Abstract
In order to study the complex effects of photoperiod, temperature, and light intensity on the spore maturation and release number of Ulva prolifera, we cultured thalli segment (2–3 mm) under three different photoperiods (L:D = 12:12, 14:10 and 10:14), temperature (15°C (LT), 25°C (MT) and 30°C (HT)) and light intensity (100, 200 and 400 µmol m−2 s−1, noted as LL, ML and HL, respectively) conditions. Then the maturation time, spore release number and chlorophyll fluorescence were analyzed. The results suggested that: 1) The spore maturation time was accelerated by higher temperature or higher light intensity from 62 h to 36 h, and changes in day length accelerated the spore maturation to a certain extent as compared with 12:12 light/dark cycle; 2) Higher light intensity significantly decreased the chlorophyll fluorescence (Fv′/Fm′, NPQ, rETRmax and a) of the mature reproductive segment under 30°C with 12:12 light/dark cycle. But when in the other photoperiods (10:14 and 14:10 conditions), the inhibitory effects of high light intensity were alleviated significantly; 3) The optimum condition for the spore maturation and release was 12:12 light/dark cycle, 25°C, 400 µmol m−2 s−1, with both shorter and longer photoperiod reducing the spore release number; 4) Higher light intensity significantly increased the spore release number under 25°C, but these effects were alleviated by 30°C treatment. This study is the first attempt to elucidate the coincidence effects of photoperiod, temperature and light intensity on the reproduction of Ulva, which would help to reveal the mechanism of the rapid proliferation of green tide.
Similar content being viewed by others
References
Baerenfaller, K., Massonnet, C., Hennig, L., Russenberger, D., Sulpice, R., Walsh, S., et al., 2015. A long photoperiod relaxes energy management in Arabidopsis leaf six. Current Plant Biology, 2: 34–45.
Castelar, B., Reis, R. P., and dos Santos Calheiros, A. C., 2014. Ulva lactuca and U. flexuosa (Chlorophyta, Ulvophyceae) cultivation in Brazilian tropical waters: Recruitment, growth, and ulvan yield. Journal of Applied Phycology, 26: 1989–1999.
Cui, J. J., Shi, J. T., Zhang, J., Wang, L. T., Fan, S. Y., Xu, Z. Y., et al., 2018. Rapid expansion of Ulva blooms in the Yellow Sea, China through sexual reproduction and vegetative growth. Marine Pollution Bulletin, 130: 223–228.
Cui, J. J., Zhang, J. H., Huo, Y. Z., Zhou, L., Wu, Q., Chen, L., et al., 2015. Adaptability of free-floating green tide algae in the Yellow Sea to variable temperature and light intensity. Marine Pollution Bulletin, 101: 660–666.
Dan, A., Hiraoka, M., Ohno, M., and Critchley, A. T., 2002. Observations on the effect of salinity and photon fluence rate on the induction of sporulation and rhizoid formation in the green alga Enteromorpha prolifera (Muller) J. Agardh (Chlorophyta, Ulvales). Fisheries Science, 68: 1182–1188.
Drop, B., Yadav, K. N. S., Boekema, E. J., and Croce, R., 2014. Consequences of state transitions on the structural and functional organization of Photosystem I in the green alga Chlamydomonas reinhardtii. Plant Journal, 78: 181–191.
Eilers, P. H. C., and Peeters, J. C. H., 1988. A model for the relationship between light intensity and the rate of photosynthesis in phytoplankton. Ecological Modelling, 42: 199–215.
Forbord, S., Skjermo, J., Arff, J., Handå, A., Reitan, K. I., Bjerregaard, R., et al., 2012. Development of Saccharina latissima (Phaeophyceae) kelp hatcheries with year-round production of zoospores and juvenile sporophytes on culture ropes for kelp aquaculture. Journal of Applied Phycology, 24: 393–399.
Fu, M. L., Cao, S. C., Li, J. S., Zhao, S., Liu, J. L., Zhuang, M. M., et al., 2022. Controlling the main source of green tides in the Yellow Sea through the method of biological competition. Marine Pollution Bulletin, 177: 113561.
Gao, G., Clare, A. S., Rose, C., and Caldwell, G. S., 2017. Intrinsic and extrinsic control of reproduction in the green tide-forming alga, Ulva rigida. Environmental and Experimental Botany, 139: 14–22.
Gao, G., Clare, A. S., Rose, C., and Caldwell, G. S., 2018. Ulva rigida in the future ocean: Potential for carbon capture, bioremediation, and biomethane production. Global Change Biology Bioenergy, 10: 39–51.
Gao, G., Zhong, Z. H., Zhou, X. H., and Xu, J. T., 2016. Changes in morphological plasticity of Ulva prolifera under different environmental conditions: A laboratory experiment. Harmful Algae, 59: 51–58.
