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Environmental Influences on Faecal Indicator Organisms in Coastal Waters and Their Accumulation in Bivalve Shellfish

Estuaries and Coasts volume 36, pages 834–853 (2013)Cite this article

Abstract

Shellfish production areas are often located in shallow estuarine and coastal systems impacted by fluxes of faecal indicator organisms (FIOs) that exhibit extreme spatial and temporal variability. FIO abundance and distribution in the marine environment are determined by the combined effects of light intensity, water mixing, sewage content and suspended particulate matter. Favourable conditions for FIO survival are low solar radiation, low temperature, low salinity, low densities of micro-predators and high levels of organic matter. Rainfall is the parameter most commonly associated with peak levels of FIOs. Resuspension of contaminated sediments in the water column dominates FIO distribution in shallow and depositional estuaries during storm conditions. Water/flesh FIO ratios may differ between shellfish growing waters because salinities and water temperatures also influence filter-feeding activity. Data are lacking on the role of biological processes on FIOs uptake and clearance in shellfish, particularly during periods of good water quality. FIO accumulation is usually of higher magnitude in mussels and cockles than in oysters and surf clams. It is proposed that differences in FIO accumulation rates are associated with the biological activity and the position of shellfish in the water column in relation to the location of impacting pollution sources. Accurate information on catchment hydrology, land uses, FIO loads from sewerage-related sources and livestock production areas are required to adequately characterise the microbiological status of shellfisheries.

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Fig. 1

Abbreviations

CSO:

Combined sewer overflow

ENT:

Enterococci

FC:

Faecal coliform

FIO:

Faecal indicator organism

WwTW:

Wastewater treatment works

References

  • Ahn, J.H., S.B. Grant, C.Q. Surbeck, N.P. Nezlin, and S. Jiang. 2005. Coastal water quality impact of stormwater runoff from an urban watershed in southern California. Environmental Science and Technology 39: 5940–5953.

    CAS  Article  Google Scholar 

  • Alexander, D.B., and T.J. Koretsky. 1996. Seasonal comparison of fecal coliform concentrations in the Trask River and a study of the survival of Escherichia coli in Tillamook Bay water. Final Report to the Tillamook Bay National Estuary Project. http://ir.library.oregonstate.edu/xmlui/bitstream/handle/1957/3850/Seasonal_ocr.pdf?sequence=1. Accessed 25 Nov 2011.

  • Alkan, U., D.J. Elliott, and L.M. Evison. 1995. Survival of enteric bacteria in relation to simulated solar radiation and other environmental factors in marine waters. Water Research 29(9): 2071–2081.

    CAS  Article  Google Scholar 

  • Amouroux, I., and D. Soudant. 2011. Comparison of microbiological contamination level between different species of shellfish. Proceedings of the 8th International Conference on Molluscan Shellfish Safety, Charlottetown, Prince Edward Island, Canada, 12–17 June 2011

  • Anderson, K.L., J.E. Whitlock, and V.J. Harwood. 2005. Persistence and differential survival of fecal indicator bacteria in subtropical waters and sediments. Applied and Environmental Microbiology 71(6): 3041–3048.

    CAS  Article  Google Scholar 

  • Aslan-Yilmaz, A., E. Okuş, and S. Ővez. 2004. Bacteriological indicators of anthropogenic impact prior to and during the recovery of water quality in an extremely polluted estuary, Golden Horn, Turkey. Marine Pollution Bulletin 49: 951–958.

    CAS  Article  Google Scholar 

  • Barcina, I., B. Ayo, A. Muela, L. Egea, and J. Iriberri. 1991. Predation rates of flagellate and ciliated protozoa on bacterioplankton in a river. FEMS Microbiology Ecology 85: 141–160.

    Article  Google Scholar 

  • Barcina, I., J.M. González, J. Iriberri, and L. Egea. 1989. Effect of visible light on progressive dormancy of Escherichia coli cells during the survival process in natural fresh water. Applied and Environmental Microbiology 55(1): 246–251.

    CAS  Google Scholar 

  • Beaudeau, P., N. Tousset, F. Bruchon, A. Lefèvre, and H.D. Taylor. 2001. In situ measurement and statistical modelling of Escherichia coli decay in small rivers. Water Research 35(13): 3168–3178.

    CAS  Article  Google Scholar 

  • Bellair, J.T., G.A. Parr-Smith, and I.G. Wallis. 1977. Significance of diurnal variations in fecal coliform die-off rates in the design of ocean outfalls. Journal of the Water Pollution Control Federation 49(9): 2022–2030.

