A novel model for cyanobacteria bloom formation: The critical role of anoxia and ferrous iron

Freshwater Biology

Volumn 59, Issue 6, 2014, Pages 1323-1340

  Molot, L A ^a   Watson, S B ^b   Creed, I F ^c   Trick, C G ^c   Mccabe, S K ^a   Verschoor, M J ^a   Sorichetti, R J ^c   Powe, C ^a   Venkiteswaran, J J ^d   Schiff, S L ^d  

^a YORK UNIVERSITY   (Canada)

^b ENVIRONMENT CANADA   (Canada)

^c UNIVERSITY OF WESTERN ONTARIO   (Canada)

^d UNIVERSITY OF WATERLOO   (Canada)

Author keywords

Cyanobacteria; Eutrophication; Freshwaters; Nuisance algae; Nutrient cycling

Indexed keywords

ALGAE; CYANOBACTERIA; EUKARYOTA;

EID: 84897963680     PISSN: 00465070     EISSN: 13652427     Source Type: Journal    
DOI: 10.1111/fwb.12334     Document Type: Article

References (144)

1. Anderson N., Blomqvist P. & Renberg I. (1997) An experimental and palaeoecological study of algal responses to lake acidification and liming in three central Swedish lakes. European Journal of Phycology, 32, 35-48.
2. Aubriot L. & Bonilla S. (2012) Rapid regulation of phosphate uptake in freshwater cyanobacterial blooms. Aquatic Microbial Ecology, 67, 251-263.
3. Bell T. & Kalff J. (2001) The contribution of picophytoplankton in marine and freshwater systems of different trophic status and depth. Limnology and Oceanography, 46, 1243-1248.
4. Berman-Frank I., Cullen J., Shaked Y., Sherrell R. & Falkowski P. (2001) Iron availability, cellular iron quotas, and nitrogen fixation in Trichodesmium. Limnology and Oceanography, 46, 1249-1260.
5. Berman-Frank I., Quigg A., Finkel Z.V., Irwin A.J. & Haramaty L. (2007) Nitrogen-fixation stargetgies and Fe requirements in cyanobacteria. Limnology and Oceanography, 52, 2260-2269.
6. Bernard A. & Symonds R.B. (1989) The significance of siderite in the sediments from Lake Nyos, Cameroon. Journal of Volcanology and Geothermal Research, 39, 187-194.
7. Blomqvist P., Pettersson A. & Hyenstrand P. (1994) Ammonium-nitrogen - a key regulatory factor causing dominance of non-nitrogen-fixing cyanobacteria in aquatic systems. Archiv für Hydrobiologie, 132, 141-164.
8. Blomqvist S., Gunnars A. & Elmgren R. (2004) Why the limiting nutrient differs between temperate coastal seas and freshwater lakes: a matter of salt. Limnology and Oceanography, 49, 2236-2241.
9. Boudreau B. & Westrich J. (1984) The dependence of bacterial sulfate reduction on sulfate concentration in marine sediments. Geochimica et Cosmochimica Acta, 48, 2503-2516.
10. Boukhalfa H. & Crumbliss A.L. (2002) Chemical aspects of siderophore mediated iron transport. BioMetals, 15, 325-339.
11. Brand L. (1991) Minimum iron requirements of marine phytoplankton and the implications for the biogeochemical control of new production. Limnology and Oceanography, 36, 1756-1771.
12. Brunberg A.-K. & Blomqvist P. (2003) Recruitment of Microcystis (Cyanophyceae) from lake sediments: the importance of littoral inocula. Journal of Phycology, 39, 58-63.
13. Bryant L.D., Lorrai C., McGinnis D.F., Brand A., Wüest A. & Little J.C. (2010) Variable sediment oxygen uptake in response to dynamic forcing. Limnology and Oceanography, 55, 950-964.
14. Callieri C., Modenutti B., Queimalinos C., Bertoni R. & Balseiro E. (2007) Production and biomass of picophytoplankton and larger autotrophs in Andean ultraoligotrophic lakes: differences in light harvesting efficiency in deep layers. Aquatic Ecology, 41, 511-523.