Gao, S., Chen, X. Y., Yi, Q. Q., Wang, G. C., Pan, G. H., Lin, A. P., 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: e8571.
Guillard, R. R., and Ryther, J. H., 1962. Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt, and Detonula confervacea (cleve) Gran. Canadian Journal of Microbiology, 8: 229–239.
Haeder, D. P., Richter, P. R., Villafane, V. E., and Walter Helbling, E., 2014. Influence of light history on the photo-synthetic and motility responses of Gymnodinium chlorophorum exposed to UVR and different temperatures. Journal of Photochemistry and Photobiology B-Biology, 138: 273–281.
Han, H. B., Wei, Z. L., Hou, Y. Z., Cheng, Q. F., Zhang, J. H., He, P. M., et al., 2015. Effect of temperature and light intensity on the release and germination of Ulva prolifera spores/gametes. Marine Fisheries, 31: 517–524 (in Chinese with English abstract).
Han, T., and Choi, G. W. 2005, A novel marine algal toxicity bioassay based on sporulation inhibition in the green macroalga Ulva pertusa (Chlorophyta). Aquatic Toxicology, 75: 202–212.
Han, T., Han, Y. S., Park, C. Y., Jun, Y. S., Kwon, M. J., Kang, S. H., et al., 2008. Spore release by the green alga Ulva: a quantitative assay to evaluate aquatic toxicants. Environmental Pollution, 153: 699–705.
He, Y. L., Wang, Y., Hu, C. Y., Sun, X., Li, Y. H., and Xu, N. J., 2019. Dynamic metabolic profiles of the marine macroalga Ulva prolifera during fragmentation-induced proliferation. PLoS One, 14: e0214491.
Heinrich, S., Valentin, K., Frickenhaus, S., John, U., and Wiencke, C., 2012. Transcriptomic analysis of acclimation to temperature and light stress in Saccharina latissima (Phaeophyceae). PLoS One, 1 (8): e44342.
Hiraoka, M., and Enomoto, S., 1998. The induction of reproductive cell formation of Ulva pertusa Kjellman (Ulvales, Ulvophyceae). Phycological Research, 46: 199–203.
Hiraoka, M., and Shimada, S., 2004. Biology of a special green laver, Ulva prolifera from the Shimanto River. Aquabiology, 26: 508–515.
Huo, Y. Z., Hua, L., Wu, H. L., Zhang, J. H., Cui, J. J,, Huang, X. W., et al., 2014. Abundance and distribution of Ulva microscopic propagules associated with a green tide in the southern coast of the Yellow Sea. Harmful Algae, 39: 357–364.
Jiang, J. N., Li, Y. H., Hu, C. Y., Zhu, W. R., and Xu, N. J., 2022. Transcriptomic analysis reveals the regulation mechanism of sporogenesis in Ulva prolifera. Frontiers in Marine Science, 9: 802006.
Jiang, J. N., Yu, Y. Y., Zheng, M. S., Liu, N. N., Li, Y. H., and Xu, N. J., 2020a. High light might alleviate inhibitory effects of high temperature on growth and physiological parameters of Ulva prolifera. Aquaculture Research, 51: 2062–2070.
Jiang, M., Gao, L., Huang, R., Lin, X., and Gao, G., 2020b. Differential responses of bloom-forming Ulva intestinalis and economically important Gracilariopsis lemaneiformis to marine heatwaves under changing nitrate conditions. Science of the Total Environment, 840: 156591.
Kalita, T. L., and Titlyanov, E. A., 2011. The effect of temperature on infradian rhythms of reproduction in Ulva fenestrata Postels et Ruprecht, 1840 (Chlorophyta: Ulvales). Russian Journal of Marine Biology, 31: 52–61.
Li, Y. H., Zhong, J. L., Zheng, M. S., Zhuo, P. L., and Xu, N. J., 2018. Photoperiod mediates the effects of elevated CO2 on the growth and physiological performance in the green tide alga Ulva prolifera. Marine Environmental Research, 141: 24–29.
Lin, A. P., Shen, S. D., Wang, G., Yi, Q., Qiao, H., Niu, J., et al., 2011. Comparison of chlorophyll and photosynthesis parameters of floating and attached Ulva prolifera. Journal of Integrative Plant Biology, 53: 25–34.
Lin, A. P., Shen, S. D., Wang, J. W., and Yan, B. L., 2008. Reproduction diversity of Enteromorpha prolifera. Journal of Integrative Plant Biology, 50: 622–629.
Liu, Y., Xu, J. T., and Gao, K. S., 2012. CO2-driven seawater acidification increases photochemical stress in a green alga. Phycologia, 51: 562–566.