    Google Scholar 

  • Beucher, M. 1993. Etude de l’accumulation, de la retention et du relargage de bacteries enteriques par l’huitre Crassostrea gigas. Memoire pour l’obtention du Diplôme de l’Ecole Pratique des Hautes Etudes. [in French]

  • Bernard, F.R. 1989. Uptake and elimination of coliform bacteria by four marine bivalve molluscs. Canadian Journal of Aquatic Sciences 46: 1592–1599.

    Article  Google Scholar 

  • Biancani, P.J., R.H. Carmichael, J.H. Daskin, W. Burkhardt III, and K.R. Calci. 2012. Seasonal and spatial effects of wastewater effluent on growth, survival, and accumulation of microbial contaminants by oysters in Mobile Bay, Alabama. Estuaries and Coasts 35: 121–131.

    CAS  Article  Google Scholar 

  • Boehm, A.B. 2007. Enterococci concentrations in diverse coastal environments exhibit extreme variability. Environmental Science & Technology 41(24): 8227–8232.

    CAS  Article  Google Scholar 

  • Boehm, A.B., B.F. Sanders, and C.D. Winant. 2002a. Cross-shelf transport at Huntington Beach. Implications for the fate of sewage discharged through an offshore ocean outfall. Environmental Science & Technology 36: 1899–1906.

    CAS  Article  Google Scholar 

  • Boehm, A.B., S.B. Grant, J.H. Kim, S.L. Mowbray, C.D. McGee, C.D. Clark, D.M. Foley, and D.E. Wellman. 2002b. Decadal and shorter period variability of surf zone water quality at Huntington Beach, California. Environmental Science & Technology 36(18): 3885–3892.

    CAS  Article  Google Scholar 

  • Boehm, A.B., and S.B. Weisberg. 2005. Tidal forcing of enterococci at marine recreational beaches at fortnightly and semidiurnal frequencies. Environmental Science and Technology 39(15): 5575–5583.

    CAS  Article  Google Scholar 

  • Bonilla, T.D., K. Nowosielski, M. Cuvelier, A. Hartz, M. Green, N. Esiobu, D.S. McCorquodale, J.M. Fleisher, and A. Rogerson. 2007. Prevalence and distribution of fecal indicator organisms in South Florida beach sand and preliminary assessment of health effects associated with beach sand exposure. Marine Pollution Bulletin 54: 1472–1482.

    CAS  Article  Google Scholar 

  • Bonilla, T.D., K. Nowosielski, N. Esiobu, D.S. McCorquodale, and A. Rogerson. 2006. Species assemblages of Enterococcus indicate potential sources of fecal bacteria at a south Florida recreational beach. Marine Pollution Bulletin 52: 807–810.

    CAS  Article  Google Scholar 

  • Braga, E.S., C.V.D.H. Bonetti, L. Burone, and J.B. Filho. 2000. Eutrophication and bacterial pollution caused by industrial and domestic wastes at the Baixada Santista Estuarine system—Brazil. Marine Pollution Bulletin 40(2): 165–173.

    CAS  Google Scholar 

  • Brettar, I., and M.G. Höfle. 1992. Influence of ecosystematic factors on survival of Escherichia coli after large-scale release into lake water mesocosms. Applied and Environmental Microbiology 58(7): 2201–2210.

    CAS  Google Scholar 

  • Burkhardt III, W., and K.R. Calci. 2000. Selective accumulation may account for shellfish-associated viral illness. Applied and Environmental Microbiology 66(4): 1375–1378.

    CAS  Article  Google Scholar 

  • Burkhardt III, W., W.D. Watkins, and S.R. Rippey. 1992. Seasonal effects on accumulation of microbial indicator organisms by Mercenaria mercenaria. Applied and Environmental Microbiology 58(3): 826–831.

    Google Scholar 

  • Burton Jr., G.A., D. Gunnison, and G.R. Lanza. 1987. Survival of pathogenic bacteria in various freshwater sediments. Applied and Environmental Microbiology 53(4): 633–638.

    Google Scholar 

  • Boelen, P., I. Obernostere, A. Vink, and G.J. Buma. 1999. Attenuation of biologically effective UV radiation in tropical Atlantic waters measured with a biochemical DNA dosimeter. Photochemistry and Photobiology 69(1): 34–40.

    CAS  Article  Google Scholar 

  • Bonadonna, L., L. Volterra, F.A. Aulicino, and L. Mancini. 1990. Accumulation power of some bivalve molluscs. Marine Pollution Bulletin 21(2): 81–84.

    Article  Google Scholar 

  • Brock, R.L., G.R. Galbraith, and B.A. Benseman. 1985. Relationships of rainfall, river flow, and salinity to faecal coliform levels in a mussel fishery. New Zealand Journal of Marine and Freshwater Research 19: 485–494.

