The role of environmental parameters in the structure of phytoplankton assemblages and cyanobacteria toxins in two hypereutrophic lakes

Hydrobiologia

Volumn 691, Issue 1, 2012, Pages 255-268

  Xie, L ^a   Rediske, R R ^a   Hong, Y ^a   O'Keefe, J ^a   Gillett, N D ^a   Dyble, J ^b   Steinman, A D ^a  

^a GRAND VALLEY STATE UNIVERSITY   (United States)

^b NOAA EARTH SYSTEM RESEARCH LABORATORY   (United States)

Author keywords

Cylindrospermopsis; Environmental parameters; Limnothrix; Microcystins; Planktothrix

Indexed keywords

COMMUNITY STRUCTURE; CONCENTRATION (COMPOSITION); CYANOBACTERIUM; ENVIRONMENTAL FACTOR; EUTROPHIC ENVIRONMENT; HYPERTROPHIC ENVIRONMENT; PHOSPHORUS; PHYTOPLANKTON; TEMPORAL DISTRIBUTION; TOXIN; WATER CHEMISTRY; WATERSHED;

MICHIGAN; MONA LAKE; SPRING LAKE [MICHIGAN]; UNITED STATES;

ANABAENA FLOS-AQUAE; CYANOBACTERIA; CYLINDROSPERMOPSIS; CYLINDROSPERMOPSIS RACIBORSKII; LIMNOTHRIX; PLANKTOTHRIX;

EID: 84861582755     PISSN: 00188158     EISSN: 15735117     Source Type: Journal    
DOI: 10.1007/s10750-012-1077-1     Document Type: Article

References (83)

