Effects of phosphorus availability on macroalgae: A review





Green tides, Macroalgae, Phosphorous, Phosphate, Seaweeds


Phosphorous is considered as an essential nutrient for life. Its availability in the water dictates the primary productivity, including macroalgae. In this paper, peer-reviewed articles reporting the effects of phosphorous on macroalgae for the past decades and up to the present were reviewed and recapitulated. The literature revealed that while phosphorous is one of the limiting nutrients in an open ocean, eutrophication in some coastal areas, which is fueled by anthropogenic activities, contributes to the excess phosphorous resulting in the occurrence of green tides. The general influences of phosphorous availability to many macroalgae were enhanced growth and biomass, especially with the interaction effect with nitrogen. However, some studies reported that the high concentration of phosphorous has deleterious effects on macroalgae. Hence, future studies are needed to fully understand the role of phosphorous availability in macroalgae.


Abou-Aisha, K. M., Kobbia, I. A., El Abyad, M. S., Shabana, E., & Schanz, F. (1995). Impact of Phosphorus Loadings on Macro-algal Communities in the Red Sea Coast of Egypt. Water, Air, and Soil Pollution, 83(3), 285-297.

Andersen, J. H., & Conley, D. J. (2009). Eutrophication in coastal marine ecosystems: towards better understanding and management strategies. In J. H. Andersen, & D. J. Conley (Eds.), Eutrophication in Coastal Ecosystems (pp. 1-4). Springer.

Andersen, J. H., Schlüter, L., & Ærtebjerg, G. (2006). Coastal Eutrophication: Recent Developments in Definitions and Implications for Monitoring Strategies. Journal of Plankton Research, 28(7), 621-628. https://doi.org/10.1093/plankt/fbl001

Carpenter, S. R. (2005). Eutrophication of Aquatic Ecosystems: Bistability and Soil Phosphorus. Proceedings of the National Academy of Sciences, 102(29), 10002-10005. https://doi.org/10.1073/pnas.0503959102

Charlier, R. H., Morand, P., & Finkl, C. W. (2008). How Brittany and Florida Coasts Cope with Green Tides. International Journal of Environmental Studies, 65(2), 191-208. https://doi.org/10.1080/00207230701791448

Comber, S., Gardner, M., Georges, K., Blackwood, D., & Gilmour, D. (2013). Domestic Source of Phosphorus to Sewage Treatment Works. Environmental Technology, 34(10), 1349-1358. https://doi.org/10.1080/09593330.2012.747003

Den Haan, J., Huisman, J., Brocke, H. J., Goehlich, H., Latijnhouwers, K. R., Van Heeringen, S., ... & Visser, P. M. (2016). Nitrogen and Phosphorus Uptake Rates of Different Species from a Coral Reef Community after a Nutrient Pulse. Scientific Reports, 6, 28821. https://doi.org/10.1038/srep28821

Diaz, M., Darnhofer, I., Darrot, C., & Beuret, J. E. (2013). Green tides in Brittany: What Can We Learn about Niche–regime Interactions?. Environmental Innovation and Societal Transitions, 8, 62-75. https://doi.org/10.1016/j.eist.2013.04.002

Diaz, R. J., & Rosenberg, R. (2008). Spreading Dead Zones and Consequences for Marine Ecosystems. Science, 321(5891), 926-929. https://doi.org/10.1126/science.1156401

Douglas, E. J., Haggitt, T. R., & Rees, T. A. V. (2014). Supply- and Demand-driven Phosphate Uptake and Tissue Phosphorus in Temperate Seaweeds. Aquatic Biology, 23(1), 49-60. https://doi.org/10.3354/ab00601

Duhamel, S., Diaz, J. M., Adams, J. C., Djaoudi, K., Steck, V., & Waggoner, E. M. (2021). Phosphorus as an Integral Component of Global Marine Biogeochemistry. Nature Geoscience, 14(6), 359-368. https://doi.org/10.1038/s41561-021-00755-8

Elser, J. J., Bracken, M. E., Cleland, E. E., Gruner, D. S., Harpole, W. S., Hillebrand, H., ... & Smith, J. E. (2007). Global Analysis of Nitrogen and Phosphorus Limitation of Primary Producers in Freshwater, Marine and Terrestrial Ecosystems. Ecology Letters, 10(12), 1135-1142. https://doi.org/10.1111/j.1461-0248.2007.01113.x

Farahdiba, A. U., Hidayah, E. N., Asmar, G. A., & Myint, Y. W. (2020). Growth and Removal of Nitrogen and Phosphorus by a Macroalgae Cladophora glomerata under Different Nitrate Concentrations. Nature Environment and Pollution Technology, 19(2), 809-813. https://doi.org/10.46488/NEPT.2020.v19i02.038

Fletcher, R. L. (1996). The occurrence of “green tides”-a review. In W. Schramm, & P. H. Nienhuis (Eds.), Marine Benthic Vegetation (pp. 7-43). Springer.