    Article  Google Scholar 

  • Buck, O., D.K. Niyogi, and C.R. Townsend. 2004. Scale-dependence of land use effects on water quality of streams in agricultural catchments. Environmental Pollution 130: 287–299.

    CAS  Article  Google Scholar 

  • Byappanahalli, M.N., R.L. Whitman, D.A. Shively, M.J. Sadowsky, and S. Ishii. 2006. Population structure, persistence, and seasonality of autochthonous Escherichia coli in temperate, coastal forest soil from a Great Lakes watershed. Environmental Microbiology 8(3): 504–513.

    CAS  Article  Google Scholar 

  • Cabelli, V.J., and W.P. Heffernan. 1970. Accumulation of Escherichia coli by the Northern Quahaug. Applied Microbiology 19(2): 239–244.

    CAS  Google Scholar 

  • California Regional Water Quality Control Board, 2001. Controlling pathogens in Tomales Bay, California. Total maximum daily load: sources and loadings. Progress Report, June 30, 2001. CRWQCB—San Francisco Bay Region. Available at: http://www.krisweb.com/biblio/tomales_crwqcb_sfrwqcb_2001_tmdlprogrptsources.pdf. Accessed 03 Feb 2011.

  • Campos, C.J.A., and R.A. Cachola. 2007. Faecal coliforms in bivalve harvesting areas of the Alvor Lagoon (southern Portugal): influence of seasonal variability and urban development. Environmental Monitoring and Assessment 133(1–3): 31–41.

    Article  Google Scholar 

  • Campos, C.J.A., K. Hargin, S. Kershaw, R.J. Lee, and O.C. Morgan. 2011. Rainfall and river flows are predictors for β-glucuronidase positive Escherichia coli accumulation in mussels and Pacific oysters from the Dart Estuary (England). Journal of Water and Health 9(2): 368–381.

    Article  Google Scholar 

  • Campos, C.J.A., and S. Kershaw. 2012. Review of knowledge on impact of chronic microbial contamination on bivalve shellfish. Cefas report to Defra under project WT0923—impact of chronic microbial pollution on shellfish.

  • Carlucci, A.F., and D. Pramer. 1959. Factors affecting the survival of bacteria in sea water. Applied Microbiology 7: 388–392.

    CAS  Google Scholar 

  • Carlucci, A.F., and D. Pramer. 1960. An evaluation of factors affecting the survival of Escherichia coli in sea water II. Salinity, pH, and nutrients. Applied Microbiology 8: 247–250.

    CAS  Google Scholar 

  • Carlucci, A.F., P.V. Scarpino, and D. Pramer. 1961. Evaluation of factors affecting survival of Escherichia coli in sea water. Applied Microbiology 9: 400–404.

    CAS  Google Scholar 

  • Catalao Dionisio, L.P., G. Rheinheimer, and J.J. Borrego. 2000. Microbiological pollution of Ria Formosa (South of Portugal). Marine Pollution Bulletin 40(2): 186–193.

    Article  Google Scholar 

  • Chandran, A., and A.A.M. Hatha. 2005. Relative survival of Escherichia coli and Salmonella typhimurium in a tropical estuary. Water Research 39: 1397–1403.

    CAS  Article  Google Scholar 

  • Characklis, G.W., M.J. Dilts, O.D. Simmons III, C.A. Likirdopulos, L.-A.H. Krometis, and M.D. Sobsey. 2005. Microbial portioning to settleable particles in stormwater. Water Research 39: 1773–1782.

    CAS  Article  Google Scholar 

  • Chigbu, P., S. Gordon, and T. Strange. 2004. Influence of inter-annual variations in climatic factors on fecal coliform levels in Mississippi Sound. Water Research 38: 4341–4352.

    CAS  Article  Google Scholar 

  • Chigbu, P., S. Gordon, and T. Strange. 2005. Fecal coliform bacteria disappearance rates in a north-central Gulf of Mexico estuary. Estuarine, Coastal and Shelf Science 65: 309–318.

    Article  Google Scholar 

  • Churchland, L.M., G. Kan, and A. Ages. 1982. Variation in fecal pollution indicators through tidal cycles in the Fraser River estuary. Canadian Journal of Microbiology 28(2): 239–247.

    CAS  Article  Google Scholar 

  • Clausen, I., and H.U. Riisgård. 1996. Growth, filtration and respiration in the mussel Mytilus edulis: no evidence for physiological regulation of the filter-pump to nutritional needs. Marine Ecology Progress Series 141: 37–45.