15. Callieri C. & Stockner J.G. (2002) Freshwater autotrophic picoplankton: a review. Journal of Limnology, 61, 1-14.
16. Camacho A., Garcia-Pichel F., Vicente E. & Castenholz R.W. (1996) Adaptation to sulfide and to the underwater light field in three cyanobacterial isolates from Lake Arcas (Spain). FEMS Microbiology Ecology, 21, 293-301.
17. Camacho A., Vicente E. & Miracle M. (2000) Ecology of a deep-living Oscillatoria (=Planktothrix) population in the sulphide-rich waters of a Spanish karstic lake. Archiv für Hydrobiologie, 148, 333-355.
18. Caraco N.F., Cole J.J. & Likens G.E. (1990) A comparison of phosphorus immobilization in sediments of freshwater and coastal marine systems. Biogeochemistry, 9, 277-290.
19. Carey C.C., Weathers K.C. & Cottingham K.L. (2008) Gloeotrichia echinulata blooms in an oligotrophic lake: helpful insights from eutrophic lakes. Journal of Plankton Research, 30, 893-904.
20. Carignan R. & Tessier A. (1988) The co-diagenesis of sulfur and iron in acid lake sediments of southwestern Québec. Geochimica Cosmochmica Acta, 52, 1179-1188.
21. Cavender-Bares K., Mann E., Chisholm S., Ondrusek M. & Bidigare R. (1999) Differential response of equatorial Pacific phytoplankton to iron fertilization. Limnology and Oceanography, 44, 237-246.
22. Codd G.A., Azevrdo S.M.F.O., Bagchi S.N., Burch M.D., Carmichael W.W., Harding W.R. et al. (2005) CYANONET. A global network for cyanobacterial bloom and toxin risk assessment. Initial situation assessment and recommendations. IHP-VI Technical Documents in Hydrology No. 76, UNESCO, Paris.
23. Cole J.J., Lane J., Marino R. & Howarth R. (1993) Molybdenum assimilation by cyanobacteria and phytoplankton in fresh-water and salt-water. Limnology and Oceanography, 38, 25-35.
24. Conley D.J., Paerl H.W., Howarth R.W., Boesch D.F., Seitzinger S.P., Havens K.E. et al. (2009) Controlling eutrophication: nitrogen and phosphorus. Science, 323, 1014-1015.
25. Cook R.B. (1984) Distributions of ferrous iron and sulfide in an anoxic hypolimnion. Canadian Journal of Fisheries and Aquatic Sciences, 41, 286-293.
26. Cooke G.D., Welch E.B., Martin A.B., Fulmer D.G., Hyde J.B. & Schrieve G.D. (1993) Effectiveness of Al, Ca, and Fe salts for control of internal phosphorus loading in shallow and deep lakes. Hydrobiologia, 253, 323-335.
27. 59Fe scavenging. Limnology and Oceanography, 38, 1554-1561.
28. Dang T.C., Fujii M., Rose A.L., Bligh M. & Waite T.D. (2012) Characteristics of the freshwater cyanobacterium Microcystis aeruginosa grown in iron-limited continuous culture. Applied and Environmental Microbiology, 78, 1574-1583.
29. Davison W. (1993) Iron and manganese in lakes. Earth-Science Reviews, 34, 119-163.
30. Downing J.A., Watson S.B. & McCauley E. (2001) Predicting cyanobacteria dominance in lakes. Canadian Journal of Fisheries and Aquatic Sciences, 58, 1905-1908.
31. Emerson S. & Widmer G. (1978) Early diagenesis in anaerobic lake sediments - II. Thermodynamic and kinetic factors controlling the formation of iron phosphate. Geochimica et Cosmochimica Acta, 42, 1307-1316.
32. Futter M.N. (2003) Patterns and trends in southern Ontario lake ice phenology. Environmental Monitoring and Assessment, 88, 431-444.