1. APHA (American Public Health Association), 1998. Standard Methods for the Evaluation of Water and Wastewater, 20th ed. APHA, Washington, DC.
2. Barco, M., J. Rivera & J. Caixach, 2002. Analysis of cyanobacterial hepatotoxins in water samples by microbore reversed-phase liquid chromatography-electrospray ionisation mass spectrometry. Journal of Chromatography A 959: 103-111.
3. Biddanda, B., A. D. Steinman, L. Nemeth, R. Rediske, Y. Hong & S. Kendall, 2008. Nutrient bioassays of plankton biomass and metabolism in an urbanized drowned river-mouth lake, Mona Lake, Michigan. Journal of Freshwater Ecology 23: 41-53.
4. Blomqvist, P., A. Petterson & P. Hyenstrand, 1994. Ammonium-nitrogen: a key regulatory factor causing dominance of non-nitrogen fixing cyanobacteria in aquatic systems. Archiv für Hydrobiologie 132: 141-164.
5. Bouvy, M., D. Falca, M. Marinho, M. Pagano & A. Moura, 2000. Occurrence of Cylindrospermopsis (cyanobacteria) in 39 Brazilian tropical reservoirs during the 1998 drought. Aquatic Microbiology Ecology 23: 13-27.
6. Bray, J. R. & J. T. Curtis, 1957. An ordination of the upland forest communities of southern Wisconsin. Ecological Monographs 27: 325-349.
7. Briand, J. F., S. Jacquet, C. Bernard & J. F. Humbert, 2003. Health hazards for terrestrial vertebrates from toxic cyanobacteria in surface water. Veterinary Research 34: 361-377.
8. Briand, J. F., C. Leboulanger, J. F. Humbert, C. Bernard & P. Dufour, 2004. Cylindrospermopsis raciborskii (cyanobacteria) invasion at mid-latitudes: selection, wide physiological tolerance, or global warming? Journal of Phycology 40(2): 231-238.
9. Carmichael, W. W., 1992. Health effects of toxin-producing cyanobacteria: "the cyanohabs". Human and Ecological Risk Assessment 7: 1393-1407.
10. Chapin, D. M., L. C. Bliss & L. J. Bledsoe, 1991. Environmental regulation of nitrogen fixation in a high arctic lowland ecosystem. Canadian Journal of Botany 69(12): 2744-2755.
11. Chapman, A. D. & C. L. Schelske, 1997. Recent appearance of Cylindrospermopsis (cyanobacteria) in five hypereutrophic Florida lakes. Journal of Phycology 33: 191-195.
12. Chorus, I., 2001. Cyanotoxins, Occurrence, Causes, Consequences. Springer- Verlag KG, Berlin.
13. Chorus, I. & J. Bartram, 1999. Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management. E & FN Spon, London, United Kingdom.
14. Clarke, K. R., 1993. Non-parametric multivariate analysis of changes in community structure. Australian Journal Ecology 18: 117-143.
15. Conroy, J. D., E. L. Quinlan, D. D. Kane & D. A. Culver, 2007. Cylindrospermopsis in Lake Erie: testing its association with other cyanobacterial genera and major limnological parameters. Journal of Great Lakes Research 33: 519-535.
16. Cooke, G. D., E. B. Welch & S. A. Peterson, 1993. Restoration and Management of Lakes and Reservoirs, 2nd ed. Lewis Publishers, Boca Raton, FL.
17. Dyble, J., H. W. Paerl & B. A. Neilan, 2002. Genetic characterization of Cylindrospermopsis raciborskii (Cyanobacteria) isolated from diverse geographic origins based on nifH and cpcBA-IGS nucleotide sequence analysis. Applied and Environmental Microbiology 68(5): 2567-2571.
18. Dyble, J., G. L. Fahnenstiel, R. W. Litaker, D. F. Millie & P. A. Tester, 2008. Microcystin concentrations and genetic diversity of Microcystis in the lower Great Lakes. Environmental Toxicology 23(4): 507-516.
19. Evans, E. D., 1992. Mona, White and Muskegon Lakes in Muskegon County, Michigan. The 1950s to the 1980s. Michigan Department of Natural Resources. MI/DNR/SWR-92/261.
20. Falconer, I. R. & A. R. Humpage, 2005. Health risk assessment of cyanobacterial (blue-green algal) toxins in drinking water. International Journal of Environmental Research and Public Health 2: 43-50.
21. Fastner, J., I. Flieger & U. Neumann, 1998. Optimized extraction of microcystins from field samples-a comparison of different solvents and procedures. Water Research 10: 3177-3181.
22. Fastner, J., R. Heinze, A. R. Humpage, U. Mischke, G. K. Eaglesham & I. Chorus, 2003. Cylindrospermopsin occurrence in two German lakes and preliminary assessment of toxicity and toxin production of Cylindrospermopsis raciborskii (cyanobacteria) isolates. Toxicon 42: 313-321.
