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Contemporary Problems of Ecology

, Volume 12, Issue 2, pp 109–125 | Cite as

Green Tides: New Consequences of the Eutrophication of Natural Waters (Invited Review)

  • M. I. GladyshevEmail author
  • Y. I. Gubelit
Article
  • 46 Downloads

Abstract

In recent decades, alongside the comparatively well-studied bloom caused by phytoplankton, a bloom of marine and fresh waters caused by littoral benthic macroalgae of three genera—Ulva, Cladophora, and Spirogyra—have become a global phenomenon. In the present review, an attempt is made to gain an understanding of why it is these taxa of green filamentous algae that start to grow rapidly in the spring in many water bodies and streams, including oligotrophic waters, and then float up from the bottom, forming floating mats (metaphyton); then their decaying masses are washed ashore and cause substantial ecological and economical losses. Peculiar and common ecological and physiological features of Ulva, Cladophora, and Spirogyra favorable for the formation of green tides are considered. Although eutrophication (the supply of nitrogen and phosphorus from agricultural lands, industrial and domestic wastewaters, and aquaculture) is the evident cause of the increase in algal biomass, it is suggested that the location of external fluxes of inorganic nutrients (surface runoff or groundwater discharge), as well as the biogenic redirection of internal fluxes of nitrogen and phosphorus from pelagial to littoral (benthification), play a key role in the formation of green tides. Measures for controlling green tides are discussed. The necessity for detailed studies of the metaphytonic form of vegetation of benthic macroalgae is emphasized. Obviously, a revision of the present concept of oligotrophic/eutrophic waters which considers only the pelagic compartments of aquatic ecosystems is required.

Keywords

nuisance algal blooms Ulva Cladophora Spirogyra metaphyton benthification 

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References

  1. Abed, R.M.M., Al Kindi, S., Schramm, A., and Barry, M.J., Short-term effects of flooding on bacterial community structure and nitrogenase activity in microbial mats from a desert stream, Aquat. Microb. Ecol., 2011, vol. 63, pp. 245–254.CrossRefGoogle Scholar
  2. Adams, M.S. and Stone, W., Field studies on photosynthesis of Cladophora glomerata (Chlorophyta) in Green bay, Lake Michigan, Ecology, 1973, vol. 54, pp. 853–862.CrossRefGoogle Scholar
  3. Agrawal, S.B. and Ciiaudhary, B.R., Effect of certain environmental factors on zygospore germination of Spirogyra hyaline, Folia Microbiol., 1994, vol. 39, pp. 291–295.CrossRefGoogle Scholar
  4. Agrawal, S.B. and Singh, V., Viability of dried filaments, survivability and reproduction under water stress, and survivability following heat and UV exposure in Lyngbya martensiana, Oscillatoria agardhii, Nostoc calcicola, Hormidium fluitans, Spirogyra sp. and Vaucheria geminate, Folia Microbiol., 2002, vol. 47, pp. 61–67.CrossRefGoogle Scholar
  5. Arora, M. and Sahoo, D., Green algae, in The Algae World, Sahoo, D. and Seckbach, J., Eds., Dordrecht: Springer-Verlag, 2015, pp. 91–120.CrossRefGoogle Scholar
  6. Auer, M.T. and Canale, R.P., Ecological and mathematical modeling of Cladophora in Lake Huron: 3. The dependence of growth rates on internal phosphorus pool size, J. Great Lakes Res., 1982, vol. 8, pp. 93–99.CrossRefGoogle Scholar
  7. Back, S., Lehvo, A., and Blomster, J., Mass occurrence of the unattached Enteromorpha interstinalis on the Finnish Baltic coast, Ann. Bot. Fenn., 2000, vol. 37, pp. 155–161.Google Scholar
  8. Berezina, N.A., Gubelit, Yu.I., Polyak, Yu.M., Sharov, A.N., Kudryavtseva, V.A., Lubimtsev, V.A., Petukhov, V.A., and Shigaeva, T.D., An integrated approach to the assessment of the eastern Gulf of Finland health: A case study of coastal habitats, J. Mar. Syst., 2017, vol. 171, pp. 159–171 doi:  https://doi.org/10.1016/j.jmarsys.2016.08.013 CrossRefGoogle Scholar
  9. Berger, R., Henriksson, E., Kautsky, L., and Malm, T., Effects of filamentous algae and deposited matter on the survival of Fucus vesiculosus L. germlings in the Baltic Sea, Aquat. Ecol., 2003, vol. 37, pp. 1–11.CrossRefGoogle Scholar