33. Garlick S., Oren A. & Padan E. (1977) Occurrence of facultative anoxygenic photosynthesis among filamentous and unicellular cyanobacteria. Journal of Bacteriology, 129, 623-629.
34. Gervais F., Siedel U., Heilmann B., Weithoff G., Heisig-Gunkel G. & Nicklisch A. (2003) Small-scale vertical distribution of phytoplankton, nutrients and sulphide below the oxycline of a mesotrophic lake. Journal of Plankton Research, 25, 273-278.
35. Ghassemi M. & Christman R.F. (1968) Properties of the yellow organic acids of natural waters. Limnology and Oceanography, 13, 583-597.
36. Gibbs M.M., Hickey C.W. & Özkundakci D. (2011) Sustainability assessment and comparison of efficacy of four P-inactivation agents for managing internal phosphorus loads in lakes: sediment incubations. Hydrobiologia, 658, 253-275.
37. Glass J.B., Wolfe-Simon F.W. & Anbar A.D. (2009) Coevolution of metal availability and nitrogen assimilation in cyanobacteria and algae. Geobiology, 7, 100-123.
38. Harrington J.M. & Crumbliss A.L. (2009) The redox hypothesis in siderophore-mediated iron uptake. BioMetals, 22, 679-689.
39. Havens K.E. (2008) Cyanobacteria blooms: effects on aquatic ecosystems. Advances in Experimental Medicine and Biology, 619, 733-747.
40. Havens K.E., James R., East T. & Smith V. (2003) N: P ratios, light limitation, and cyanobacterial dominance in a subtropical lake impacted by non-point source nutrient pollution. Environmental Pollution, 122, 379-390.
41. Head R.M., Jones R.I. & Bailey-Watts A.E. (1999a) An assessment of the influence of recruitment from the sediment on the development of planktonic populations of cyanobacteria in a temperate mesotrophic lake. Freshwater Biology, 41, 759-769.
42. Head R.M., Jones R.I. & Bailey-Watts A.E. (1999b) Vertical movements by planktonic cyanobacteria and the translocation of phosphorus: implications for lake restoration. Aquatic Conservation: Marine and Freshwater Ecosystems, 9, 111-120.
43. Hecky R.E., Campbell P. & Hendzel L. (1993) The stoichiometry of carbon, nitrogen, and phosphorus in particulate matter of lakes and oceans. Limnology and Oceanography, 38, 709-724.
44. Hecky R.E. & Kilham P. (1988) Nutrient limitation of phytoplankton in freshwater and marine environments: a review of recent evidence on the effects of enrichment. Limnology and Oceanography, 33(4, part 2), 796-822.
45. Hopkinson B.M. & Morel F.M.M. (2009) The role of siderophores in iron acquisition by photosynthetic marine microorganisms. BioMetals, 22, 659-669.
46. Howarth R.W., Marino R., Lane J.M. & Cole J.J. (1988) Nitrogen-fixation in fresh-water, estuarine, and marine ecosystems. 1. Rates and importance. Limnology and Oceanography, 33, 669-687.
47. Hudnell H.K., Jones C., Labisi B., Lucero V., Hill D.R. & Eilers J. (2010) Freshwater harmful algal bloom (FHAB) suppression with solar powered circulation (SPC). Harmful Algae, 9, 208-217.
48. Ibelings B.W., Mur L.R. & Walsby A.E. (1991) Diurnal changes in buoyancy and vertical distribution in populations of Microcystis in two shallow lakes. Journal of Plankton Research, 13, 419-436.
49. Jancula D. & Maršálek B. (2011) Critical review of actually available chemical compounds for prevention and management of cyanobacterial blooms. Chemosphere, 85, 1415-1422.
50. Jensen H. & Andersen F. (1992) Importance of temperature, nitrate, and pH for phosphate release from aerobic sediments of 4 shallow, eutrophic lakes. Limnology and Oceanography, 37, 577-589.
51. Jensen H. & Thamdrup B. (1993) Iron-bound phosphorus in marine-sediments as measured by bicarbonate-dithionite extraction. Hydrobiologia, 253, 47-59.