23. Fergusson, K. M. & C. P. Saint, 2003. Multiplex PCR assay for Cylindrospermopsis raciborskii and cylindrospermopsin-producing cyanobacteria. Environmental Toxicology 18: 120-125.
24. Francis, G., 1878. Poisonous Australian lake. Nature 18: 11-12.
25. Graneli, W., 1999. Internal phosphorus loading in Lake Ringsjon. Hydrobiologia 404: 19-26.
26. Hamilton, D. W., M. Riehle, W. Monaghan & A. S. G. Curtis, 2005. Articular chondrocyte passage number: influence on adhesion, migration, cytoskeletal organization and phenotype in response to nano- and micro-metric topography. Cell Biology International 29: 408-421.
27. Hillebrand, H., C.-D. Dürselen, D. Kirschtel, U. Pollingher & T. Zohary, 1999. Biovolume calculation for pelagic and benthic microalgae. Journal of Phycology 35: 403-424.
28. Hong, Y., A. D. Steinman, B. Biddanda, R. R. Rediske & G. Fahnenstiel, 2006. Occurrence of the toxin-producing cyanobacterium Cylindrospermopsis raciborskii in Mona and Muskegon Lakes, Michigan. Journal of Great Lakes Research 32: 645-652.
29. Istvanovics, V., H. M. Shafik, M. Presing & S. Juhos, 2000. Growth and phosphate uptake kinetics of the cyanobacterium, Cylindrospermopsis raciborskii (cyanophyceae) in throughflow cultures. Freshwater Biology 43(2): 257-275.
30. Jacoby, J. M., D. C. Collier, E. B. Welch, F. J. Hardy & M. Crayton, 2000. Environmental factors associated with a toxic bloom of Microcystis. aeruginosa. Canadian Journal of Fisheries and Aquatic Sciences 57: 231-240.
31. Jiang, Y., B. Ji, R. N. S. Wong & M. H. Wong, 2008. Statistical study of the effects of environmental factors on the growth and microcystins production of bloom-forming cyanobacterium-Microcystis aeruginosa. Harmful Algae 7: 127-136.
32. Kahru, M., J. M. Leppänen, O. Rud & O. P. Savchuk, 2000. Cyanobacteria blooms in the Gulf of Finland triggered by saltwater inflow into the Baltic Sea. Marine Ecology Progress Series 207: 13-18.
33. Kirk, J. T. O., 1994. Light and Photosynthesis in Aquatic Ecosystems. Cambridge University Press, Melbourne, Australia.
34. Köhler, J. & S. Hoeg, 2000. Phytoplankton selection in a river-lake system during two decades of changing nutrient supply. Hydrobiologia 424: 13-24.
35. Kotak, B. G., A. K. Y. Lam, E. E. Prepas, S. L. Kenefick & S. E. Hrudey, 1995. Variability of the hepatotoxin, microcysin-LR in hypereutrophic drinking water lakes. Journal of Phycology 31: 248-263.
36. Kotak, B. G., A. K. Y. Lam, E. E. Prepas & S. E. Hrudey, 2000. Role of chemical and physical variables in regulating microcystin-LR concentration in phytoplankton of eutrophic lakes. Canadian Journal of Fisheries and Aquatic Sciences 57: 1584-1593.
37. Likens, G. E., 1972. Nutrients, Eutrophication. American Society Limnology & Oceanography Special Symposium, Vol. 1.
38. Long, B. M., G. J. Jones & P. T. Orr, 2001. Cellular microcystin content in n-limited Microcystis aeruginosa can be predicted from growth rate. Applied and Environmental Microbiology 67: 278-283.
39. Nicklisch, A., 1994. Does mortality by nitrogen deficiency influence the succession of Limnothrix redekei and Planktothrix agardhii. Verhandlungen des Internationalen Verein Limnologie 25: 2214-2217.
40. Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, R. B. O'Hara, G. L. Simpson, P. Solymos, M. Henry, H. Stevens & H. Wagner, 2009. Vegan: Community Ecology Package. R Package Version 1. 15-23. (URL http://vegan.r-forge.r-project.org).
41. Oliver, R. L. & G. G. Ganf, 2000. Freshwater blooms. In Whitton, B. A. & M. Potts (eds), The Ecology of Cyanobacteria Their Diversity in Time and Space. Kluwer Academic Publishers, Dordrecht, The Netherlands: 149-194.
42. Orr, P. T. & G. J. Jones, 1998. Relationship between microcystin production and cell division rates in nitrogen limited Microcystis aeruginosa cultures. Limnology & Oceanography 43: 1604-1614.
43. Osswald, J., S. Rellán, A. Gago & V. Vasconcelos, 2007. Toxicology and detection methods of the alkaloid neurotoxin produced by cyanobacteria, anatoxin-a. Environmental International 33: 1070-1089.