  10. Berry, H.A. and Lembi, C.A., Effects of temperature and irradiance on the seasonal variation of a Spirogyra (Chlorophyta) population in a midwestern lake (U.S.A.), J. Phycol., 2000, vol. 36, pp. 841–851.CrossRefGoogle Scholar
  11. Bhat, N.A., Wanganeo, A., and Raina, R., Seasonal dynamics of phytoplankton community in a tropical wetland, Environ. Monit. Assess., 2015, vol. 187, p. 4136.CrossRefPubMedGoogle Scholar
  12. Biggs, B.J.F., Goring, D.G., and Nikora, V.I., Subsidy and stress responses of stream periphyton to gradients in water velocity as a function of community growth form, J. Phycol., 1998, vol. 34, pp. 598–607.CrossRefGoogle Scholar
  13. Bormans, M., Marsalek, B., and Jancula, D., Controlling internal phosphorus loading in lakes by physical methods to reduce cyanobacterial blooms: a review, Aquat. Ecol., 2016, vol. 50, pp. 407–422.CrossRefGoogle Scholar
  14. Brookes, J.D. and Carey, C.C., Resilience to blooms, Science, 2011, vol. 334, pp. 46–47.CrossRefPubMedGoogle Scholar
  15. Boughey, A.S. Ecology of Populations, New York: Macmillan, 1968.Google Scholar
  16. Byappanahalli, M.N., Shively, D.A., Nevers, M.B., Sadowsky, M.J., and Whitman, R.L., Growth and survival of Escherichia coli and enterococci populations in the macro-alga Cladophora (Chlorophyta), FEMS Microbiol. Ecol., 2003, vol. 46, pp. 203–211.CrossRefPubMedGoogle Scholar
  17. Byappanahalli, M.N., Sawdey, R., Ishii, S., Shively, D.A., Ferguson, J., Whitman, R.L., and Sadowsky, M.J., Seasonal stability of Cladophora-associated Salmonella in Lake Michigan watersheds, Water Res., 2009, vol. 43, pp. 806–814.CrossRefPubMedGoogle Scholar
  18. Cattaneo, A., Hudon, C., Vis, C., and Gagnon, P., Hydrological control of filamentous green algae in a large fluvial lake (Lake Saint-Pierre, St. Lawrence River, Canada), J. Great Lakes Res., 2013, vol. 39, pp. 409–419.CrossRefGoogle Scholar
  19. Chambouvet, A., Morin, P., Marie, D., and Guillou, L., Control of toxic marine dinoflagellate blooms by serial parasitic killers, Science, 2008, vol. 322, pp. 1254–1257.CrossRefPubMedGoogle Scholar
  20. Chang, Y.H., Kub, C.R., and Lu, H.L., Effects of aquatic ecological indicators of sustainable green energy landscape facilities, Ecol. Eng., 2014, vol. 71, pp. 144–153.CrossRefGoogle Scholar
  21. Chavez-Sanchez, T., Pinon-Gimate, A., Serviere-Zaragoza, E., Lopez-Bautista, J.M., and Casas-Valdez, M., Ulva blooms in the southwestern Gulf of California: Reproduction and biomass, Estuarine, Coastal Shelf Sci., 2018, vol. 200, pp. 202–211.CrossRefGoogle Scholar
  22. Choo, K., Snoeijs, P., and Pedersen, M., Oxidative stress tolerance in the filamentous green algae Cladophora glomerata and Enteromorpha ahlneriana, J. Exp. Mar. Biol. Ecol., 2004, vol. 298, pp. 111–123.CrossRefGoogle Scholar
  23. Cohen, R.A. and Fong, P., Using opportunistic green macroalgae as indicators of nitrogen supply and sources to estuaries, Ecol. Appl., 2006, vol. 16, pp. 1405–1420.CrossRefPubMedGoogle Scholar
  24. Cuhel, R.L. and Aguilar, C., Ecosystem transformations of the Laurentian Great Lake Michigan by nonindigenous biological invaders, Annu. Rev. Mar. Sci., 2013, vol. 5, pp. 289–320.CrossRefGoogle Scholar
  25. Dodds, W.K. and Gudder, D.A., Ecology of Cladophora, J. Phycol., 1992, vol. 28, pp. 415–427.CrossRefGoogle Scholar
  26. Dong, B.C., Liu, R.H., and Yu, F.H., Effects of Spirogyra arcta on biomass and structure of submerged macrophyte communities, Plant Species Biol., 2015, vol. 30, pp. 28–36.CrossRefGoogle Scholar
  27. Entwisle, T.J., Phenology of Cladophora—Stigeoclonium community in two urban creeks of Melbourne, Aust. J. Mar. Freshwater Res., 1989, vol. 40, pp. 471–489.CrossRefGoogle Scholar
  28. Filipkowska, A., Lubecki, L., Szymczak-Żyła, M., Kowalewska, G., Żbikowski, R., and Szefer, P., Utilization of macroalgae from the Sopot beach (Baltic Sea), Oceanologia, 2008, vol. 50, pp. 255–273.Google Scholar
  29. Flores-Moya, A., Costas, E., Bañares-España, E., García-Villada, L., Altamirano, M., and López-Rodaset, V., Adaptation of Spirogyra insignis (Chlorophyta) to an extreme natural environment (sulphurous waters) through preselective mutations, New Phytol., 2005, vol. 166, pp. 655–661.CrossRefPubMedGoogle Scholar
