, Kadel P, Pang Shaojun. 2008. Control of reproduction rhythmicity by environmental and endogenous signals in Ulva pseudocurvata (Chlorophyta). J Phycol, 44(4): 866–873

    Article  Google Scholar 

  • Luo Minbo, Liu Feng. 2011. Salinity-induced oxidative stress and regulation of antioxidant defense system in the marine macroalga Ulva prolifera. J Exp Mar Bio Ecol, 409(1–2): 223–228

    Article  Google Scholar 

  • Luo Minbo, Liu Feng, Xu Zhaoli. 2012. Growth and nutrient uptake capacity of two co-occurring species, Ulva prolifera and Ulva linza. Aquat Bot, 100: 18–24

    Article  Google Scholar 

  • Nielsen S L, Sand-Jensen K. 1990. Allometric settling of maximal photosynthetic growth rate to surface/volume ratio. Limnol Oceanogr, 35(1): 177–180

    Article  Google Scholar 

  • O’Brien M C, Wheeler P A. 1987. Short term uptake of nutrients by Enteromorpha prolifera (Chlorophyceae). J Phycol, 23(4): 547–556

    Article  Google Scholar 

  • Shi Xiaoyong, Qi Mingyan, Tang Hongjie, et al. 2015. Spatial and temporal nutrient variations in the Yellow Sea and their effects on Ulva prolifera blooms. Estuar Coast Shelf Sci, 163: 36–43

    Article  Google Scholar 

  • Sutherland J E, Lindstrom S C, Nelson W A, et al. 2011. A new look at an ancient order: generic revision of the Bangiales (Rhodophyta). J Phycol, 47(5): 1131–1151

    Article  Google Scholar 

  • Tan I H, Blomster J, Hansen G, et al. 1999. Molecular phylogenetic evidence for a reversible morphogenetic switch controlling the gross morphology of two common genera of green seaweeds, Ulva and Enteromorpha. Mol Biol Evol, 16(8): 1011–1018

    Article  Google Scholar 

  • Taylor R, Fletcher R L, 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. Bot Mar, 44: 327–336

    Article  Google Scholar 

  • Wang Yangyang, Huo Yuanzi, Cao Jiachun, et al. 2010. Influence of low temperature and low light intensity on growth of Ulva compressa. Journal of Fishery Sciences of China (in Chinese), 17(3): 593–599

    Google Scholar 

  • Wang Ying, Wang You, Zhu Lin, et al. 2012. Comparative studies on the ecophysiological differences of two green tide macroalgae under controlled laboratory conditions. PLoS One, 7(8): e38245

    Article  Google Scholar 

  • Wang Zongling, Xiao Jie, Fan Shiliang, et al. 2015. Who made the world’s largest green tide in China?—an integrated study on the initiation and early development of the green tide in Yellow Sea. Limnol Oceanogr, 60(4): 1105–1117

    Article  Google Scholar 

  • Wu Hongxi, Xu Aiguang, Wu Meining. 2000. Preliminary study on experimental ecology of Enteromorpha prolifera (Miill.). J Zhejiang Ocean Univer (Nat Sci) (in Chinese), 19(3): 230–234

    Google Scholar 

  • Wang Jianwei, Yan Binlun, Lin Apeng, et al. 2007. Ecological factor research on the growth and induction of spores release in Enteromorpha prolifera (Chlorophyta). Marine Science Bulletin (in Chinese), 26(2): 60–65

    Google Scholar 

  • Wu Xiaowen, Li Ruixiang, Xu Zongjun, et al. 2010. Mesocosm experiments of nutrient effects on Enteromorpha prolifera growth. Adv Mar Sci, (in Chinese), 28(4): 538–544

    Google Scholar 

  • Xiao Jie, Li Yan, Song Wei, et al. 2013. Discrimination of the common macroalgae (Ulva and Blidingia) in coastal waters of Yellow Sea, northern China, based on restriction fragment-length polymorphism (RFLP) analysis. Harmful Algae, 27: 130–137

    Article  Google Scholar 

  • Xin Dinghao, Ren Song, He Peimin, et al. 2009. Preliminary study on experimental ecology of Enteromorpha in Yellow Sea. Mar Environ Sci (in Chinese), 28(2): 190–192

    Google Scholar 

  • Ye Naihao, Zhang Xiaowen, Mao Yuze, et al. 2011. ‘Green tides’ are overwhelming the coastline of our blue planet: taking the world’s largest example. Ecol Res, 26(3): 477–485

    Article  Google Scholar 

  • Zhang Jianheng, Huo Yuanzi, Yu Kefeng, et al. 2013. Growth characteristics and reproductive capability of green tide algae in Rudong coast, China. J Appl Phycol, 25(3): 795–803

    Article  Google Scholar 

  • Zhang Xiaohong, Wang Zongling, Li Ruixiang, et al. 2012. Microscopic observation on population growth and reproduction of Entromorphra prolifera under different temperature and salinity. Adv Mar Sci (in Chinese), 30(2): 276–283

    Google Scholar 

  • Zhang Xiaowen, Xu Dong, Mao Yuze, et al. 2011. Settlement of vegetative fragments of Ulva prolifera confirmed as an important seed source for succession of a large-scale green tide bloom. Limnol Oceanogr, 56(1): 233–242

    Article  Google Scholar 

  • Zhao Jin, Jiang Peng, Liu Zhengyi, et al. 2011. Genetic variation of Ulva (Enteromorpha) prolifera (Ulvales, Chlorophyta)–the causative species of the green tides in the Yellow Sea, China. J Appl Phycol, 23(2): 227–233

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Chunlei Gao.

Additional information

Foundation item: The Special Funds for Basic Ocean Science Research of FIO under contract Nos 2012T08, 2014G33 and 2008T30; the National Natural Science Foundation of China—Shandong Joint Funded Project “Marine Ecology and Environmental Sciences” under contract No. U1406403; the National Natural Science Foundation of China under contract Nos 41206162 and 41206161; the National Basic Research Program (973 Program) of China under contract No. 2010CB428703.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xiao, J., Zhang, X., Gao, C. et al. Effect of temperature, salinity and irradiance on growth and photosynthesis of Ulva prolifera . Acta Oceanol. Sin. 35, 114–121 (2016). https://doi.org/10.1007/s13131-016-0891-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13131-016-0891-0

Key words

Navigation