52. Jeppesen E., Sondergaard M., Jensen J., Havens K., Anneville O., Carvalho L. et al. (2005) Lake responses to reduced nutrient loading - an analysis of contemporary long-term data from 35 case studies. Freshwater Biology, 50, 1747-1771.
53. Katsev S., Tsandev I., L'Heureux I. & Rancourt D.G. (2006) Factors controlling long-term phosphorus efflux from lake sediments: exploratory reactive-transport modeling. Chemical Geology, 234, 127-147.
54. Keating K. (1977) Allelopathic Influence on blue-green bloom sequence in a eutrophic lake. Science, 196, 885-887.
55. Keating K. (1978) Blue-green-algal inhibition of diatom growth - transition from mesotrophic to eutrophic community structure. Science, 199, 971-973.
56. Keeney D., Chen R. & Graetz D. (1971) Importance of denitrification and nitrate reduction in sediments to nitrogen budgets of lakes. Nature, 233, 66.
57. Klausmeier C.A., Lichtman E., Daufresne T. & Levin S.A. (2004) Optimal nitrogen-to-phosphorus stoichiometry of phytoplankton. Nature, 429, 171-174.
58. Kleeberg A., Herzog C. & Hupfer M. (2013) Redox sensitivity of iron in phosphorus binding does not impede lake restoration. Water Research, 47, 1491-1502.
59. Kranzler C., Lis H., Shaked Y. & Keren N. (2011) The role of reduction in iron uptake processes in a unicellular, planktonic cyanobacterium. Environmental Microbiology, 13, 2990-2999.
60. Kranzler C., Rudolf M., Keren N. & Schleiff E. (2013) Iron in cyanobacteria. Advances in Botanical Research, 65, 57-105.
61. Kusta A., Sañudo-Wilhemy S.A. & Carpenter E.J. (2003) Iron requirements for dinitrogen- and ammonium-supported growth in cultures of Trichodesmium (IMS 101): comparison with nitrogen fixation rates and iron:carbon ratios of field populations. Limnology and Oceanography, 48, 1869-1884.
62. Lewandowski J., Schauser I. & Hupfer M. (2003) Long term effects of phosphorus precipitations with alum in hypereutrophic Lake Süsser See (Germany). Water Research, 37, 3194-3204.
63. Lewis W.M. Jr & Wurtsbaugh W.A. (2008) Control of lacustrine phytoplankton by nutrients: erosion of the phosphorus paradigm. International Review of Hydrobiology, 93, 446-465.
64. Lewis W.M. Jr, Wurtsbaugh W.A. & Paerl H.W. (2011) Rationale for control of anthropogenic nitrogen and phosphorus to reduce eutrophication of inland waters. Environmental Science & Technology, 45, 10300-10305.
65. Loewen M.R., Ackerman J.D. & Hamblin F.F. (2007) Environmental implications of stratification and turbulent mixing in a shallow basin. Canadian Journal of Fisheries and Aquatic Sciences, 64, 43-57.
66. Loh P.S., Molot L.A., Nürnberg G.K., Watson S.B. & Ginn B. (2013) Evaluating relationships between sediment chemistry and anoxic phosphorus and iron release across three different water bodies. Inland Waters, 3, 105-118.
67. Maldonado M.T. & Price N.M. (1996) Influence of N substrate on Fe requirements of marine centric diatoms. Marine Ecology Progress Series, 141, 161-172.
68. Maldonado M.T. & Price N.M. (1999) Utilization of iron bound to strong organic ligands by plankton communities in the subarctic Pacific Ocean. Deep-Sea Research Part II-Topical Studies in Oceanography, 46, 2447-2473.
69. Mann E.L. & Chisholm S.W. (2000) Iron limits the cell division rate of Prochlorococcus in the eastern equatorial Pacific. Limnology and Oceanography, 45, 1067-1076.
70. Manning P.G., Murphy T.P. & Prepas E.E. (1991) Intensive formation of vivianite in the bottom sediments of mesotrophic Narrow Lake, Alberta. Canadian Mineralogist, 29, 77-85.
