Increasing occurrence of the benthic filamentous cyanobacterium Lyngbya wollei: A symptom of freshwater ecosystem degradation

Freshwater Science

Volumn 33, Issue 2, 2014, Pages 606-618

  Hudon, Christiane ^a   Sève, Michèle De ^b   Cattaneo, Antonella ^c  

^a ENVIRONMENT CANADA   (Canada)

^b M A de Sève Consultants ^*  (Canada)

^c UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Benthic filamentous mats; Cyanobacteria; Geographical distribution; Lyngbya wollei; Metabolism; Metaphyton; Nuisance species; Proliferation; Toxins

Indexed keywords

CYANOBACTERIUM; ENVIRONMENTAL DEGRADATION; ESTHETICS; FISH; FRESHWATER ECOSYSTEM; GEOGRAPHICAL DISTRIBUTION; INVERTEBRATE; MACROPHYTE; METABOLISM; RECREATIONAL ACTIVITY; SPECIES OCCURRENCE; TOXIN;

CANADA; GREAT LAKES [NORTH AMERICA]; LAURENTIAN MOUNTAINS; QUEBEC [CANADA]; SAINT LAWRENCE RIVER;

EID: 84903594378     PISSN: 21619549     EISSN: 21619565     Source Type: Journal    
DOI: 10.1086/675932     Document Type: Article

References (84)