    Article  Google Scholar 

  • Converse, R.R., M.F. Piehler, and R.T. Noble. 2011. Contrasts in concentrations and loads of conventional and alternative indicators of fecal contamination in coastal stormwater. Water Research 45: 5229–5240.

    CAS  Article  Google Scholar 

  • Cornax, R., M.A. Moriñigo, P. Romero, and J.J. Borrego. 1990. Survival of pathogenic microorganisms in seawater. Current Microbiology 20: 293–298.

    Article  Google Scholar 

  • Cotner, J.B., R.H. Sada, H. Bootsma, T. Johengen, J.F. Cavaletto, and W.S. Gardner. 2000. Nutrient limitation of heterotrophic bacteria in Florida Bay. Estuaries 23: 611–620.

    CAS  Article  Google Scholar 

  • Coulliette, A.D., E.S. Money, M.L. Serre, and R.T. Noble. 2009. Space/time analysis of fecal pollution and rainfall in an eastern North Carolina estuary. Environmental Science and Technology 43(10): 3728–3735.

    CAS  Article  Google Scholar 

  • Coulliette, A.D., and R.T. Noble. 2008. Impacts of rainfall on the water quality of the Newport River Estuary (Eastern North Carolina, USA). Journal of Water and Health 6(4): 473–482.

    CAS  Article  Google Scholar 

  • Craig, D.L., H.J. Fallowfield, and N.J. Cromar. 2001. The effects of temperature and sediment characteristics on survival of Escherichia coli in recreational coastal water and sediment. Environmental Health 1(1): 43–50.

    Google Scholar 

  • Crowther, J., D. Kay, and M.D. Wyer. 2001. Relationships between microbial water quality and environmental conditions in coastal recreational waters: the Fylde coast, UK. Water Research 35(17): 4029–4038.

    CAS  Article  Google Scholar 

  • Crowther, J., D. Kay, and M.D. Wyer. 2002. Faecal-indicator concentrations in waters draining lowland pastoral catchments in the UK: relationships with land use and farming practices. Water Research 36: 1725–1734.

    CAS  Article  Google Scholar 

  • Cusson, M., R. Tremblay, G. Daigle, and M. Roussy. 2005. Modeling the depuration potential of blue mussels (Mytilus spp.) in response to thermal shock. Aquaculture 250: 183–193.

    Article  Google Scholar 

  • Davies, C.M., J.A.H. Long, M. Donald, and N.J. Ashbolt. 1995. Survival of fecal microorganisms in marine and freshwater sediments. Applied and Environmental Microbiology 61(5): 1888–1896.

    CAS  Google Scholar 

  • Davies-Colley, R.J., R.G. Bell, and A.M. Donnison. 1994. Sunlight inactivation of enterococci and fecal coliforms in sewage effluent diluted in seawater. Applied and Environmental Microbiology 60: 2049–2058.

    CAS  Google Scholar 

  • De Brauwere, A., B. de Brye, P. Servais, J. Passerat, and E. Deleersnijder. 2011. Modelling Escherichia coli concentrations in the tidal Scheldt river and estuary. Water Research 45: 2724–2738.

    Article  CAS  Google Scholar 

  • Desmarais, T.R., H.M. Solo-Gabriele, and C.J. Palmer. 2002. Influence of soil on fecal indicator organisms in a tidally influenced subtropical environment. Applied and Environmental Microbiology 68(3): 1165–1172.

    CAS  Article  Google Scholar 

  • Doyle, J.D., B. Tunnicliff, R. Kramer, R. Kuehl, and S.K. Brickler. 1992. Instability of fecal coliform populations in waters and bottom sediments at recreational beaches in Arizona. Water Research 26(7): 979–988.

    Article  Google Scholar 

  • Enzinger, R.M., and R.C. Cooper. 1976. Role of bacteria and protozoa in the removal of Escherichia coli from estuarine waters. Applied and Environmental Microbiology 31(5): 758–763.

    CAS  Google Scholar 

  • Erkenbrecher Jr., C.W. 1981. Sediment bacterial indicators in an urban shellfishing subestuary of the lower Chesapeake Bay. Applied and Environmental Microbiology 42(3): 484–492.

    Google Scholar 

  • Fanshawe, T. 1995. Investigation of the effect of salinity on the uptake and elimination of Escherichia coli, by Mytilus edulis. M.Sc. thesis of the University College of North Wales, Bangor.

  • Faust, M.A. 1976. Coliform bacteria from diffuse sources as a factor in estuarine pollution. Water Research 10: 619–627.