71. Maranger R., Bird D.F. & Price N.M. (1998) Iron acquisition by photosynthetic marine phytoplankton from ingested bacteria. Nature, 396, 248-251.
72. Marino R., Howarth R.W., Shamess J. & Prepas E.E. (1990) Molybdenum and sulfate as controls on the abundance of nitrogen-fixing cyanobacteria in saline lakes in Alberta. Limnology and Oceanography, 35, 245-259.
73. McKay R., Wilhelm S., Hall J., Hutchins D., Al-Rshaidat M., Mioni C. et al. (2005) Impact of phytoplankton on the biogeochemical cycling of iron in subantarctic waters southeast of New Zealand during FeCycle. Global Biogeochemical Cycles, 19, GB4S24.
74. McQueen D.J. & Lean D.R.S. (1987) Influence of water temperature and nitrogen to phosphorus ratios on the dominance of blue-green algae in Lake St-George, Ontario. Canadian Journal of Fisheries and Aquatic Sciences, 44, 598-604.
75. Michalak A.M., Anderson E.J., Beletsky D., Boland S., Bosch N.S., Bridgeman T.B. et al. (2013) Record-setting algal bloom in Lake Erie caused by agricultural and meteorological trends consistent with expected future conditions. Proceedings of the National academy of Sciences of the United States of America, 110, 6448-6452.
76. Millie D.F., Fahnenstiel G.L., Bressie J.D., Pigg R.J., Rediske R.R., Klarer D.M. et al. (2009) Late-summer phytoplankton in western Lake Erie (Laurentian Great Lakes): bloom distributions, toxicity, and environmental influences. Aquatic Ecology, 43, 915-934.
77. Molot L.A. & Brown E.J. (1986) Method for determining the temporal response of microbial phosphate-transport affinity. Applied and Environmental Microbiology, 51, 524-531.
78. Molot L.A. & Dillon P.J. (2003) Variation in iron, aluminum and dissolved organic carbon mass transfer coefficients in lakes. Water Research, 37, 1759-1768.
79. Molot L.A., Heintsch L. & Nicholls K.H. (1990) Responses of phytoplankton in acidic lakes in Ontario to whole-lake neutralization. Canadian Journal of Fisheries and Aquatic Sciences, 47, 422-431.
80. Molot L.A., Li G., Findlay D.L. & Watson S.B. (2010) Iron-mediated suppression of bloom-forming cyanobacteria by oxine in a eutrophic lake. Freshwater Biology, 55, 1102-1117.
81. 2 in aqueous solution - basic principles and a simple heuristic description. Chemosphere, 68, 2080-2084.
82. Murphy T., Lean D.R.S. & Nalewajko C. (1976) Blue-green algae - their excretion of iron-selective chelators enables them to dominate other algae. Science, 192, 900-902.
83. Neilands J. (1995) Siderophores - structure and function of microbial iron transport compounds. Journal of Biological Chemistry, 270, 26723-26726.
84. Nixon S.W., Ammerman J.W., Atkinson L.P., Berounsky V.M., Billen G., Boicourt W.C. et al. (1996) The fate of nitrogen and phosphorus at the land-sea margin of the North Atlantic Ocean. Biogeochemistry, 35, 141-180.
85. Nürnberg G.K. (2004) Quantified hypoxia and anoxia in lakes and reservoirs. The Scientific World Journal, 4, 42-54.
86. Nürnberg G.K. (2007) Low-Nitrate-Days (LND), a potential indicator of cyanobacteria blooms in a eutrophic hardwater reservoir. Water Quality Research Journal of Canada, 42, 269-283.
87. Ontario Ministry of Environment and Energy (1994) Water Management Policies Guidelines and Provincial Water Quality Objectives, Toronto, ON, Canada.
88. Paerl H.W. (1988) Nuisance phytoplankton blooms in coastal, estuarine and inland waters. Limnology and Oceanography, 33(4, part 2), 823-847.
89. Paerl H.W., Hall N.S. & Calandrino E.S. (2011a) Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Science of the Total Environment, 409, 1739-1745.