1. Ahern, K. S., C. R. Ahern, and J. W. Udy. 2008. In situ field experiment shows Lyngbya majuscula (cyanobacterium) growth stimulated by added iron, phosphorus and nitrogen. Harmful Algae 7:389-404.
2. Alaerts-Smeesters, E., and E. Magnin. 1974. Étude préliminaire du phytoplancton du lac Saint-Louis, élargissement du fleuve Saint-Laurent près de Montréal, Québec. Canadian Journal of Botany 52:489-501.
3. Albert, S., J. M. O'Neil, J. W. Udy, K. S. Ahern, C. M. O'Sullivan, and W. C. Dennison. 2005. Blooms of the cyanobacterium Lyngbya majuscula in coastal Queensland, Australia: Disparate sites, common factors. Marine Pollution Bulletin 51: 428-437.
4. Beer, S., W. Spencer, and G. Bowes. 1986. Photosynthesis and growth of the filamentous blue-green alga Lyngbya wollei in relation to its environment. Journal of Aquatic Plant Management 4:61-65.
5. Beer, S., W. E. Spencer, and G. Bowes. 1992. HCO3-use and evidence for a carbon concentrating process in the mat-forming cyanophyte Lyngbya birgei G.M. Smith. Aquatic Botany 42: 159-171.
6. Bishop, M. J., S. P. Powers, H. J. Porter, and C. H. Peterson. 2006. Benthic biological effects of seasonal hypoxia in a eutrophic estuary predate rapid coastal development. Estuarine Coastal and Shelf Science 70:415-422.
7. Bonilla, I., L. Bolanos, and P. Mateo. 1995. Interaction of boron and calcium in the cyanobacteria Anabaena and Synechococcus. Physiologia Plantarum 94:31-36.
8. Bridgeman, T. B., and W. A. Penamon. 2010. Lyngbya wollei in western Lake Erie. Journal of Great Lakes Research 36:167-171.
9. Bridgeman, T. B., J. D. Chaffin, D. D. Kane, J. D. Conroy, S. E. Panek, and P. M. Armenio. 2011. From river to lake: Phosphorus partitioning and algal community compositional changes in western Lake Erie. Journal of Great Lakes Research 38: 90-97.
10. Burkholder, J. M., P. M. Glibert, and H. M. Skelton. 2008. Mixotrophy, a major mode of nutrition for harmful algal species in eutrophic waters. Harmful Algae 8:77-93.
11. Burns, J. 2010. Toxic cyanobacteria in Florida waters. Chapter 5. Pages 127-137 in H. K. Hudnell (editor). Cyanobacterial harmful algal blooms: State of the science and research needs.
12. International Symposium on Cyanobacterial Harmful Algal Blooms (ISOC-HAB). Springer, Dordrecht, The Netherlands.
13. Camacho, F. A., and R. W. Thacker. 2006. Amphipod herbivory on the freshwater cyanobacterium Lyngbya wollei: Chemical stimulants and morphological defences. Limnology and Oceanography 51:1870-1875.
14. Capper, A., and V. J. Paul. 2008. Grazer interactions with four species of Lyngbya in southeast Florida. Harmful Algae 7: 717-728.
15. Capper, A., I. R. Tibbetts, J. M. O'Neil, and G. M. Shaw. 2005. The fate of Lyngbya majuscula toxins in three potential consumers. Journal of Chemical Ecology 31:1595-1606.
16. Capper, A., I. R. Tibbetts, J. M. O'Neil, and G. R. Shaw. 2006. Dietary selectivity for the toxic cyanobacterium Lyngbya majuscula and resultant growth rates in two species of opisthobranch mollusc. Journal of Experimental Marine Biology and Ecology 331:133-144.
17. Carmichael, W. W. 2001. Health effects of toxin-producing cyanobacteria: The CyanoHABs. Human Ecological Risk Assessment 7:1393-1407. (Pubitemid 33817358)
18. Carmichael, W. W., W. R. Evans, Q. Q. Yin, P. Bell, and L. Moczydlowski. 1997. Evidence for paralytic shellfish poisoning in the freshwater cyanobacterium Lyngbya wollei (Farlow ex Gomont) comb. nov. Applied and Environmental Microbiology 63:3104-3110. (Pubitemid 27337800)
19. Chorus, I., and J. Bartram. 1999. Toxic Cyanobacteria in water: A guide to their public health consequences, monitoring, and management. E&F Spon, London, UK.
20. Cowell, B. C., and C. Dawes. 2004. Growth and nitrate-nitrogen uptake by the cyanobacterium Lyngbya wollei. Journal of Aquatic Plant Management 42:69-71. (Pubitemid 39067220)
21. Cowell, B. C., and P. Silver Botts. 1994. Factors influencing the distribution, abundance and growth of Lynbya wollei in central Florida. Aquatic Botany 49:1-17. (Pubitemid 2151230)