    Article  Google Scholar 

  • Faust, M.A., A.E. Aotaky, and M.T. Hargadon. 1975. Effect of physical parameters in the in situ survival of Escherichia coli MC-6 in an estuarine environment. Applied Microbiology 30(5): 800–806.

    CAS  Google Scholar 

  • Fenchel T (1988) Microfauna in pelagic food chains. In Nitrogen cycling in coastal marine environments, eds. Blackburn, T.H., and J. Sorensen. Chichester: Wiley.

  • Ferguson, C.M., B.G. Coote, N.J. Ashbolt, and I.M. Stevenson. 1996. Relationships between indicators, pathogens and water quality in an estuarine system. Water Research 30(9): 2045–2054.

    CAS  Article  Google Scholar 

  • Fiandrino, A., Y. Martin, P. Got, J.L. Bonnefont, and M. Troussellier. 2003. Bacterial contamination of Mediterranean coastal seawater as affected by riverine inputs: simulation approach applied to a shellfish breeding area (Thau lagoon, France). Water Research 37: 1711–1722.

    CAS  Article  Google Scholar 

  • Foppen, J.W.A., and J.F. Schijven. 2006. Evaluation of data from the literature on the transport and survival of Escherichia coli and thermotolerant coliforms in aquifers under saturated conditions. Water Research 40(3): 401–426.

    CAS  Article  Google Scholar 

  • Fries, J.S., G.W. Characklis, and R.T. Noble. 2008. Sediment–water exchange of Vibrio sp. and fecal indicator bacteria: implications for persistence and transport in the Neuse River Estuary, North Carolina, USA. Water Research 42: 941–950.

    CAS  Article  Google Scholar 

  • Fu, L.-L., J.-B. Shuai, Y. Wang, H.-J. Ma, and J.-R. Li. 2011. Temporal genetic variability and host sources of Escherichia coli associated with fecal pollution from domesticated animals in the shellfish culture environment of Xiangshan Bay, East China Sea. Environmental Pollution 159: 2808–2814.

    CAS  Article  Google Scholar 

  • Fujioka, R.S., H.H. Hashimoto, E.B. Siwak, and R.H.F. Young. 1981. Effect of sunlight on survival of indicator bacteria in seawater. Applied and Environmental Microbiology 41(3): 690–696.

    CAS  Google Scholar 

  • Galtsoff, P.S. 1964. The American oyster, Crassostrea virginica Gmelin. Fishery Bulletin of the Fish and Wildlife Service 64.

  • Gameson, A.L.H., and J.R. Saxon. 1967. Field studies on effect of daylight on mortality of coliform bacteria. Water Research 1: 279–295.

    Article  Google Scholar 

  • Garcia-Armisen, T., and P. Servais. 2007. Respective contributions of point and non-point sources of E. coli and enterococci in a large urbanised watershed (the Seine River, France). Journal of Environmental Management 82: 512–518.

    CAS  Article  Google Scholar 

  • García-Lara, J., J. Martínez, M. Vilamú, and J. Vives-Rego. 1993. Effect of previous growth conditions on the starvation-survival of Escherichia coli in seawater. Journal of General Microbiology 139: 1425–1431.

    Article  Google Scholar 

  • Garrido-Pérez, M.C., E. Anfuso, A. Acevedo, and J.A. Perales-Vargas-Machuca. 2008. Microbial indicators of faecal contamination in waters and sediments of beach bathing zones. International Journal of Hygiene and Environmental Health 211: 510–517.

    Article  Google Scholar 

  • Gauthier, M.J., P.M. Munro, and S. Mohajer. 1987. Influence of salts and sodium chloride on the recovery of Escherichia coli from seawater. Current Microbiology 15: 5–10.

    CAS  Article  Google Scholar 

  • Gerba, C.P., and J.S. McLeod. 1976. Effect of sediments on the survival of Escherichia coli in marine waters. Applied and Environmental Microbiology 32(1): 114–120.

    CAS  Google Scholar 

  • Gerdes, D. 1983. The Pacific oyster Crassostrea gigas: part I. Feeding behaviour of larvae and adults. Aquaculture 31(2–4): 195–219.

    Article  Google Scholar 

  • Goto, D.K., and T. Yan. 2011. Effects of land uses on fecal indicator bacteria in the water and soil of a tropical watershed. Microbes and Environments 26(3): 254–260.

    Article  Google Scholar 

  • Gourmelon, M., P. Lazure, D. Hervio-Heath, J.C. Le Saux, M.P. Caprais, F.S. Le Guyader, M. Catherine, and M. Pommepuy. 2010. Microbial modelling in coastal environments and early warning systems: useful tools to limit shellfish microbial contamination. In Safe management of shellfish and harvest waters, eds. Rees, G., K. Pond, D. Kay, J. Bartram, and J. Santo Domingo. London: IWA.