44. Padisák, J., 1997. Cylindrospermopsis raciborskii (Woloszynska) Seenayya et Subba Raju, an expanding, highly adaptive cyanobacterium: worldwide distribution and review of its ecology. Archiv für Hydrobiologie/Supplement 107: 563-593.
45. Paerl, H. W., 1988. Nuisance phytoplankton blooms in coastal, estuarine and inland waters. Limnology & Oceanography 33: 823-847.
46. Paerl, H. W., 1996. Microscale physiological and ecological studies of aquatic cyanobacteria: macroscale implications. Microsystems Research Technology 33: 47-72.
47. Paerl, H. W. & J. Ustach, 1982. Blue-green algal scums: an explanation for their occurrence during freshwater blooms. Limnology & Oceanography 27: 212-217.
48. Paerl, H. W., R. S. Fulton III, P. H. Moisander & J. Dyble, 2001. Harmful freshwater algal blooms, with an emphasis on cyanobacteria. Scientific World 1: 76-113.
49. Pearson, M. J., A. J. D. Ferguson, G. A. Codd, C. S. Reynolds, J. K. Fawell, R. M. Hamilton, S. R. Howard & M. R. Attwood, 1990. Toxic Blue-Green Algae. Water Quality Series. No. 2. National Rivers Authority, London, England.
50. Posselt, A. J., M. A. Burford & G. Shaw, 2009. Pulses of phosphate promote dominance of the toxic cyanophyte Cylindrospermopsis raciborskii in a subtropical water reservoir. Journal of Phycology 45: 540-546.
51. Preußel, K., A. Stuken, C. Wiedner, I. Chorus & J. Fastner, 2006. First report on cylindrospermopsin producing Aphanizomenon flos-aquae (Cyanobacteria) isolated from two German lakes. Toxicon 47: 156-162.
52. R Development Core Team, 2008. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. (URL http://www.R-project.org).
53. Reynolds, C. S., 1987. Cyanobacterial water-blooms. In Callow, J. A. (ed.), Advances in Botanical Research, Vol. 13. Academic Press, London: 67-143.
54. Reynolds, C. S., 1992. Eutrophication and the management of planktonic algae: what Vollenweider couldn't tell us. In Sutcliffe, D. W. & J. G. Jones (eds), Eurtrophication: Research and Application to Water Supply. Freshwater Biological Association, Ambleside, UK: 4-29.
55. Rinta-Kanto, J. M., E. A. Konopko, J. M. DeBruyn, R. A. Bourbonniere, G. L. Boyer & S. W. Wilhelm, 2009. Lake Erie Microcystis: relationship between microcystin production, dynamics of genotypes and environmental parameters in a large lake. Harmful Algae 8: 665-673.
56. Roji, C. & M. Alvarez Cobelas, 1994. Population dynamics of Limnothrix redekei, Oscillatoria lanceaformis, Planktorix agardhii and Pseudanabaena limnetica (cyanobacteria) in a shallow hypertrophic shallow hypertrophic lake (Spain). Hydrobiologia 276: 165-171.
57. Rücker, J., C. Wiedner & P. Zippel, 1997. Factors controlling the dominance of Planktothrix agardhii and Limnothrix redekei in eutrophic shallow lakes. Hydrobiologia 342(343): 107-115.
58. Rücker, J., A. Stuken, B. Nixdorf, J. Fastner, I. Chorus & C. Wiedner, 2007. Concentrations of particulate and dissolved cylindrospermopsin in 21 Aphanizomenon-dominated temperate lakes. Toxicon 50: 800-809.
59. Sas, H., 1989. Lake Restoration by Reduction of Nutrient Loading: Expectations, Experiences, Extrapolations. St. August in: Academia Verlag Richarz: 497 pp.
60. Schembri, M. A., B. A. Neilan & C. P. Saint, 2001. Identification of genes implicated in toxin production in the cyanobacterium Cylindrospermopsis raciborskii. Environmental Toxicology 16(5): 413-421.
61. Seip, K. L., H. Sas & S. Vermu, 1992. Nutrient-chlorophyll trajectories across trophic gradents. Aquatic Sciences 54: 58-76.
62. Spencer, C. N. & D. L. King, 1989. Role of light, carbon dioxide and nitrogen in regulation of buoyancy, growth and bloom formation of Anabaena flos-aquae. Journal of Plankton Research 11: 283-296.
63. Steinman, A. D. & M. A. Ogdahl, 2008. Ecological effects following an alum treatment in Spring Lake, Michigan. Journal of Environmental Quality 37: 22-29.
64. Steinman, A. D., R. R. Rediske & K. R. Reddy, 2004. The reduction of internal phosphorus loading using alum in Spring Lake, Michigan. Journal of Environmental Quality 33: 2040-2048.