22. Doyle, R., and R. M. Smart. 1995. Potential use of native aquatic plants for long-Term control of problem aquatic plants in Guntersville Reservoir, Alabama. Report 2: Competitive interactions between beneficial and nuisance species. Technical Report A-93-6. US Army Engineer Waterways Experiment Station, US Army Corps of Engineers, Vicksburg, Mississippi.
23. Doyle, R. D., and M. Smart. 1998. Competitive reduction of noxious Lyngbya wollei mats by rooted plants. Aquatic Botany 61:17-32. (Pubitemid 28268272)
24. Evans, J., A. Wilkie, J. Burkhardt, and R. Haynes. 2007. Rethinking exotic plants: Using citizen observation in a restoration proposal for Kings Bay, Florida. Ecological Restoration 25:199-210. (Pubitemid 47511976)
25. Farlow, W. G. 1877. Remarks on some algae found in the water supplies of the City of Boston. Bulletin of the Bussey Institute 2:75-80.
26. Fogg, G. E. 1969. The physiology of algal nuisance. Proceedings of the Royal Society London Series B: Biological Sciences 173:175-189.
27. Foss, A. J., E. J. Phlips, M. Yilmaz, and A. Chapman. 2012. Characterization of paralytic shellfish toxins from Lyngbya wollei dominated mats collected from two Florida springs. Harmful Algae 16:98-107.
28. Gélinas, M., A. Lajeunesse, C. Gagnon, and F. Gagné. 2013. Temporal and seasonal variation in acetylcholinesterase activity and glutathione-S-Transferase in amphipods collected in mats of Lyngbya wollei in the St Lawrence River (Canada). Ecotoxicology and Environmental Safety 94:54-59.
29. Gilby, B. L., D. D. Burfeind, and I. R. Tibbetts. 2011. Lyngbya majuscula blooms and the diet of small subtropical benthivorous fishes. Marine Biology 158:245-255.
30. Gomont, M. 1892. Monographie des Oscillatoriées. Annales de Sciences Naturelles Botaniques 15:263-368.
31. Gross, E. D., and D. F. Martin. 1996. Iron dependence of Lyngbya majuscula. Journal of Aquatic Plant Management 34:17-20.
32. Haney, J. F., J. J. Sasner, and M. Ikawa. 1995. Effects of products released by Aphanizomenon flos-Aquae and purified saxitoxin on the movements of Daphnia carinata feeding appendages. Limnology and Oceanography 40:263-272.
33. Hecky, R. E., R. F. H. Smith, D. R. Barton, S. J. Guildford, W. D. Taylor, M. N. Charlton, and T. Howell. 2004. The nearshore phosphorus shunt: A consequence of ecosystem engineering by dreissenids in the Laurentian Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 61:1285-1293. (Pubitemid 39623470)
34. Heffernan, J., D. M. Liebowitz, T. K. Frazer, J. M. Evans, and M. J. Cohen. 2010. Algal blooms and the nitrogen-enrichment hypothesis in Florida springs: Evidence, alternatives, and adaptive management. Ecological Applications 20:816-829.
35. Heisler, J., P. M. Glibert, J. M. Burkholder, D. M. Anderson, W. Cochlan, W. C. Dennison, Q. Dortch, C. J. Gobler, C. A. Heil, E. Humphries, A. Lewitus, R. Magnien, H. G. Marshall, K. Sellner, D. A. Stockwell, D. K. Stoecker, M. Suddleson. 2008. Eutrophication and harmful algal blooms: A scientific consensus. Harmful Algae 8:3-13.
36. Higgins, S. N., E. T. Howell, R. E. Hecky, R. E. Guildford, and S. J. Smith. 2005. The wall of green: The status of Cladophora glomerata on the northern shores of Lake Erie's eastern basin, 1995-2002. Journal of Great Lakes Research 31: 547-563.
37. Hudon, C., A. Cattaneo, A.-M. Tourville Poirier, P. Brodeur, P. Dumont, Y. Mailhot, J.-P. Amyot, S.-P. Despatie, and Y. de Lafontaine. 2012. Oligotrophication from wetland epuration alters the riverine trophic network and carrying capacity for fish. Aquatic Sciences 74:495-511.
38. Joyner, J. J., W. L. Litaker, and H. W. Pearl. 2008. Morphological and genetic evidence that the cyanobacterium Lyngbya wollei encompasses at least two species. Applied and Environmental Microbiology 74:3710-3717.
39. Kraufvelin, P., S. Salovius, H. Christie, F. E. Moy, R. Karez, and M. Pedersen. 2006. Eutrophication-induced changes in benthic algae affect behaviour and fitness of the marine amphipod Gammarus locusta. Aquatic Botany 84:199-209. (Pubitemid 43243788)
40. Kuffner, I. B., and V. J. Paul. 2001. Effects of nitrate, phosphate and iron on the growth of macroalgae and benthic cyanobacteria from Cocos lagoon, Guam. 2001. Marine Ecology Progress Series 222:63-72.
