Cladophora in the Great Lakes: Impacts on beach water quality and human health

Water Science and Technology

Volumn 62, Issue 1, 2010, Pages 68-76

  Verhougstraete, M P ^a   Byappanahalli, M N ^b   Rose, J B ^a   Whitman, R L ^b  

^a MICHIGAN STATE UNIVERSITY   (United States)

^b US Geological Survey's   (United States)

Author keywords

Cladophora; Great lakes; Indicator bacteria; Public health; Recreational water quality

Indexed keywords

CLADOPHORA; GREAT LAKES; INDICATOR BACTERIA; PUBLIC HEALTH; RECREATIONAL WATER QUALITY;

BACTERIA; BACTERIOLOGY; BEACHES; ESCHERICHIA COLI; HEALTH; LAKES; WATER ANALYSIS; WATER QUALITY;

WATER POLLUTION;

BEACH; COLIFORM BACTERIUM; ENVIRONMENTAL FACTOR; GREEN ALGA; HEALTH POLICY; LITERATURE REVIEW; PUBLIC HEALTH; RECREATIONAL FACILITY; SEASONALITY; WATER QUALITY;

BACTERIAL GROWTH; BACTERIAL SURVIVAL; CAMPYLOBACTER; CLADOPHORA; ESCHERICHIA COLI; FECES; GREEN ALGA; LAKE; MICROBIAL ACTIVITY; NONHUMAN; PERIPHYTON; REVIEW; SALMONELLA; SEASHORE; SHIGELLA; WATER CONTAMINATION; WATER POLLUTION; WATER QUALITY; ARTICLE; HUMAN; MICROBIOLOGY; STANDARD; SWIMMING; UNITED STATES;

GREAT LAKES [NORTH AMERICA];

ALGAE; BACTERIA (MICROORGANISMS); CAMPYLOBACTER; CLADOPHORA; ENTEROBACTERIACEAE; ESCHERICHIA COLI; SALMONELLA; SHIGELLA;

FRESH WATER;

ALGAE, GREEN; BATHING BEACHES; FRESH WATER; GREAT LAKES REGION; HUMANS; WATER POLLUTION;

EID: 77957288001     PISSN: 02731223     EISSN: None     Source Type: Journal    
DOI: 10.2166/wst.2010.230     Document Type: Review

References (43)