  30. Freeman, M.C., The role of nitrogen and phosphorus in the development of Cladophora glomerata (L.) Kützing in the Manawatu River, New Zealand, Hydrobiologia, 1986, vol. 131, pp. 23–30.CrossRefGoogle Scholar
  31. Frossard, V., Versanne-Janodet, S., and Aleya, L., Factors supporting harmful macroalgal blooms in flowing waters: A 2-year study in the Lower Ain River, France, Harmful Algae, 2014, vol. 33, pp. 19–28.CrossRefGoogle Scholar
  32. Gao, G., Clarea, A.S., Rose, C., and Caldwell, G.S., Intrinsic and extrinsic control of reproduction in the green tide-forming alga, Ulva rigida, Environ. Exp. Bot., 2017, vol. 139, pp. 14–22.CrossRefGoogle Scholar
  33. Ge, C., Yu, X., Kan, M., and Qu, C., Adaptation of Ulva pertusa to multiple-contamination of heavy metals and nutrients: Biological mechanism of outbreak of Ulva sp. green tide, Mar. Pollut. Bull., 2017, vol. 125, pp. 250–253.CrossRefPubMedGoogle Scholar
  34. Ge, S., Madill, M., and Champagne, P., Use of freshwater macroalgae Spirogyra sp. for the treatment of municipal wastewaters and biomass production for biofuel applications, Biomass Bioenergy, 2018, vol. 111, pp. 213–223.CrossRefGoogle Scholar
  35. Gelwick, F.P. and Matthews, W.J., Effects of algivorous minnows (Campostoma) on spatial and temporal heterogeneity of stream periphyton, Oecologia, 1997, vol. 112, pp. 386–392.CrossRefPubMedGoogle Scholar
  36. Golubkov, S.M., Berezina, N.A., Gubelit, Yu.I., Demchuk, A.S., Golubkov, M.S., and Tiunov, A.V., A relative contribution of carbon from green tide algae Cladophora glomerata and Ulva intestinalis in the coastal food webs in the Neva Estuary (Baltic Sea), Mar. Pollut. Bull., 2018, vol. 126, pp. 43–50.CrossRefPubMedGoogle Scholar
  37. Gorain, P.C., Sengupta, S., Satpati, G.G., Paul, I., Tripathi, S., and Pal, R., Carbon sequestration in macroalgal mats of brackish-water habitats in Indian Sunderbans: potential as renewable organic resource, Sci. Total Environ., 2018, vol. 626, pp. 689–702.CrossRefPubMedGoogle Scholar
  38. Graham, J.M., Auer, M.T., Canale, R.P., and Hoffmann, J.P., Ecological studies and mathematical modeling of Cladophora in Lake Huron. 4. Photosynthesis and respiration as functions of light and temperature, J. Great Lakes Res., 1982, vol. 8, pp. 100–111.CrossRefGoogle Scholar
  39. Gubelit, Yu.I. and Kovalchuk, N.A., Macroalgal blooms and species diversity in the Transition Zone of the eastern Gulf of Finland, Hydrobiologia, 2010, vol. 656, no. 1, pp. 83–86.CrossRefGoogle Scholar
  40. Gubelit, Y.I., Makhutova, O.N., Sushchik, N.N., Kolmakova, A.A., Kalachova, G.S., and Gladyshev, M.I., Fatty acid and elemental composition of littoral “green tide” algae from the Gulf of Finland, the Baltic Sea, J. Appl. Phycol., 2015, vol. 27, pp. 375–386.CrossRefGoogle Scholar
  41. Gubelit, Yu., Polyak, Yu., Dembska, G., Pazikowska-Sapota, G., Zegarowski, L., Kochura, D., Krivorotov, D., Podgornaya, E., Burova, O., and Maazouzi, Ch., Nutrient and metal pollution of the eastern Gulf of Finland coastline: sediments, macroalgae, microbiota, Sci. Total Environ., 2016, vol. 550, pp. 806–819. doi:  https://doi.org/10.1016/j.scitotenv.2016.01.122 CrossRefPubMedGoogle Scholar
  42. Gubelit, Yu.I. and Vainshtein, M.B., Growth of Enterobacteria on algal mats in the eastern part of the Gulf of Finland, Inland Water Biol., 2011, vol. 4, no. 2, pp. 132–136.CrossRefGoogle Scholar
  43. Gulati, R.D., Dionisio Pires, L.M., and van Donk, E., Lake restoration studies: failures, bottlenecks, and prospects of new ecotechnological measures, Limnologica, 2008, vol. 38, pp. 233–247.CrossRefGoogle Scholar
  44. Hainz, R., Wober, C., and Schagerl, M., The relationship between Spirogyra (Zygnematophyceae, Streptophyta) filament type groups and environmental conditions in Central Europe, Aquat. Bot., 2009, vol. 91, pp. 173–180.CrossRefGoogle Scholar
  45. Han, H., Chen, Y., Jørgensen, S.E., Nielsen, S.N., and Hu, W., A system-dynamic model on the competitive growth between Potamogeton malaianus Miq. and Spirogyra sp., Ecol. Model., 2009, vol. 220, pp. 2206–2217.CrossRefGoogle Scholar
  46. Harris, V.A., Cladophora confounds coastal communities—public perceptions and management dilemmas, Proc. Workshop “Cladophora Research and Management in the Great Lakes,” Boostma, H., Jenson, E., Young, E., and Berges, J., Eds., Milwaukee, WI: Univ. of Wisconsin-Milwaukee, 2005, no. 2005-01.Google Scholar