Lüning, K., 1988. Photoperiodic control of sorus formation in the brown alga Laminaria saccharina. Marine Ecology Progress Series, 45: 137–144.
Lüning, K., Kadel, P., and Pang, S., 2008. Control of reproduction rhythmicity by environmental and endogenous signals in Ulva pseudocurvata (Chlorophyta) 1. Journal of Phycology, 44: 866–873.
Nordby, Ø., 1974. Light microscopy of meiotic zoosporogenesis and mitotic gametogenesis in Ulva mutabilis Foyn. Journal of Cell Science, 15: 443–455.
Smith, G. M., 1947. On the reproduction of some Pacific coast species of Ulva. American Journal of Botany, 34: 80–87.
Sousa, A. I., Martins, I., Lillebø, A. I., Flindt, M. R., and Pardal, M. A., 2007. Influence of salinity, nutrients and light on the germination and growth of Enteromorpha sp. spores. Journal of Experimental Marine Biology and Ecology, 341: 142–150.
Sun, Y. Q., Liu, J. L., Xia, J., Tong, Y. C., Li, C. X., Zhao, S., et al., 2022a. Research development on resource utilization of green tide algae from the southern Yellow Sea. Energy Reports, 8 (Supplement 4): 295–303.
Sun, Y. Q., Yao, L. L., Liu, J. L., Tong, Y. C., Xia, J., Zhao, X. H., et al., 2022b. Prevention strategies for green tides at source in the southern Yellow Sea. Marine Pollution Bulletin, 178: 113646.
Wang, H., Lin, A. P., Gu, W. H., Huan, L., Gao, S., and Wang, G. C., 2016. The sporulation of the green alga Ulva prolifera is controlled by changes in photosynthetic electron transport chain. Scientific Reports, 6: 24923.
Wang, S. Y., Huo, Y., Zhang, J. H., Cui, J. J., Wang, Y., Yang, L. L., et al., 2018. Variations of dominant free-floating Ulva species in the source area for the world’s largest macroalgal blooms, China: Differences of ecological tolerance. Harmful Algae, 74: 58–66.
Wang, Y., Wang, Y., Zhu, L., Zhou, B., and Tang, X. X., 2012. Comparative studies on the ecophysiological differences of two green tide macroalgae under controlled laboratory conditions. PLoS One, 7 (8): e38245.
Wichard, T., and Oertel, W., 2010. Gametogenesis and gamete release of Ulva mutabilis and Ulva lactuca (Chlorophyta): Regulatory effects and chemical characterization of the ‘swarming inhibitor’. Journal of Phycology, 46: 248–259.
Xia, Z. Y., Yuan, H. Q., Liu, J. L., Sun, Y. Q., Tong, Y. C., Zhao, S., et al., 2022. A review of physical, chemical, and biological green tide prevention methods in the southern Yellow Sea. Marine Pollution Bulletin, 180: 113772.
Xu, Z. G., Wu, H., Zhan, D., Sun, F., Sun, J., and Wang, G., 2014. Combined effects of light intensity and NH4+-enrichment on growth, pigmentation, and photosynthetic performance of Ulva prolifera (Chlorophyta). Chinese Journal of Oceanology and Limnology, 32: 1016–1023.
Zhao, J., Peng, J., Liu, Z. Y., Wei, W., Lin, H. Z., Li, F. C., et al., 2013. The Yellow Sea green tides were dominated by one species, Ulva (Enteromorpha) prolifera, from 2007 to 2011. Chinese Science Bulletin, 58: 2298–2302.
Zhao, X., Cui, J. J., Zhang, J. H., Shi, J. T., Kang, X. Y., Liu, J. L., et al., 2019. Reproductive strategy of the floating alga Ulva prolifera in blooms in the Yellow Sea based on a combination of zoid and chromosome analysis. Marine Pollution Bulletin, 146: 584–590.
Zhao, X. Y., Tang, X. X., Zhang, H. X., Qu, T. F., and Wang, Y., 2016. Photosynthetic adaptation strategy of Ulva prolifera floating on the sea surface to environmental changes. Plant Physiology and Biochemistry, 107: 116–125.
Acknowledgements
This study was supported by the Natural Science Foundation of Zhejiang Province (No. LY23D060003), the Key Program of Science and Technology Innovation in Ningbo (2021Z114, 2023Z118), and was also sponsored by K. C. Wong Magna Fund in Ningbo University.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Jiang, J., Yu, Y., Chen, Y. et al. Photoperiod Mediates the Effects of Temperature and Light Intensity on the Proliferation of Ulva prolifera. J. Ocean Univ. China 23, 255–263 (2024). https://doi.org/10.1007/s11802-024-5473-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11802-024-5473-8