1. Alderisio, K. A. & DeLuca, N. 1999 Seasonal enumeration of fecal coliform bacteria from the feces of ring-billed gulls (Larus delawarensis) and Canada geese (Branta canadensis). Appl. Environ. Microbiol. 65, 5628-5630.
2. Alm, E., Burke, J. & Spain, A. 2003 Fecal indicator bacteria are abundant in wet sand at freshwater beaches. Water Res. 37, 3978-3982.
3. Alm, E. W., Burke, J. & Hagan, E. 2006 Persistence and potential growth of the fecal indicator bacteria, Escherichia coli, in shoreline sand at Lake Huron. J. Great Lakes Res. 32, 401-405.
4. Beversdorf, L. J., Bornstein-Forst, S. M. & McLellan, S. L. 2007 The potential for beach sand to serve as a reservoir for Escherichia coli and the physical influences on cell die-off. J. Appl. Microbiol. 102, 1372-1381.
5. Blum, J. L. 1982 Colonization and growth of attached algae at the Lake Michigan water line. J. Great Lakes Res. 8, 10-15.
6. Bootsma, H., Young, E. B. & Berges, J. A. 2005 Temporal and spatial patterns of Cladophora bio-mass and nutrient stoichiometry in Lake Michigan. Cladophora Research and Management in the Great Lakes: a Workshop at the Great Lakes WATER Institute, University of Wisconsin-Milwaukee, 8 December 2004.
7. Brettar, I. & Höfle, M. G. 1992 Influence of ecosystamatic factors on survival of E. coli after large-scale release into lake water mesocosms. Appl. Environ. Microbiol. 58, 2201-2210.
8. Byappanahalli, M. N. & Whitman, R. L. 2009 Clostridium botulinum type E occurs and grows in the alga Cladophora glomerata. Can. J. Fish. Aquat. Sci. 66, 879-882.
9. Byappanahalli, M. N., Shively, D. A., Nevers, M. B., Sadowsky, M. J. & Whitman, R. L. 2003a Growth and survival of Escherichia coli and enterococci populations in the macro-alga Cladophora (Chlorophyta). Fed. Eur. Microbiol. Soc. 46, 203-211.
10. Byappanahalli, M., Fowler, M., Shively, D. & Whitman, R. 2003b Ubiquity and persistence of Escherichia coli in a Midwestern coastal stream. Appl. Environ. Microbiol. 69, 4549-4555.
11. Byappanahalli, M. N., Whitman, R. L., Shively, D. A., Sadowsky, M. J. & Ishii, S. 2006 Population structure, persistence, and seasonality of autochthonous Escherichia coli in temperate, coastal forest soil from a Great Lakes watershed. Environ. Microbiol. 8, 504-513.
12. Byappanahalli, M. N., Whitman, R. L., Shively, D. A., Ferguson, J., Ishii, S. & Sadowsky, M. J. 2007 Population structure of Cladophora-borne E. coli in nearshore water of Lake Michigan. Water Res. 41, 3649-3654.
13. Byappanahalli, M. N., Sawdey, R., Ishii, S., Shively, D. A., Ferguson, J. A., Whitman, R. L. & Sadowsky, M. J. 2009 Seasonal stability of Cladophora-associated Salmonella in Lake Michigan watersheds. Water Res. 43, 806-814.
14. Chilton, E. W., Lowe, R. L. & Schurr, K. M. 1986 Invertebrate communities associated with Bangia atropirpurea and Cladophora glomerata in western Lake Erie. J. Great Lakes Res. 12, 149-153.
15. Chow-Fraser, P. 1998 A conceptual model to aid restoration of Cootes Paradise Marsh, a degraded coastal wetland of Lake Ontario, Canada. Wetlands Ecol. Manage. 6, 43-57.
16. Crowder, A. & Bristow, M. 1986 Aquatic macrophytes in the Bay of Quinte. Can. Spec. Publ. Fish. Aquat. Sci. 86, 114-127.
17. Dodds, W. K. & Gudder, D. A. 1992 The ecology of Cladophora. J. Phycol. 28, 415-427.
18. Englebert, E. T., McDermott, C. & Kleinheinz, G. T. 2008a Impact of alga Cladophora on the survival of E. coli, Salmonella, and Shigella in laboratory microcosm. J. Great Lakes Res. 34, 377-382.
19. Englebert, E. T., McDermott, C. & Kleinheinz, G. T. 2008b Effects of the nuisance algae, Cladophora, on Escherichia coli at recreation beaches in Wisconsin. Sci. Total Environ. 404, 10-17.
20. Garrido-Perez, M. C., Anfuso, E., Acevedo, A. & Perales-Vargas- Machuca, J. A. 2008 Microbial indicators of faecal contamination in waters and sediments of beach bathing zones. Int. J. Hyg. Environ. Health 211, 510-517.
21. Graham, L. E. 1982 Cytology, ultrastructure, taxonomy, and phylogenetic relationships of Great Lakes filamentous algae. J. Great Lakes Res. 8, 54-60.
22. Ishii, S. & Sadowsky, M. 2008 Escherichia coli in the environment: implications for water quality and human health. Microb. Environ. 23, 101-108.
23. Ishii, S., Yan, T., Shively, D. A., Byappanahalli, M. N., Whitman, R. L. & Sadowsky, M. J. 2006a Cladophora (Chlorophyta) spp. Harbor human bacterial pathogens in nearshore water of Lake Michigan. Appl. Environ. Microbiol. 72, 4545-4553.