  47. Havens, K.E., East, T.L., Hwang, S.J., Rodusky, A.J., Sharfstein, B., and Steinman, A.D., Algal responses to experimental nutrient addition in the littoral community of a subtropical lake, Freshwater Biol., 1999, vol. 42, pp. 329–344.CrossRefGoogle Scholar
  48. Hawes, I., The seasonal dynamics of Spirogyra in a shallow, maritime Antarctic lake, Polar Biol., 1988, vol. 8, pp. 429–437.CrossRefGoogle Scholar
  49. Higgins, S.N., Modeling the growth dynamics of Cladophora in eastern Lake Erie, PhD Thesis Waterloo: Univ. of Waterloo, 2005.Google Scholar
  50. Higgins, S.N., Hecky, R.E., and Guildford, S.J., The collapse of benthic macroalgal blooms in response to self—shading, Freshwater Biol., 2008a, vol. 53, pp. 2557–2572.CrossRefGoogle Scholar
  51. Higgins, S.N., Malkin, S.Y., Howell, E.T., Guildford, S.J., Campbell, L., Hiriart-Baer, V., and Hecky R.E., An ecological review of Cladophora glomerata (Chlorophyta) in the Laurentian Great Lakes, J. Phycol., 2008b, vol. 44, pp. 839–854.CrossRefPubMedGoogle Scholar
  52. Hoffmann, J.P. and Graham, L.E., Effects of selected physiochemical factors on growth and zoosporogenesis of Cladophora glomerata (Chlorophyta), J. Phycol., 1984, vol. 20, pp. 1–7.CrossRefGoogle Scholar
  53. Hofmann, L.C., Nettleton, J.C., Neefus, C.D., and Mathieson, A.C., Cryptic diversity of Ulva (Ulvales, Chlorophyta) in the Great Bay estuarine system (Atlantic USA): introduced and indigenous distromatic species, Eur. J. Phycol., 2010, vol. 45, no. 3, pp. 230–239.CrossRefGoogle Scholar
  54. Hondzo, M. and Wang, H., Effects of turbulence on growth and metabolism of periphyton in a laboratory flume, Water Resour. Res., 2002, vol. 38, no. 12, p. 1277. doi:  https://doi.org/10.1029/2002WR001409 CrossRefGoogle Scholar
  55. Hupfer, M. and Lewandowski, J., Oxygen controls the phosphorus release from lake sediments—a long-lasting paradigm in limnology, Int. Rev. Hydrobiol., 2008, vol. 93, pp. 415–432.CrossRefGoogle Scholar
  56. Ibelings, B.W., Bormans, M., Fastner, J., and Visser, P.M., CYANOCOST special issue on cyanobacterial blooms: synopsis—a critical review of the management options for their prevention, control and mitigation, Aquat. Ecol., 2016, vol. 50, pp. 595–605.CrossRefGoogle Scholar
  57. Ikegaya, H., Nakase, T., Iwata, K., Tsuchida, H., Sonobe, S., and Shimmen, T., Studies on conjugation of Spirogyra using monoclonal culture, J. Plant Res., 2012, vol. 125, pp. 457–464.CrossRefPubMedGoogle Scholar
  58. Ishida, N., Mitamura, O., and Nakayama, M., Seasonal variation in biomass and photosynthetic activity of epilithic algae on a rock at the upper littoral area in the north basin of Lake Biwa, Japan, Limnology, 2006, vol. 7, pp. 175–183.CrossRefGoogle Scholar
  59. Jeppesen, E., Sondergaard, M., Krovang, B., Jensen, J.P., Svendsen, L.M., and Lauridsen, T.L., Lake and catchment management in Denmark, Hydrobiologia, 1999, vols. 395–396, pp. 419–432.CrossRefGoogle Scholar
  60. Johnson, R., The benthic food web on nearshore hard substrates at Peacock Point, eastern Lake Erie, MSc Thesis, Waterloo: Univ. of Waterloo, 2004.Google Scholar
  61. Klemencic, A.K. and Toman, M.J., Influence of environmental variables on benthic algal associations from selected extreme environments in Slovenia in relation to the species identification, Period. Biol., 2010, vol. 112, pp. 179–191.Google Scholar
  62. Komulaynen, S.F., Green algae as a structural element of phytoperiphyton communities in streams of NW Russia, Biologia, 2008, vol. 63, pp. 859–865.CrossRefGoogle Scholar
  63. Kraufvelin, P. and Salovius, S., Animal diversity in Baltic rocky shore macroalgae: can Cladophora glomerata compensate for lost Fucus vesiculosus? Estuarine, Coastal Shelf Sci., 2004, vol. 61, pp. 369–378.CrossRefGoogle Scholar
  64. Kravtsova, L.S., Izhboldina, L.A., Khanaev, I.V., Pomazkina, G.V., Rodionova, E.V., Domysheva, V.M., Sakirko, M.V., Tomberg, I.V., Kostornova, T.Y., Kravchenko, O.S., and Kupchinsky, A.B., Nearshore benthic blooms of filamentous green algae in Lake Baikal, J. Great Lakes Res., 2014, vol. 40, pp. 441–448.CrossRefGoogle Scholar