Gladyshev, M. I., & Gubelit, Y. I. (2019). Green Tides: Green Tides: New Consequences of the Eutrophication of Natural Waters (Invited Review). Contemporary Problems of Ecology, 12(2), 109-125. https://doi.org/10.1134/S1995425519020057

Hansen, N. C., Daniel, T. C., Sharpley, A. N., & Lemunyon, J. L. (2002). The Fate and Transport of Phosphorus in Agricultural Systems. Journal of Soil and Water Conservation, 57(6), 408-417.

Harrison, P. J., & Hurd, C. L. (2001). Nutrient Physiology of Seaweeds: Application of Concepts to Aquaculture. Cahiers de Biologie Marine, 42(1-2), 71-82.

Hernández, I., Fernandez-Engo, M., Pérez-Lloréns, J. L., & Vergara, J. J. (2005). Integrated Outdoor Culture of Two Estuarine Macroalgae as Biofilters for Dissolved Nutrients from Sparus auratus Waste Waters. Journal of Applied Phycology, 17(6), 557-567. https://doi.org/10.1007/s10811-005-9006-6

Kumari, P., Kumar, M., Reddy, C. R. K., & Jha, B. (2014). Nitrate and Phosphate Regimes Induced Lipidomic and Biochemical Changes in the Intertidal Macroalga Ulva lactuca (Ulvophyceae, Chlorophyta). Plant and Cell Physiology, 55(1), 52-63. https://doi.org/10.1093/pcp/pct156

Kwon, H. K., Kang, H., Oh, Y. H., Park, S. R., & Kim, G. (2017). Green Tide Development associated with Submarine Groundwater Discharge in a Coastal Harbor, Jeju, Korea. Scientific Reports, 7(1), 1-9. https://doi.org/10.1038/s41598-017-06711-0

Larned, S. T. (1998). Nitrogen-versus Phosphorus-limited Growth and Sources of Nutrients for Coral Reef Macroalgae. Marine Biology, 132(3), 409-421. https://doi.org/10.1007/s002270050407

Li, H., Zhang, Y., Han, X., Shi, X., Rivkin, R. B., & Legendre, L. (2016). Growth Responses of Ulva prolifera to Inorganic and Organic Nutrients: Implications for Macroalgal Blooms in the Southern Yellow Sea, China. Scientific Reports, 6(1), 1-11. https://doi.org/10.1038/srep26498

Liu, X., Wang, Z., & Zhang, X. (2016). A Review of the Green Tides in the Yellow Sea, China. Marine Environmental Research, 119, 189-196. https://doi.org/10.1016/j.marenvres.2016.06.004

Lobban, C. S., Harrison, P. J., & Duncan, M. J. (1985). Physiological ecology of seaweeds. Cambridge University Press.

Lourenco, S. O., Barbarino, E., Nascimento, A., & Paranhos, R. (2005). Seasonal Variations in Tissue Nitrogen and Phosphorus of Eight Macroalgae from a Tropical Hypersaline Coastal Environment. Cryptogamie-Algologie, 26(4), 355-372.

Lundberg, P., Weich, R. G., Jensen, P., & Vogel, H. J. (1989). Phosphorus-31 and Nitrogen-14 NMR Studies of the Uptake of Phosphorus and Nitrogen Compounds in the Marine Macroalgae Ulva lactuca. Plant Physiology, 89(4), 1380-1387. https://doi.org/10.1104/pp.89.4.1380

Menéndez, M., & Comın, F. A. (2000). Spring and Summer Proliferation of Floating Macroalgae in a Mediterranean Coastal Lagoon (Tancada Lagoon, Ebro Delta, NE Spain). Estuarine, Coastal and Shelf Science, 51(2), 215-226. https://doi.org/10.1006/ecss.2000.0637

Menéndez, M., Herrera Silveira, J. A., & Comín, F. A. (2002). Effect of Nitrogen and Phosphorus Supply on Growth, Chlorophyll Content and Tissue Composition of the Macroalga Chaetomorpha linum (OF Mull), Kutz, in a Mediterranean Coastal Lagoon. Scientia Marina, 66(4), 355-364.