  • Goyal, S.M., C.P. Gerba, and J.L. Melnick. 1979. Human enteroviruses in oysters and their overlying waters. Applied and Environmental Microbiology 37(3): 572–581.

    CAS  Google Scholar 

  • Grant, S.B., J.H. Kim, B.H. Jones, S.A. Jenkins, J. Wasyl, and C. Cudaback. 2005. Surf zone entrainment, along-shore transport, and human health implications of pollution from tidal outlets. Journal of Geophysical Research 110(C10025): 1–20.

    Google Scholar 

  • Guillon-Cottard, I., H. Augier, J.J. Console, and O. Esmieu. 1998. Study of microbiological pollution of a pleasure boat harbour using mussels as bioindicators. Marine Environmental Research 45(3): 239–247.

    CAS  Article  Google Scholar 

  • Hassan, E.S. 1993. Monitoring of microbial water quality and saprophytic bacterial genera of the Abu Dhabi coastal area, U.A.E. Marine Biology 116: 489–495.

    Article  Google Scholar 

  • Holland, A.F., D.M. Sanger, C.P. Gawle, S.B. Lerberg, M.S. Santiago, H.M. Riekerk, L.E. Zimmerman, and G.I. Scott. 2004. Linkages between tidal creek ecosystems and the landscape and demographic attributes of their watersheds. Journal of Experimental Marine Biology and Ecology 298: 151–178.

    Article  Google Scholar 

  • Hirn, J., H. Viljamaa, and M. Raevuori. 1980. The effect of physicochemical, phytoplankton and seasonal factors on faecal indicator bacteria in northern brackish water. Water Research 14: 279–285.

    CAS  Article  Google Scholar 

  • Hrenovic, J., and T. Ivankovic. 2009. Survival of Escherichia coli and Acinectobacter junii at various concentrations of sodium chloride. EurAsian Journal of Biosciences 3: 144–151.

    Article  Google Scholar 

  • Hughes, K.A. 2003. Influence of seasonal environmental variables on the distribution of presumptive fecal coliforms around an Antarctic research station. Applied and Environmental Microbiology 69(8): 4884–4891.

    CAS  Article  Google Scholar 

  • Huot, Y., W.H. Jeffrey, R.F. Davis, and J.J. Cullen. 2000. Damage to DNA in bacterioplankton: a model of damage by ultraviolet radiation and its repair as influenced by vertical mixing. Photochemistry and Photobiology 72(1): 62–74.

    CAS  Article  Google Scholar 

  • Isobe, K.O., M. Tarao, N.H. Chiem, L.Y. Minh, and H. Takada. 2004. Effect of environmental factors on the relationship between concentrations of Coprostanol and fecal indicator bacteria in tropical (Mekong Delta) and temperate (Tokyo) freshwaters. Applied and Environmental Microbiology 70(2): 814–821.

    CAS  Article  Google Scholar 

  • Izbicki, J.A., P.W. Swarzenski, C.D. Reich, C. Rollins, and P.A. Holden. 2009. Sources of fecal indicator bacteria in urban streams and ocean beaches, Santa Barbara, California. Annals of Environmental Science 3: 139–178.

    CAS  Google Scholar 

  • Jamieson, R., R. Gordon, D. Joy, and H. Lee. 2004. Assessing microbial pollution of rural surface waters. A review of current watershed scale modeling approaches. Agricultural Water Management 70: 1–17.

    Article  Google Scholar 

  • Janelidze, N., E. Jaiani, N. Lashkhi, A. Tskhvediani, T. Kokashvili, T. Gvarishvili, D. Jgenti, E. Mikashavidze, R. Diasamidze, S. Narodny, R. Obiso, C.A. Whitehouse, A. Huq, and M. Tediashvili. 2011. Microbial water quality of the Georgian coastal zone of the Black Sea. Marine Pollution Bulletin 62: 573–580.

    CAS  Article  Google Scholar 

  • Jeng, H.A.C., A.J. Englande, R.M. Bakeer, and H.B. Bradford. 2005. Impact of urban stormwater runoff on estuarine environmental quality. Estuarine, Coastal and Shelf Science 63: 513–526.

    Article  Google Scholar 

  • Ji, Z.-G. 2008. Hydrodynamics and water quality: modeling rivers, lakes, and estuaries. Hoboken: Wiley.

    Book  Google Scholar 

  • Jõers, A., N. Kaldalu, and T. Tenson. 2010. The frequency of persisters in Escherichia coli reflects the kinetics of awakening from dormancy. Journal of Bacteriology 192(13): 3379–3384.