  65. Krupek, R.A., Empinotti, A., Santos, R.K., and Araujo, E.A.T., Influence of physical characteristics of environment (light and current velocity) on the substrate occupation by Spirogyra sp. in stream ecosystems, Braz. J. Bot., 2014, vol. 37, pp. 453–459.CrossRefGoogle Scholar
  66. Kumar, J., Dhar, P., Tayade, A. B, Gupta, D., Chaurasia, O.P., Upreti, D.K., Toppo, K., Arora, R., Suseela, M.R., and Srivastava, R.B., Chemical composition and biological activities of trans-Himalayan alga Spirogyra porticalis (Muell.) Cleve, PLoSOne, 2015, vol. 10, no. 2, p. e0118255. doi:  https://doi.org/10.1371/journal.pone.0118255 CrossRefGoogle Scholar
  67. Kwon, H.K., Kang, H., Oh, Y.H., Park, S.R., and Kim, G., Green tide development associated with submarine groundwater discharge in a coastal harbor, Jeju, Korea, Sci. Rep., 2017, vol. 7, pp. 6325.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Larsen, A. and Sand-Jensen, K., Salt tolerance and distribution of estuarine benthic macroalgae in the Kattegat—Baltic Sea area, Phycologia, 2006, vol. 45, pp. 13–23.CrossRefGoogle Scholar
  69. Lee, J.W. and Kim, G.H., Two-track control of cellular machinery for photomovement in Spirogyra varians (Streptophyta, Zygnematales), Plant Cell Physiol., 2017, vol. 58, pp. 1812–1822.CrossRefPubMedGoogle Scholar
  70. Lehvo, A. and Bäck, S., Survey of macroalgal mats in the Gulf of Finland, Baltic Sea, Aquat. Conserv., 2001, vol. 11, pp. 11–18.CrossRefGoogle Scholar
  71. Lenzi, M., What can be done about massive macroalgal blooms? J. Aquacult. Res. Dev., 2014, vol. 5, no. 8, p. 1000292.Google Scholar
  72. Li, H., Zhang, Y., Tang, H., Shi, X., Rivkin, R.B., and Legendre, L., Spatiotemporal variations of inorganic nutrients along the Jiangsu coast, China, and the occurrence of macroalgal blooms (green tides) in the southern Yellow Sea, Harmful Algae, 2017, vol. 63, pp. 164–172.CrossRefPubMedGoogle Scholar
  73. Liess, A. and Kahlert, M., Gastropod grazers and nutrients, but not light, interact in determining periphytic algal diversity, Oecologia, 2007, vol. 152, pp. 101–111.CrossRefPubMedGoogle Scholar
  74. Liu, D., Keesing, J.K., Xing, Q., and Shi, P., World’s largest macroalgal bloom caused by expansion of seaweed aquaculture in China, Mar. Pollut. Bull., 2009, vol. 58, pp. 888–895.CrossRefPubMedGoogle Scholar
  75. Liu, J., Su, N., Wang, X., and Du, J., Submarine ground-water discharge and associated nutrient fluxes into the Southern Yellow Sea: A case study for semi-enclosed and oligotrophic seas-implication for green tide bloom, J. Geophys. Res.: Oceans, 2017, vol. 122, pp. 139–152.CrossRefGoogle Scholar
  76. Liu, R.H., Dong, B.C., Li, H.L., Zhang, Q., and Yu, F.H., Patchy distributions of Spirogyra arcta do not affect growth of the submerged macrophyte Ceratophyllum demersum, Plant Species Biol., 2012, vol. 27, pp. 210–217.CrossRefGoogle Scholar
  77. Lurling, M., Mackay, E., Reitzel, K., and Spears, B.M., Editorial—a critical perspective on geo-engineering for eutrophication management in lakes, Water Res., 2016, vol. 97, pp. 1–10.CrossRefPubMedGoogle Scholar
  78. Mackay, E.B., Maberly, S.C., Pan, G., Reitzel, K., Bruere, A., Corker, N., Douglas, G., Egemose, S., Hamilton, D., Hatton-Ellis, T., Huser, B., Li, W., Meis, S., Moss, B., Lürling, M., et al., Geoengineering in lakes: welcome attraction or fatal distraction? Inland Waters, 2014, vol. 4, pp. 349–356.CrossRefGoogle Scholar
  79. Mantai, K.E., Some aspects of photosynthesis in Cladophora glomerata, J. Phycol., 1974, vol. 10, pp. 288–291.Google Scholar
  80. Martem’yanov, V.I. and Mavrin, A.S., Threshold environmental concentrations of cations determining the boundaries of survival of the filamentous alga Spirogyra sp. in freshwater reservoirs, Contemp. Probl. Ecol., 2012, vol. 5, no. 3, pp. 250–254.CrossRefGoogle Scholar
  81. Martins, I., Pardal, M.A., Lilleboa, A.I., Flindt, M.R., and Marques, J.C., Hydrodynamics as a major factor controlling the occurrence of green macroalgal blooms in a eutrophic estuary: A case study on the influence of precipitation and river management, Estuarine, Coastal Shelf Sci., 2001, vol. 52, pp. 165–177.CrossRefGoogle Scholar
  82. McCormick, P.V., Shuford, R.B.E. III, Backus, J.G., and Kennedy, W.C., Spatial and seasonal patterns of periphyton biomass and productivity in the northern Everglades, Florida, U.S.A., Hydrobiologia, 1998, vol. 362, pp. 185–208.CrossRefGoogle Scholar