24. Ishii, S., Ksoll, W. B., Hicks, R. E. & Sadowsky, M. J. 2006b Presence and growth of naturalized Escherichia coli in temperate soils from Lake Superior watersheds. Appl. Environ. Microbiol. 72, 612-621.
25. Ishii, S., Hansen, D. L., Hicks, R. E. & Sadowsky, M. J. 2007 Beach sand and sediments are temporal sinks and sources of Escherichia coli in Lake Superior. Environ. Sci. Technol. 41, 2203-2209.
26. Johnson, L. A. K., Brown, M. B., Carruthers, E. A., Ferguson, J. A., Dombek, P. E. & Sadowsky, M. J. 2004 Sample size, library composition, and genotypic diversity among natural populations of Escherichia coli from different animals influence accuracy of determining sources of fecal pollution. Appl. Environ. Microbiol. 70, 4478-4485.
27. Kinzelman, J. L., Whitman, R. L., Byappanahalli, M., Jackson, E. & Bagley, R. C. 2003 Evaluation of beach grooming techniques on Escherichia coli density in foreshore sand at North Beach, Racine, WI. Lake Reservoir Manage. 19, 349-354.
28. Kleinheinz, G. T. & Englebert, E. 2005 Cladophora and the beach: implications for public health in Cladophora Research and Management in the Great Lakes. Great Lakes Water Institute Special report No. 2005-01.
29. Ksoll, W. B., Ishii, S., Sadowsky, M. J. & Hicks, R. E. 2007 Presence and sources of fecal coliform bacteria in epilithic periphyton communities of Lake Superior. Appl. Environ. Microbiol. 73, 3771-3778.
30. Lougheed, V. L., Crosbie, B. & Chow-Fraser, P. 2001 Primary determinants of macrophyte community structure in 62 marshes across the Great Lakes basin: latitude, land use, and water quality effects. Can. J. Fish. Aquat. Sci. 58, 1603-1612.
31. Olapade, O. A., Depas, M. M., Jenson, E. T. & McLellan, S. L. 2006 Microbial communities and fecal indicator bacteria associated with Cladophora mats on beach sites along Lake Michigan shores. Appl. Environ. Microbiol. 72, 1932-1938.
32. Ricca, D. M. & Cooney, J. J. 1998 Coliphage and indicator bacteria in birds around Boston Harbor. J. Ind. Microbiol. Biotechnol. 21, 28-30.
33. Signoretto, C., Burlacchini, G., del Mar Lleo, M., Pruzzo, C., Zampini, M., Pane, L., Franzini, G. & Caepari, P. 2004 Adhesion of Enterococcus faecalis in the nonculturable state to plankton is the main mechanism responsible for persistence of this bacterium in both Lake and Seawater. Appl. Environ. Microbiol. 70, 6892-6896.
34. Taft, C. E. 1975 History of Cladophora in the Great Lakes. In: Shear, H. & Konasewich, D. E. (eds) Cladophora in the Great Lakes. Great lakes Research Advisory Board, International Joint Commission Regional Office, Windsor, Ontario, Canada, pp. 5-6.
35. United States Environmental Protection Agency 1986 Ambient Water Quality Criteria for Bacteria-1986. EPA 440/5-84-002. Office of Water, Regulations and Standards Criteria and Standards Division, Washington, DC.
36. United States Environmental Protection Agency 2009 Periphyton as Indicators. (web). http://www.epa.gov/bioindicators/html/periphyton.html. 2 August 2009.
37. Vital, M., Hammes, F. & Egil, T. 2008 Escherichia coli O157 can grow in natural freshwater at low carbon concentrations. Environ. Microbiol. 10, 2387-2396.
38. Wade, T. J., Calderon, R. L., Brenner, K. P., Sams, E., Beach, M., Haugland, R., Wymer, L. & Dufour, A. P. 2008 High sensitivity of children to swimming-associated gastrointestinal illness: results using a rapid assay of recreational water quality. Epidemiology 19, 375-383.
39. Weinbauer, M. G. & Höfle, M. G. 1998 Distribution and life strategies of two bacterial populations in a eutrophic lake. Appl. Environ. Microbiol. 64, 3776-3783.
40. Whitman, R. L. & Nevers, M. B. 2003 Foreshore sand as a source of Escherichia coli in nearshore water of a Lake Michigan beach. Appl. Environ. Microbiol. 69, 5555-5562.
41. Whitman, R. L., Shivel, D. A., Pawlik, H., Nevers, M. B. & Byappanahalli, M. N. 2003 Occurrence of E. coli and enterococci in Cladophora (Chlorophyta) in nearshore water and beach sand of Lake Michigan. Appl. Environ. Microbiol. 69, 4714-4719.
42. Whitman, R. L., Byers, S. E., Shively, D. A., Ferguson, D. M. & Byappanahalli, M. 2005 Occurrence and growth characteristics of Escherichia coli and enterococci within the accumulated fluid of the northern pitcher plant (Sarracenia purpurea L.). Can. J. Microbiol. 51, 1027-1037.
43. Whitman, R. L., Nevers, M. B. & Byappanahalli, M. N. 2006 Examination of the watershed-wide distribution of Escherichia coli along southern Lake Michigan: an integrated approach. Appl. Environ. Microbiol. 72, 7301-7310.