65. Steinman, A. D., R. R. Rediske, X. Chu, R. Denning, L. Nemeth, D. Uzarski, B. Biddanda & M. Luttenton, 2006a. An environmental assessment of an impacted, urbanized watershed: The Mona Lake Watershed, Michigan. Archive für Hydrobiologie 166: 117-144.
66. Steinman, A. D., L. Nemeth, E. Nemeth & R. R. Rediske, 2006b. Factors influencing internal P loading in a western Michigan, drowned river-mouth lake. Journal of the North American Benthologcial Society 25(2): 304-312.
67. Steinman, A. D., X. Chu & M. Ogdahl, 2009. Spatial and temporal variability of internal and external phosphorus loads in Mona Lake, Michigan. Aquatic Ecology 43: 1-18.
68. Stone, D. & W. Bress, 2007. Addressing public health risks for cyanobacteria in recreational freshwaters: the Oregon and Vermont framework. Integrated Environmental Assessment and Management 3(1): 137-143.
69. Sutherland, T. F., C. Leonard & F. J. R. Taylor, 1992. A segmented pipe sampler for integrated profiling of the upper water column. Journal of Plankton Research 14: 915-923.
70. Tonk, L., P. M. Visser, G. Christiansen, E. Dittmann, E. O. F. M. Snelder, C. Wiedner, L. R. Mur & J. Huisman, 2005. The microcystin composition of the cyanobacterium Planktothrix agardhii changes toward a more toxic variant with increasing light intensity. Applied and Environmental Microbiology 71(9): 5177-5181.
71. USEPA, 1983. Methods for Chemical Analysis of Water and Wastes. U. S. Environmental Protection Agency, Cincinnati, OH. EPA-600-/4-79-020.
72. USEPA, 1997a. Lake Michigan Mass Balance Method 086. Chlorophyll-Spectrophotometric Method. Great Lakes National Program Office, United States Environmental Protection Agency, Chicago, IL.
73. USEPA, 1997b. Lake Michigan Mass Balance Method 087. Standard Operating Procedure for Phytoplankton Analysis. Great Lakes National Program Office. United States Environmental Protection Agency, Chicago, IL.
74. Vidal, L. & C. Kruk, 2008. Cylindrospermopsis raciborskii (Cyanobacteria) extends its distribution to Latitude 34°53′S: taxonomical and ecological features in Uruguayan eutrophic lakes. Pan-American Journal of Aquatic Sciences 3: 142-151.
75. Vollenweider, R. A. & J. J. Kerekes, 1982. Eutrophication of waters: monitoring, assessment and control. OECD Cooperative programme on monitoring of inland waters (Eutrophication Control), Environment Directorate, OECD, Paris: 154 pp.
76. Watanabe, M. F. & S. Oishi, 1985. Effects of environmental factors on toxicity of a cyanobacterium (Microcystis aeruginosa) under culture conditions. Applied and Environmental Microbiology 49: 1342-1344.
77. WHO, 1999. In Chorus, I. & J. Bartram (eds.), Toxic Cyanobacteria in Water: A Guide to Their Public Health Consequences, Monitoring and Management. World Health Organization, Geneva, Switzerland. Spon Press, London.
78. Xie, L., P. Xie & H. J. Tang, 2003. Enhancement of dissolved phosphorus release from sediment to lake water by Microcystis blooms-an enclosure experiment in a hyper-eutrophic, subtropical Chinese lake. Environmental Pollution 112(3): 391-399.
79. Xie, L., J. Hagar, R. Rediske, J. O'Keefe, J. Dyble & A. D. Steinman, 2011. The influence of environmental conditions and hydrologic connectivity on cyanobacteria assemblages in two drowned river mouth lakes. Journal of Great Lakes Research. doi: 10. 1016/j. jglr. 2011. 05. 002.
80. Yéprémian, C., M. F. Gugger, E. Briand, A. Catherine, C. Berger, C. Quiblier & C. Bernard, 2007. Microcystins ecotypes in a perennial Planktothrix agardhii bloom. Water Research 41: 4446-4456.
81. Yilmaz, M., E. J. Phlips, N. J. Szabo & S. Badylak, 2008. A comparative study of Florida strains of Cylindrospermopsis and Aphanizomenon for cylindrospermopsin production. Toxicon 51: 130-139.
82. Zevenboom, W. & L. R. Mur, 1980. N2-fixing Cyanobacteria: why they do not become dominant in Dutch, hypertrophic lakes. In Barica, J. & L. R. Mur (eds), Hypertrophic Ecosystems. Developments in Hydrobiology 2. Dr W. Junk Publishers, The Hague: 123-130.
83. Zurawell, R. W., H. Chen, J. Bruke & E. E. Prepas, 2005. Hepatotoxic cyanobacteria: a review of the biological importance of microcystins in freshwater environments. Journal of Toxicology Environmental Health, Part B: Critical Reviews 8: 1-37.