  83. McCrackin, M.L., Jones, H.P., Jones, P.C., and Moreno-Mateos, D., Recovery of lakes and coastal marine ecosystems from eutrophication: a global meta-analysis, Limnol. Oceanogr., 2017, vol. 62, pp. 507–518.CrossRefGoogle Scholar
  84. Migliore, G., Alisi, C., Sprocati, A.R., Massi, E., Ciccoli, R., Lenzi, M., Wang, A., and Cremisini, C., Anaerobic digestion of macroalgal biomass and sediments sourced from the Orbetello Lagoon, Italy, Biomass Bioenergy, 2012, vol. 42, pp. 69–77.CrossRefGoogle Scholar
  85. Mihranyan, A., Cellulose from cladophorales green algae: from environmental problem to high-tech composite materials, J. Appl. Polym. Sci., 2011, vol. 119, pp. 2449–2460.CrossRefGoogle Scholar
  86. Mills, E.L., Casselman, J.M., Dermott, R., Fitzsimons, J.D., Gal, G., Holeck, K.T., Hoyle, J.A., Johannsson, O.E., Lantry, B.F., Makarewicz, J.., Millard, E.S., Munawar, I.F., Munawar, M., O’Gorman, R., Owens, R.W., et al., Lake Ontario: food web dynamics in a changing ecosystem (1970–2000), Can. J. Fish. Aquat. Sci., 2003, vol. 60, pp. 471–490.CrossRefGoogle Scholar
  87. Mohamed, Z.A., Allelopathic activity of Spirogyra sp.: stimulating blooming formation and toxin production by Oscillatoria agardhii in some irrigation canals, Egypt, J. Plankton Res., 2002, vol. 24, pp. 137–141.CrossRefGoogle Scholar
  88. Morand, P. and Merceron, M., Macroalgal population and sustainability, J. Coastal Res., 2005, vol. 21, pp. 1009–1020.CrossRefGoogle Scholar
  89. Munir, N., Imtiaz, A., Sharif, N., and Naz, S., Optimization of growth conditions of different algal strains and determination of their lipid contents, J. Anim. Plant Sci., 2015, vol. 25, pp. 546–553.Google Scholar
  90. Nelson, T.A. and Gregg, B.C., Determination of EC50 for normal oyster larval development in extracts from bloom forming green seaweeds, Nautilus, 2013, vol. 127, pp. 156–159.Google Scholar
  91. Nelson, T.A., Lee, D.J., and Smith, B.C., Are “green tides” harmful algal blooms? Toxic properties of water-soluble extracts from two bloom-forming macroalgae, Ulva fenestrate and Ulvaria obscura (Ulvophyceae), J. Phycol., 2003, vol. 39, pp. 874–879.CrossRefGoogle Scholar
  92. Nelson, T.A. Haberlin, K., Nelson, A.V., Ribarich, H., Hotchkiss, R., van Alstyne, K.L., Buckingham, L., Simunds, D.J., and Fredrickson, K., Ecological and physiological controls of species composition in green macroalgal blooms, Ecology, 2008, vol. 89, pp. 1287–1298.CrossRefPubMedGoogle Scholar
  93. Nozaki, K., Abrupt change in primary productivity in a littoral zone of Lake Biwa with the development of a filamentous green-algal community, Freshwater Biol., 2001, vol. 46, pp. 587–602.CrossRefGoogle Scholar
  94. Nozaki, K., Darijav, K., Akatsuka, T., Goto, N., and Mitamura, O., Development of filamentous green algae in the benthic algal community in a littoral sand-beach zone of Lake Biwa, Limnology, 2003, vol. 4, pp. 161–165.CrossRefGoogle Scholar
  95. Orihel, D.M., Baulch, H.M., Casson, N.J., North, R.L., Parsons, C.T., Seckar, D.C.M., and Venkiteswaran, J.J., Internal phosphorus loading in Canadian fresh waters: a critical review and data analysis, Can. J. Fish. Aquat. Sci., 2017, vol. 74, pp. 2005–2029.CrossRefGoogle Scholar
  96. Orlova, M.I., Anokhina, L.E., Panov, V.E., Nekrasov, A.V., and Klimentenok, S.N., Preliminary environmental state assessment for littoral zone in resort district of St. Petersburg, Res. Bull. Baltic Floating Univ., 1999, vol. 3, pp. 37–42.Google Scholar
  97. Paerl, H.W., Controlling harmful cyanobacterial blooms in a climatically more extreme world: management options and research needs, J. Plankton Res., 2017, vol. 39, pp. 763–771.CrossRefGoogle Scholar
  98. Paerl, H.W., Fulton, R.S. III, Moisander, P.H., and Dyble, J., Harmful freshwater algal blooms, with emphasis on cyanobacteria, Sci. World J., 2001, vol. 1, pp. 76–113.CrossRefGoogle Scholar
  99. Park, S.R., Kang, Y.H., and Choi, C.G., Biofilm: a crucial factor affecting the settlement of seaweed on intertidal rocky surfaces, Estuarine, Coastal Shelf Sci., 2011, vol. 91, p. 163e167.CrossRefGoogle Scholar