Ohtake, M., Nishihara, G. N., Inoue, Y., Tsuchiya, K., & Toda, T. (2020). Phosphorus Demand and Uptake during Growth and Maturation of the Brown Alga Sargassum macrocarpum. Phycological Research, 68(4), 277-289. https://doi.org/10.1111/pre.12430

Perini, V., & Bracken, M. E. (2014). Nitrogen Availability Limits Phosphorus Uptake in an Intertidal Macroalga. Oecologia, 175(2), 667-676. https://doi.org/10.1007/s00442-014-2914-x

Rybak, A. S., & Gąbka, M. (2018). The Influence of Abiotic Factors on the Bloom-forming Alga Ulva flexuosa (Ulvaceae, Chlorophyta): Possibilities for the Control of the Green Tides in Freshwater Ecosystems. Journal of Applied Phycology, 30, 1405-1416. https://doi.org/10.1007/s10811-017-1301-5

Reinhard, C. T., Planavsky, N. J., Gill, B. C., Ozaki, K., Robbins, L. J., Lyons, T. W., ... & Konhauser, K. O. (2017). Evolution of the Global Phosphorus Cycle. Nature, 541(7637), 386-389. https://doi.org/10.1038/nature20772

Roleda, M. Y., & Hurd, C. L. (2019). Seaweed Nutrient Physiology: Application of Concepts to Aquaculture and Bioremediation. Phycologia, 58(5), 552-562. https://doi.org/10.1080/00318884.2019.1622920

Runcie, J. W., Ritchie, R. J., & Larkum, A. W. (2004). Uptake Kinetics and Assimilation of Phosphorus by Catenella nipae and Ulva lactuca Can be Used to Indicate Ambient Phosphate Availability. Journal of Applied Phycology, 16(3), 181-194. https://doi.org/10.1023/B:JAPH.0000048504.76029.b4

Sarri, J. H.., Abdulmutalib, Y. A., Mohammad Tilka, M. E., Terzi, E., & Tahiluddin, A. B. (2022). Effects of Inorganic Nutrient Enrichment on the Carrageenan Yield, Growth, and Ice-ice Disease Occurrence of Red Alga Kappaphycus striatus. Aquatic Research, 5(2), 99-109. https://doi.org/10.3153/AR22009

Schaffelke, B., & Klumpp, D. W. (1998). Nutrient-limited Growth of the Coral Reef Macroalga Sargassum baccularia and Experimental Growth Enhancement by Nutrient Addition in Continuous Flow Culture. Marine Ecology Progress Series, 164, 199-211.

Smith, V. H. (2003). Eutrophication of Freshwater and Coastal Marine Ecosystems a Global Problem. Environmental Science and Pollution Research, 10(2), 126-139. https://doi.org/10.1065/espr2002.12.142

Tahiluddin, A. B., Nuñal, S. N., & Santander–de Leon, S. M. S. (2022a). Inorganic Nutrient Enrichment of Seaweed Kappaphycus: Farmers’ Practices and Effects on Growth and Ice-ice Disease Occurrence. Regional Studies in Marine Science, 55, 102593. https://doi.org/10.1016/j.rsma.2022.102593

Thingstad, T. F., Krom, M. D., Mantoura, R. F. C., Flaten, G. F., Groom, S., Herut, B., ... & Zohary, T. (2005). Nature of Phosphorus Limitation in the Ultraoligotrophic Eastern Mediterranean. Science, 309(5737), 1068-1071. https://doi.org/10.1126/science.1112632

Torrent, J., Barberis, E., & Gil‐Sotres, F. (2007). Agriculture as a Source of Phosphorus for Eutrophication in Southern Europe. Soil Use and Management, 23, 25-35. https://doi.org/10.1111/j.1475-2743.2007.00122.x

Wang, Z., Xiao, J., Fan, S., Li, Y., Liu, X., & Liu, D. (2015). Who Made the World's Largest Green Tide in China?—an Integrated Study on the İnitiation and Early Development of the Green Tide in Yellow Sea. Limnology and Oceanography, 60(4), 1105-1117. https://doi.org/10.1002/lno.10083

Westheimer, F. H. (1987). Why Nature Chose Phosphates. Science, 235(4793), 1173-1178. https://doi.org/10.1126/science.2434996

Wu, J., Sunda, W., Boyle, E. A., & Karl, D. M. (2000). Phosphate Depletion in the Western North Atlantic Ocean. Science, 289(5480), 759-762. https://doi.org/10.1126/science.289.5480.759

Xu, Z., Zou, D., & Gao, K., 2010. Effects of Elevated CO2 and Phosphorus Supply of Growth, Photosynthesis and Nutrient Uptake in the Marine Macroalga Gracilaria lemaneiformis (Rhodophyta). Botanica Marina, 53, 123-129. https://doi.org/10.1515/BOT.2010.012

Zheng, L., Wu, M., Cui, Y., Tian, L., Yang, P., Zhao, L., ... & Liu, J. (2022). What Causes the Great Green Tide Disaster in the South Yellow Sea of China in 2021?. Ecological Indicators, 140, 108988. https://doi.org/10.1016/j.ecolind.2022.108988

Zhou, M. J., Liu, D. Y., Anderson, D. M., & Valiela, I. (2015). Introduction to the Special Issue on Green Tides in the Yellow Sea. Estuarine, Coastal and Shelf Science, 163, 3-8. https://doi.org/10.1016/j.ecss.2015.06.023






Review Articles