90. Paerl H.W. & Paul V.J. (2012) Climate change: links to global expansion of harmful cyanobacteria. Water Research, 46, 1349-1363.
91. Paerl H.W. & Scott J.T. (2010) Throwing fuel on the fire: synergistic effects of excessive nitrogen inputs and global warming on harmful algal blooms. Environmental Science & Technology, 44, 7756-7758.
92. Paerl H.W., Xu H., McCarthy M.J., Zhu G., Qin B., Li Y. et al. (2011b) Controlling harmful cyanobacterial blooms in a hyper-eutrophic lake (Lake Taihu, China): the need for a dual nutrient (N & P) management strategy. Water Research, 45, 1973-1983.
93. Paterson M.J., Schindler D.W., Hecky R.E., Findlay D.L. & Rondeau K.J. (2011) Comment: lake 227 shows clearly that controlling inputs of nitrogen will not reduce or prevent eutrophication of lakes. Limnology and Oceanography, 56, 1545-1547.
94. Powe C., Verschoor M., Molot L., Loh P.S., Watson S.B. & Howell T. (2013) Assessment of cyanobacteria dominance in embayments long the Georgian Bay coastline. Final report to Georgian Bay Forever, Caledon, ON, Canada (www.georgianbayforever.org). June 10, 2013.
95. Prepas E.E., Field K.M., Murphy T.P., Johnson W.L., Burke J.M. & Tonn W.M. (1997) Introduction to the Amisk Lake Project: oxygenation of a dee, eutrophic lake. Candian Journal of Fisheries and Aquatic Sciences, 54, 2105-2110.
96. Price N. (2005) The elemental stoichiometry and composition of an iron-limited diatom. Limnology and Oceanography, 50, 1159-1171.
97. Ramm K. & Scheps V. (1997) Phosphorus balance of a polytrophic shallow lake with the consideration of phosphorus release. Hydrobiologia, 342, 43-53.
98. Rautio M., Dufresne F., Laurion I., Bonilla S., Vincent W.F. & Christoffersen K.S. (2011) Shallow freshwater ecosystems of the circumpolar Arctic. Ecoscience, 18, 204-222.
99. Raven J.A. (1988) The iron and molybdenum use efficiencies of plant growth with different energy, carbon and nitrogen sources. New Phytologist, 109, 279-287.
100. Redfield A.C., Ketchum B.H. & Richards F.A. (1963) The influence of organisms on the composition of sea-water. In: The Sea (Ed M.N. Hill), pp. 26-77, Vol. 2, Interscience, New York, NY.
101. Scavia D., Lang G.A. & Kitchell J.F. (1988) Dynamics of Lake Michigan plankton: a model evaluation of nutrient loading, competition and predation. Canadian Journal of Fisheries and Aquatic Sciences, 45, 165-177.
102. Schindler D.W. & Hecky R.E. (2009) Eutrophication: more nitrogen data needed. Science, 324, 721-722.
103. Schindler D.W., Hecky R.E., Findlay D.L., Stainton M.P., Parker B.R., Paterson M.J. et al. (2008) Eutrophication of lakes cannot be controlled by reducing nitrogen input: results of a 37-year whole-ecosystem experiment. Proceedings of the National academy of Sciences of the United States of America, 105, 11254-11258.
104. Singleton V.L. & Little J.C. (2006) Designing hypolimnetic aeration and oxygenation systems - a review. Environmental Science & Technology, 40, 7512-7520.
105. Smith J.L., Boyer G.L. & Zimba P.V. (2008) A review of cyanobacterial odorous and bioactive metabolites: impacts and management alternatives in aquaculture. Aquaculture, 280, 5-20.
106. Smith R. & Kalff J. (1983) Competition for Phosphorus among co-occurring freshwater phytoplankton. Limnology and Oceanography, 28, 448-464.
107. Smith V. (1983) Low nitrogen to phosphorus ratios favor dominance by blue-green algae in Lake phytoplankton. Science, 221, 669-671.