  100. Peckol, P. and Putnam, A.B., Differential toxic effects of Ulva lactuca (Chlorophyta) on the herbivorous gastropods, Littorina littorea and L. obtusata (Mollusca), J. Phycol., 2017, vol. 53, pp. 361–367.CrossRefPubMedGoogle Scholar
  101. Perrot, T., Rossi, N., Ménesguen, A., and Dumas, F., Modeling green macroalgal blooms on the coasts of Brittany, France to enhance water quality management, J. Mar. Syst., 2014, vol. 132, pp. 38–53.CrossRefGoogle Scholar
  102. Philips, G., Bramwell, A., Pitt, J., Stansfield, J., and Perrow, M., Practical application of 25 years’ research into the management of shallow lakes, Hydrobiologia, 1999, vols. 395–396, pp. 61–76.CrossRefGoogle Scholar
  103. Pillsbury, R.W., Lowe, R.L., Pan, Y.D., and Greenwood, J.L., Changes in the benthic algal community and nutrient limitation in Saginaw Bay, Lake Huron, during the invasion of the zebra mussel (Dreissena polymorpha), J. N. Am. Benthol. Soc., 2002, vol. 21, pp. 238–252.CrossRefGoogle Scholar
  104. Polyak, Y., Shigaeva, T., Gubelit, Y., Bakina, L., Kudryavtseva, V., and Polyak, M., Sediment microbial activity and its relation to environmental variables along the eastern Gulf of Finland coastline, J. Mar. Syst., 2017, vol. 171, pp. 101–110.CrossRefGoogle Scholar
  105. Power, M., Lowe, R., Furey, P., Welter, J., Limm, M., Finlay, J., Bode, C., Chang, S., Goodrich, M., and Sculley, J., Algal mats and insect emergence in rivers under Mediterranean climates: towards photogrammetric surveillance, Freshwater Biol., 2009, vol. 54, pp. 2101–2115.CrossRefGoogle Scholar
  106. Rai, U.N., Dubey, S., Shukla, O.P., Dwivedi, S., and Tripathi, R.D., Screening and identification of early warning algal species for metal contamination in fresh water bodies polluted from point and non-point sources, Environ. Monit. Assess., 2008, vol. 144, pp. 469–481.CrossRefPubMedGoogle Scholar
  107. Robinson, P.K. and Hawkes, H.A., Studies on the growth of Cladophora glomerata in laboratory continuous-flow culture, Br. Phycol. J., 1986, vol. 21, pp. 437–444.CrossRefGoogle Scholar
  108. Ross, S., Sheath, R., and Muller, K., Molecular phylogeography and species discrimination of freshwater Cladophora (Cladophorales, Chlorophyta) in North America, Proc. Workshop “Cladophora Research and Management in the Great Lakes,” Boostma, H., Jenson, E., Young, E., and Berges, J., Eds., Milwaukee, WI: Univ. of Wisconsin-Milwaukee, 2005, no. 2005-01.Google Scholar
  109. Ruangchuay, R., Dahamat, S., Chirapat, A., and Notoya, M., Effects of culture conditions on the growth and reproduction of Gut weed, Ulva intestinalis Linnaeus (Ulvales, Chlorophyta), Songklankarin J. Sci. Technol., 2012, vol. 34, pp. 501–507.Google Scholar
  110. Selala, C., Botha, A.-M., de Klerk, L.P., de Klerk, A.R., Myburgh, J.G., and Oberholster, P.J., Using phytoplankton diversity to determine wetland resilience, one year after a vegetable oil spill, Water, Air Soil Pollut., 2014, vol. 225, p. 2051.CrossRefGoogle Scholar
  111. Singh, S.P. and Singh, P., Effect of temperature and light on the growth of algae species: a review, Renewable Sustainable Energy Rev., 2015, vol. 50, pp. 431–444.CrossRefGoogle Scholar
  112. Smetacek, V. and Zingone, A., Green and golden seaweed tides on the rise, Nature, 2013, vol. 504, pp. 84–88.CrossRefPubMedGoogle Scholar
  113. Sushchik, N.N., Gladyshev, M.I., Ivanova, E.A., and Kravchuk, E.S., Seasonal distribution and fatty acid composition of littoral microalgae in the Yenisei River, J. Appl. Phycol., 2010, vol. 22, pp. 11–24.CrossRefGoogle Scholar
  114. Townsend, S.A., Schult, J.H., Douglas, M.M., and Skinner, S., Does the Redfield ratio infer nutrient limitation in the macroalga Spirogyra fluviatilis? Freshwater Biol., 2008, vol. 53, pp. 509–520.CrossRefGoogle Scholar
  115. Townsend, S.A., Garcia, E.A., and Douglas, M.M., The response of benthic algal biomass to nutrient addition over a range of current speeds in an oligotrophic river, Freshwater Sci., 2012, vol. 31, pp. 1233–1243.CrossRefGoogle Scholar
  116. Townsend, S., Schult, J., Douglas, M., and Lautenschlager, A., Recovery of benthic primary producers from flood disturbance and its implications for an altered flow regime in a tropical savannah river (Australia), Aquat. Bot., 2017, vol. 136, pp. 9–20.CrossRefGoogle Scholar