41. Lajeunesse, A., P. A. Segura, M. Gélinas, C. Hudon, K. Thomas, M. A. Quilliam, and C. Gagnon. 2012. Detection and confirmation of saxitoxin analogues in freshwater benthic Lyngbya wollei algae collected in the St Lawrence River (Canada) by liquid chromatography-Tandem mass spectrometry. Journal of Chromatography A 1219:93-103.
42. Lévesque, D., A. Cattaneo, C. Hudon, and P. Gagnon. 2012. Predicting the risk of proliferation of the benthic cyanobacterium Lyngbya wollei in the St. Lawrence River. Canadian Journal of Fisheries and Aquatic Sciences 69:1585-1595.
43. Lin, H.-J., and J.-J. Hung. 2004. Factors affecting macroalgal distribution in a eutrophic tropical lagoon in Taiwan. Marine Biology 144:653-664. (Pubitemid 38554836)
44. Macbeth, A. J. 2004. Investigation of an introduced subtropical alga (Lyngbya wollei) in Whiteshell Provincial Park, Manitoba. MSc Thesis, University of Manitoba, Winnipeg, Manitoba.
45. Mihali, T. K., W. W. Carmichael, and B. A. Neilan. 2011. A putative gene cluster from a Lyngbya wollei bloom that encodes paralytic shellfish toxin biosynthesis. PLoS One 6: E14657.
46. Miller, C. R. 1915. Fresh-water algae occurring in the vicinity of the island of Montréal. Canadian Record of Science 9: 391-425.
47. Mitrovic, S. M., R.L. Oliver, C. Rees, L. C. Bowling and R.T. Buckney. 2003. Critical flow velocities for the growth and dominance of Anabaena circinalis in some turbid freshwater rivers. Freshwater Biology 48:164-174. (Pubitemid 36093389)
48. Odum, H. T. 1957. Trophic structure and productivity of Silver Springs, Florida. Ecological Monographs 27:55-112.
49. O'Neil, J. M., T. W. Davis, M. A. Burford, and C. J. Gobler. 2012. The rise of harmful cyanobacteria blooms: The potential roles of eutrophication and climate change. Harmful Algae 14:313-334.
50. Onodera, H., M. Satake, Y. Oshima, T. Yasumoto, and W. Carmichael. 1997. New saxitoxin analogues form the freshwater filamentous cyanobacterium Lyngbya wollei. Natural Toxins 5:146-151. (Pubitemid 27514121)
51. Osborne, N. T., P. Webb, and G. R. Shaw. 2001. The toxins of Lyngbya majuscula and their human and ecological health effects. Environment International 27:381-392.
52. Paerl, H. W. 1990. Physiological ecology and regulation of N2 fixation in natural waters. Advances in Microbial Ecology 11: 305-344.
53. Paerl, H. W., and T. G. Otten. 2013. Harmful cyanobacterial blooms: Causes, consequences, and controls. Microbial Ecology 65:995-1010.
54. Panek, S. E. 2012. The ecology of the nuisance cyanobacterium, Lyngbya wollei, in the western basin of Lake Erie. MSc Thesis, University of Toledo, Toledo, Ohio.
55. Phlips, E. J., J. Ihnat, and M. Conroy. 1992. Nitrogen fixation by the benthic freshwater cyanobaterium Lyngbya wollei. Hydrobiologia 234:59-64.
56. Pinowska, A., R J. Stevenson, J. O. Sickman, A. Albertin, and M. Anderson. 2007. Integrated interpretation of survey for determining nutrient thresholds for macroalgae in Florida Springs. Laboratory experiments and disturbance study. Report to Florida Department of of Environmental Protection. Florida Department of Environmental Protection, Tallahassee, Florida. (Available from: Environmental Assessment Section, Florida Department of Environmental Protection, 2600 Blair Stone Rd. MS 6511, Tallahassee, Florida 32399 USA.)
57. Pittman, S., and K. Pittman. 2005. Short-Term consequences of a benthic cyanobacterial bloom (Lyngbya majuscula, Gomont) for fish and penaeid prawns in Moreton Bay (Queensland, Australia). Estuarine and Coastal Shelf Science 63:619-632.
58. Poulin, M., P. B. Hamilton, and M. Proulx. 1994. Catalogue des algues d'eau douce du Québec, Canada. Canadian Field Naturalist 109:27-110. (Pubitemid 26452205)
59. Scheffer, M., S. Rinaldi, A. Gragnani, L. R. Mur, and E. H. van Nes. 1997. On the dominance of filamentous cyanobacteria in shallow, turbid lakes. Ecology 78:272-282.
60. Schindler, D.W. 1977. Evolution of phosphorus limitation in lakes. Science 195:260-267.
61. Schopf, J. W. 2000. The fossil record: Tracing the roots of the cyanobacterial lineage. Pages 13-35 in B. A. Whitton and M. Potts (editors). The ecology of cyanobacteria. Kluwer Academic, Dordrecht, The Netherlands.