108. Sommer U. (1993) Phytoplankton competition in Plußsee - a field test of the resource-ratio hypothesis. Limnology and Oceanography, 38, 838-845.
109. Sorichetti R.J., Creed I.F. & Trick C.G. (2014a) Evidence for iron-regulated cyanobacterial predominance in oligotrophic lakes. Freshwater Biology, 59, 679-691.
110. Sorichetti R.J., McLaughlin J.T., Creed I.F. & Trick C.G. (2014b) Suitability of a cytotoxicity assay for detection of potentially harmful compounds produced by freshwater bloom-forming algae. Harmful Algae, 31, 177-187.
111. Stainsby E.A., Winter J.G., Jarjanazi H., Paterson A.M., Evans D.O. & Young J.D. (2011) Changes in the thermal stability of Lake Simcoe from 1980 to 2008. Journal of Great Lakes Research, 37, 63-71.
112. Stal L., Staal M. & Villbrandt M. (1999) Nutrient control of cyanobacterial blooms in the Baltic Sea. Aquatic Microbial Ecology, 18, 165-173.
113. Steffensen D.A. (2008) Economic cost of cyanobacterial blooms. Advances in Experimental Medicine and Biology, 619, 855-865.
114. Sunda W.G. & Huntsman S.A. (1995) Iron uptake and growth limitation in oceanic and coastal phytoplankton. Marine Chemistry, 50, 189-206.
115. Sunda W.G., Swift D.G. & Huntsman S.A. (1991) Low iron requirement for growth in oceanic phytoplankton. Nature, 351, 55-57.
116. Tang D. & Morel F.M.M. (2006) Distinguishing between cellular and Fe-oxide-associated trace elements in phytoplankton. Marine Chemistry, 98, 18-30.
117. Taylor P. & Williams P. (1975) Theoretical studies on coexistence of competing species under continuous-flow conditions. Canadian Journal of Microbiology, 21, 90-98.
118. Tilman D., Kiesling R., Sterner R., Kilham S. & Johnson F. (1986) Green, bluegreen and diatom algae - taxonomic differences in competitive ability for phosphorus, silicon and nitrogen. Archiv für Hydrobiologie, 106, 473-485.
119. Titman D. (1976) Ecological competition between algae - experimental confirmation of resource-based competition theory. Science, 192, 463-465.
120. Tortell P.D., Maldonado M.T., Granger J. & Price N.M. (1999) Marine bacteria and biogeochemical cycling of iron in the oceans. FEMS Microbiology Ecology, 29, 1-11.
121. Tortell P.D., Maldonado M.T. & Price N.M. (1996) The role of heterotrophic bacteria in iron-limited ocean ecosystems. Nature, 383, 330-332.
122. Tovar-Sanchez A., Sañudo-Wilhemy S.A., Garcia-Vargas M., Weaver R.S., Popels L.C. & Hutchins D.A. (2003) A trace metal clean reagent to remove surface-bound iron from marine phytoplankton. Marine Chemistry, 82, 91-99.
123. Trimbee A. & Prepas E.E. (1988) Dependence of lake oxygen depletion rates on maximum oxygen storage in a partially meromictic lake in Alberta. Canadian Journal of Fisheries and Aquatic Sciences, 45, 571-576.
124. Tuit C., Waterbury J. & Ravizza G. (2004) Diel variation of molybdenum and iron in marine diazotrophic cyanobacteria. Limnology and Oceanography, 49, 978-990.
125. Twiss M., Auclair J. & Charlton M. (2000) An investigation into iron-stimulated phytoplankton productivity in epipelagic Lake Erie during thermal stratification using trace metal clean techniques. Canadian Journal of Fisheries and Aquatic Sciences, 57, 86-95.
126. Verschoor M.J. & Molot L.A. (2013) A comparison of three colorimetric methods of ferrous and total reactive iron measurement in freshwaters. Limnology and Oceanography: Methods, 11, 113-125.