  117. Trochine, C., Guerrieri, M., Liboriussen, L., Meerhoff, M., Lauridsen, T.L., Sondergaard, M., and Jeppesen, E., Filamentous green algae inhibit phytoplankton with enhanced effects when lakes get warmer, Freshwater Biol., 2011, vol. 56, pp. 541–553.CrossRefGoogle Scholar
  118. Thybo-Christesen, M., Rasmussen, M.B., and Blackburn, T.H., Nutrient fluxes and growth of Cladophora sericea in a shallow Danish bay, Mar. Ecol.: Prog. Ser., 1993, vol. 100, pp. 273–281.CrossRefGoogle Scholar
  119. Triest, L., Stiers, I., and van Onsem, S., Biomanipulation as a nature-based solution to reduce cyanobacterial blooms, Aquat. Ecol., 2016, vol. 50, pp. 461–483.CrossRefGoogle Scholar
  120. Valiela, I., McClelland, J., Hauxwell, J., Behr, P.J., Hersh, D., and Foreman, K., Macroalgal blooms in shallow estuaries: controls and ecophysiological and ecosystem consequences, Limnol. Oceanogr., 1997, vol. 42, pp. 1105–1118.CrossRefGoogle Scholar
  121. van den Hoek, C. Revision of the European Species of Cladophora, Leiden: E.J. Brill, 1963.Google Scholar
  122. Vogel, V. and Bergmann, P., Culture of Spirogyra sp. in a flat-panel airlift photobioreactor, 3 Biotech., 2018, vol. 8, p. 6.CrossRefPubMedGoogle Scholar
  123. Wallentinus, I., Comparisons of nutrient uptake rates for Baltic macroalgae with different thallus morphologies, Mar. Biol., 1984, vol. 80, pp. 215–225.CrossRefGoogle Scholar
  124. Wan, A.H.L., Wilkes, R.J., Heesch, S., Bermejo, R., Johnson, M.P., and Morrison, L., Assessment and characterization of Ireland’s green tides (Ulva species), PLoS One, 2017, vol. 12, no. 1, p. e0169049.CrossRefPubMedPubMedCentralGoogle Scholar
  125. Wang, Z., Xiao, J., Fan, S., Li, Y., Liu, X., and Liu, D., 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., 2015, vol. 60, pp. 1105–1117.CrossRefGoogle Scholar
  126. Whitman, R.L., Shively, D.A., Pawlik, H., Nevers, M.B., and Byappanahalli, M.N., Occurrence of Escherichia coli and enterococci in Cladophora (Chlorophyta) in nearshore water and beach sand of Lake Michigan, Appl. Environ. Microbiol., 2003, vol. 69, pp. 4714–4719.CrossRefPubMedPubMedCentralGoogle Scholar
  127. Whitton, B.A., The biology of Cladophora in freshwaters, Water Res., 1970, vol. 4, pp. 457–476.CrossRefGoogle Scholar
  128. Wu, H., Zhang, J., Yarish, C., He, P., and Kim, J.K., Bioremediation and nutrient migration during blooms of Ulva in the Yellow Sea, China, Phycologia, 2018, vol. 57, pp. 223–231.CrossRefGoogle Scholar
  129. Ye, N., Zhang, X., Mao, Y., Liang, C., Xu, D., Zou, J., Zhuang, Z., and Wang, Q., ‘Green tides’ are overwhelming the coastline of our blue planet: taking the world’s largest example, Ecol. Res., 2011, vol. 26, pp. 477–485.CrossRefGoogle Scholar
  130. Yoshida, K. and Shimmen, T., Involvement of actin filaments in rhizoid morphogenesis of Spirogyra, Physiol. Plant, 2009, vol. 135, pp. 98–107.CrossRefPubMedGoogle Scholar
  131. Zebek, E., Seasonal dynamics of phytoplankton with relation to physicochemical water parameters above and below the hydroelectric plant on the Pasleka River (North-East Poland), Water Resour., 2014, vol. 41, pp. 583–591.CrossRefGoogle Scholar
  132. Zhang, H., Chen, R., Li, F., and Chen, L., Effect of flow rate on environmental variables and phytoplankton dynamics: results from field enclosures, Chin. J. Oceanol. Limnol., 2015, vol. 33, pp. 430–438.CrossRefGoogle Scholar
  133. Zhang, X., Xu, D., Mao, Y., Li, Y., Xue, S., Zou, J., Lian, W., Liang, C., Zhuang, Z., Wang, Q., and Ye, N., Settlement of vegetative fragments of Ulva prolifera confirmed as an important seed source for succession of a large-scale green tide bloom, Limnol. Oceanogr., 2011, vol. 56, pp. 233–242.CrossRefGoogle Scholar
  134. Zhu, B., Fitzgerald, D.G., Mayer, C.M., Rudstam, L.G., and Mills, E.L., Alteration of ecosystem function by zebra mussels in Oneida Lake: impacts on submerged macrophytes, Ecosystems, 2006, vol. 9, pp. 1017–1028.CrossRefGoogle Scholar

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© Pleiades Publishing, Ltd. 2019

Authors and Affiliations

  1. 1.Siberian Federal UniversityKrasnoyarskRussia
  2. 2.Institute of Biophysics, Siberian Branch, Krasnoyarsk Science CenterRussian Academy of SciencesKrasnoyarskRussia
  3. 3.Zoological InstituteRussian Academy of ScienceSt. PetersburgRussia

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