62. Seifert, M., G. McGregor, G. Eaglesham, W. Wickramasinghe, and G. Shaw. 2007. First evidence of cylindrospermopsin and deoxy-cylindrospermopsin by the freshwater benthic cyanobacterium Lyngbya wollei (Farlow ex Gomont) Speziale and Dyck. Harmful Algae 6:73-80 (Pubitemid 46038239)
63. Smith, V. H. 1985. Predictive models for the dominance of bluegreen algae in lakes. Water Research Bulletin 21:433-439.
64. Speziale, B. J., and L. C. Dyck. 1992. Lyngbya infestations: Comparative taxonomy of L. wollei comb. nov. (Cyanobacteria). Journal of Phycology 28:693-706.
65. Speziale, B. J., E. G. Turner, and L. C. Dyck. 1988. "Giant?" Lyngbya. Aquatics 10:4-11.
66. Speziale, B. J., E. G. Turner, and L. C. Dyck. 1991. Physiological characteristics of vertically stratified L. wollei mats. Lake Reservoir Management 7:107-114.
67. Stal, L. J. 1995. Physiological ecology of cyanobacteria in microbial mats and other communities. New Phytologist 131:1-32. (Pubitemid 26451531)
68. Stal, L. J., I. Severin and H. Bolhuis. 2010. The ecology of nitrogen fixation in cyanobacterial mats. Recent advances in phototrophic prokaryotes. Advances in Experimental Medicine and Biology 675:31-45.
69. Stevenson, R. J., A. Pinowska, A. Albertin, and O. J. Sickman. 2007. Ecological condition of algae and nutrients in Florida springs: The synthesis report. Report for contract WM8 58.
70. Florida Department of Environmental Protection, Tallahassee, Florida. (Available from: Environmental Assessment Section, Florida Department of Environmental Protection, 2600 Blair Stone Rd. MS 6511,Tallahassee, Florida 32399 USA.)
71. Tabachek, J. A. L., and M. Yurkowski. 1976. Isolation and identification of blue-green algae producing muddy odour metabolites, geosmin and 2-methylisoborneol in saline lakes in Manitoba. Journal of the Fisheries Research Board of Canada 33:25-35.
72. Taft, C. E. 1942. Additions to the algae of the west end of Lake Erie. Ohio Journal of Science 42:251-256.
73. Tall, L. 2012. Les transformations microbiennes de l'azote dans les grandes rivières. PhD Thesis, Université de Montréal, Montreal, Quebec.
74. Tourville Poirier, A. M. T., A. Cattaneo, and C. Hudon. 2010. Benthic cyanobacteria and filamentous chlorophytes affect macroinvertebrate assemblages in a large fluvial lake. Journal of the North American Benthological Society 29:737-749.
75. Turner, G. 1990. Studies on the biology of Lyngbya wollei. MSc Thesis, Clemson University, Clemson, South Carolina.
76. Vijayavel, K., M. J. Sadowsky J. A. Ferguson, and D. R. Kashian. 2013. The establishment of the nuisance cyanobacteria Lyngbya wollei in Lake St. Clair and its potential to harbor fecal indicator bacteria. Journal of Great Lakes Research (in press). doi: 10.1016/j.jglr.2013.09.018
77. Vis, C., A. Cattaneo, and C. Hudon. 2008. Shift from chlorophytes to cyanobacteria in benthic macroalgae along a gradient of nitrate depletion. Journal of Phycology 44:38-44. (Pubitemid 351225088)
78. Watkinson, A. J., J. M. O'Neil, and W. D. Dennison. 2005. Ecophysiology of the marine cyanobacterium, Lyngbya majuscula (Oscillatoriacea). Harmful Algae 4:697-715.
79. Watson, S. B. 2003. Cyanobacterial and eukaryotic algal odour compounds: Signals or by-products? A review of their biological activity. Phycologia 42:332-350. (Pubitemid 37124077)
80. Watson, S. B., J. Ridal, and G. L. Boyer. 2008. Taste and odour and cyanobacterial toxins: Impairment, prediction, and management in the Great Lakes. Canadian Journal of Fisheries and Aquatic Sciences 65:1779-1796.
81. Wehr, J. D., and R. G. Sheath (editors). 2003. Freshwater algae of North America-ecology and classification. Academic Press, San Diego, California.
82. Whitton, B. A. 1967. Phosphate accumulation by colonies of Nostoc. Plant Cell Physiology 8:293-296.
83. Wolle, F. 1887. Freshwater algae of the United States. Comenius Press, Bethlehem, Pennsylvania.
84. Yin, Q., W. Carmichael, and W. R. Evans. 1997. Factors influencing growth and toxin production by cultures of the freshwater cyanobacterium Lyngbya wollei Farlow ex Gomont. Journal of Applied Phycology 9:55-63.