127. Vincent W.F. & Quesada A. (2012) Cyanobacteria in high latitude lakes, rivers and seas. In: Ecology of Cyanobacteria II: Their Diversity in Space and Time (Ed. B.A. Whitton), pp. 371-385. DOI: 10.1007/978-94-007-3855-3_13. Springer Science+Business Media B.V., Dordrecht.
128. Voelker B., Morel F.M.M. & Sulzberger B. (1997) Iron redox cycling in surface waters: effects of humic substances and light. Environmental Science & Technology, 31, 1004-1011.
129. Vörös L., Callieri C., Balogh K. & Bertoni R. (1998) Freshwater picocyanobacteria along a trophic gradient and light quality range. Hydrobiologia, 370, 117-125.
130. Wagner F., Falkner R. & Falkner G. (1995) Information about previous phosphate fluctuations is stored via an adaptive response of the high-affinity phosphate-uptake system of the cyanobacterium Anacystis nidulans. Planta, 197, 147-155.
131. Walsby A.E. & McAllister G.K. (1987) Buoyancy regulation by Microcystis in Lake Okaro. New Zealand Journal of marine and Freshwater Research, 21, 521-524.
132. Walsby A.E., Utkilen H.C. & Johnsen I.J. (1983) Buoyancy changes of a red coloured Oscillatoria agardhii in Lake Gjersjoen, Norway. Archiv fur Hydrobiologie, 97, 18-38.
133. Walve J. & Larsson U. (2007) Blooms of Baltic Sea Aphanizomenon sp. (Cyanobacteria) collapse after internal phosphorus depletion. Aquatic Microbial Ecology, 49, 57-69.
134. Watson S.B., McCauley E. & Downing J.A. (1997) Patterns in phytoplankton taxonomic composition across temperate lakes of differing nutrient status. Limnology and Oceanography, 42, 487-495.
135. Welch E.B. & Schrieve G.D. (1994) Alum treatment effectiveness and longevity in shallow lakes. Hydrobiologia, 275, 423-431.
136. Wersin P., Höhner P., Giovani R. & Stumm W. (1991) Early diagenetic processes on iron transformations in a freshwater lake sediment. Chemical Geology, 90, 233-252.
137. Wilhelm S.W. (1995) Ecology of iron-limited cyanobacteria: a review of physiological responses and implications for aquatic systems. Aquatic Microbial Ecology, 9, 295-303.
138. Wilhelm S.W., Bullerjahn G.S., Eldridge M.L., Rinta-Kanto J.M., Poorvin L. & Bourbonniere R.A. (2006) Seasonal hypoxia and the genetic diversity of prokaryote populations in the central basin hypolimnion of Lake Erie: evidence for abundant cyanobacteria and photosynthesis. Journal of Great Lakes Research, 32, 657-671.
139. Wilhelm S.W. & Trick C.G. (1994) Iron-limited growth of cyanobacteria - multiple siderophore production is a common response. Limnology and Oceanography, 39, 1979-1984.
140. Winter J.G., DeSellas A.M., Fletcher R., Heintsch L., Morley A., Nakamoto L. et al. (2011) Algal blooms in Ontario, Canada: increases in reports since 1994. Lake and Reservoir Management, 27, 107-114.
141. Wisniewski R. (1999) Phosphate inactivation with iron chloride during sediment resuspension. Lakes & Reservoirs: Research and Management, 4, 65-73.
142. Xu H., Paerl H.W., Qin B., Zhu G. & Gao G. (2010) Nitrogen and phosphorus inputs control phytoplankton growth in eutrophic Lake Taihu, China. Limnology and Oceanography, 55, 420-432.
143. Zepp R., Faust B. & Hoigne J. (1992) Hydroxyl radical formation in aqueous reactions (pH 3-8) of iron(II) with hydrogen peroxide - the photo-Fenton reaction. Environmental Science & Technology, 26, 313-319.
144. Zhang Y. & Prepas E.E. (1996) Regulation of the dominance of planktonic diatoms and cyanobacteria in four eutrophic hardwater lakes by nutrients, water column stability, and temperature. Canadian Journal of Fisheries and Aquatic Sciences, 53, 621-633.