    Article  CAS  Google Scholar 

  • Jørgensen, C.B. 1990. Bivalve filter feeding: hydrodynamics, bioenergetics, physiology and ecology. Fredensborg: Olsen & Olsen.

    Google Scholar 

  • Jørgensen, C.B. 1996. Bivalve filter feeding revisited. Marine Ecology Progress Series 142: 287–302.

    Article  Google Scholar 

  • Kacar, A. 2011. Analysis of spatial and temporal variation in the levels of microbial indicators in the major rivers flowing into the Aegean Sea, Turkey. Ecological Indicators 11(5): 1360–1365.

    CAS  Article  Google Scholar 

  • Kashefipour, S.M., B. Lin, and R.A. Falconer. 2006. Modelling the fate of faecal indicators in a coastal basin. Water Research 40: 1413–1425.

    CAS  Article  Google Scholar 

  • Kay, D., A.C. Edwards, R.C. Ferrier, C. Francis, C. Kay, L. Rushby, J. Watkins, and A.T. McDonald. 2007. Catchment microbial dynamics: the emergence of a research agenda. Progress in Physical Geography 31(1): 59–76.

    Article  Google Scholar 

  • Kay, D., J. Crowther, C.M. Stapleton, M.D. Wyer, L. Fewtrell, A. Edwards, C.A. Francis, A.T. McDonald, J. Watkins, and J. Wilkinson. 2008. Faecal indicator organism concentrations in sewage and treated effluents. Water Research 42: 442–454.

    CAS  Article  Google Scholar 

  • Kay, D., S. Anthony, J. Crowther, B.J. Chambers, F.A. Nicholson, D. Chadwick, C.M. Stapleton, and M.D. Wyer. 2009. Microbial water pollution: a screening tool for initial catchment-scale assessment and source apportionment. Science of the Total Environment 408(23): 5649–5656.

    Article  CAS  Google Scholar 

  • Kay, D., S. Kershaw, R. Lee, M.D. Wyer, J. Watkins, and C. Francis. 2005. Results of field investigations into the impact of intermittent discharges on the microbiological quality of wild mussels (Mytilus edulis) in a tidal estuary. Water Research 42: 3033–3046.

    Article  CAS  Google Scholar 

  • Kelsey, H., D.E. Porter, G. Scott, M. Neet, and D. White. 2004. Using geographic information systems and regression analysis to evaluate relationships between land use and fecal coliform bacterial pollution. Journal of Experimental Marine Biology and Ecology 298: 197–209.

    Article  Google Scholar 

  • Kirby-Smith, W.W., and N.M. White. 2006. Bacterial contamination associated with estuarine shoreline development. Journal of Applied Microbiology 100: 648–657.

    CAS  Article  Google Scholar 

  • Koch, A.L. 1971. The adaptive responses of Escherichia coli to a feast and famine existence. Advances in Microbial Physiology 6: 144–217.

    Article  Google Scholar 

  • Koch, A.L. 1979. Microbial growth in low concentrations of nutrients. In Strategies of microbial life in extreme environments, ed. Shilo, M. Berlin: Dahlem Konferenzen.

  • Krogh, M., and L. Robinson. 1996. Environmental variables and their association with faecal coliform and faecal streptococci densities at thirteen Sydney beaches. Marine Pollution Bulletin 33(7–12): 239–248.

    CAS  Article  Google Scholar 

  • Labelle, R.L., C.P. Gerba, S.M. Goyal, J.L. Melnick, I. Chech, and G.F. Bodgan. 1980. Relationship between environmental factors, bacterial indicators, and the occurrence of enteric viruses in estuarine systems. Applied and Environmental Microbiology 39: 588–596.

    CAS  Google Scholar 

  • Laing, I., and B.E. Spencer. 2006. Bivalve cultivation: criteria for selecting a site. Cefas. Science Series Technical Report no. 136. http://www.cefas.co.uk/publications/techrep/techrep136.pdf. Accessed 10 Jan 2012.

  • Lart, W.J., and S.A. Hudson. 1993. Factors affecting Escherichia coli levels in shellfish with reference to E.E.C. Directive 91/492. Seafish Report No. 419. MAFF R & D Commission 1992/93. http://www.seafish.org/media/Publications/SR419.pdf. Accessed 1 Dec 2011.

  • Lee, R., D. Kay, R.J. Wilkinson, L. Fewtrell, and C. Stapleton. 2003. Impact of intermittent discharges on the microbial quality of shellfish. Environment Agency R&D Technical Report P2-266/TR.

  • Lee, R.J., and O.C. Morgan. 2003. Environmental factors influencing the microbiological contamination of commercially harvested shellfish. Water Science and Technology 47(3): 65–70.

    Google Scholar 

  • Lee, R.J., and R.J.O. Glover. 1998. Evaluation of the impact of different sewage treatment processes on shellfishery pollution using a geographic information system (GIS). Water Science and Technology 38(12): 15–22.

    CAS  Article  Google Scholar 

  • Lees, D. 2000. Viruses and bivalve shellfish. International Journal of Food Microbiology 59: 81–116.

    CAS  Article  Google Scholar 

  • Legendre, P., B. Baleux, and M. Troussellier. 1984. Dynamics of pollution-indicator and heterotrophic bacteria in sewage treatment lagoons. Applied and Environmental Microbiology 48(3): 586–593.

    CAS  Google Scholar 

  • Lessard, E.J., and J.M. Sieburth. 1983. Survival of natural sewage populations of enteric bacteria in diffusion and batch chambers in the marine environment. Applied and Environmental Microbiology 45(3): 950–959.

    CAS  Google Scholar 

  • Lipp, E.K., J.L. Jarrell, D.W. Griffin, J. Lukasik, J. Jacukiewicz, and J.B. Rose. 2002. Preliminary evidence for human fecal contamination in corals of the Florida Keys, USA. Marine Pollution Bulletin 44: 666–670.

    CAS  Article  Google Scholar 

  • Lipp, E.K., R. Kurz, R. Vincent, C. Rodriguez-Palacios, S.R. Farrah, and J.B. Rose. 2001. The effects of seasonal variability and weather on microbial fecal pollution and enteric pathogens in a subtropical estuary. Estuaries 24(2): 266–276.

    CAS  Article  Google Scholar 

  • Lizárraga-Partida, M., and G.V. Cárdenas. 1996. Influence of water circulation on marine and faecal bacteria in a mussel-growing area. Marine Pollution Bulletin 32(2): 196–201.

    Article  Google Scholar 

  • Loosanoff, V.L., and C.A. Nomejko. 1946. Feeding of oysters in relation to tidal stages and to periods of light and darkness. Biological Bulletin 90(3): 244–264.

    Article  Google Scholar 

  • Lucena, F., J. Lasobras, D. McIntosh, M. Forcadell, and J. Jofre. 1994. Effect of distance from the polluting focus on relative concentrations of Bacteroides fragilis phages and coliphages in mussels. Applied and Environmental Microbiology 60(7): 2272–2277.

    CAS  Google Scholar 

  • Mallin, M.A. 2006. Wading in waste. Scientific American 294: 52–59.

    Article  Google Scholar 

  • Mallin, M.A., K.E. Williams, E.C. Esham, and R.P. Lowe. 2000. Effect of human development on bacteriological water quality in coastal watersheds. Ecological Applications 10(4): 1047–1056.

    Article  Google Scholar 

  • Mallin, M.A., L.B. Cahoon, B.R. Toothman, D.C. Parsons, M.R. McIver, M.L. Ortwine, and R.N. Harrington. 2007. Impacts of raw sewage spill on water and sediment quality in an urbanised estuary. Marine Pollution Bulletin 54: 81–88.

    CAS  Article  Google Scholar 

  • Mallin, M.A., M.I. Halton, B. Song, M.E. Tavares, and S.P. Dellies. 2010. Bacterial source tracking guides management of boat head waste in a coastal resort area. Journal of Environmental Management 91: 2748–2753.

    Article  Google Scholar 

  • Mallin, M.A., S.H. Ensign, M.R. McIver, G.C. Shank, and P.K. Fowler. 2001. Demographic, landscape, and meteorological factors controlling the microbial pollution of coastal waters. In The ecology and etiology of newly emerging marine diseases, Hydrobiologia, 460:185–193, ed. J.W. Porter. The Netherlands: Kluwer Academic.

    Google Scholar 

  • Mallin, M.A., E.C. Esham, K.E. Williams, and J.E. Nearhoof. 1999. Tidal stage variability of fecal coliform and chlorophyll a concentrations in coastal creeks. Marine Pollution Bulletin 38(5): 414–422.

    CAS  Article  Google Scholar 

  • Marshall, K.C. 1979. Reactions of microorganisms, ions and macromolecules at boundary. In Boundaries in microbial ecology, ed. Ellwood, D.C. Cambridge: Harvard UP.

  • Martin, Y., M. Troussellier, and J.L. Bonnefont. 1998. Adaptative responses of E. coli to marine environmental stresses: a modelling approach based on viability and dormancy concepts. Oceanologica Acta 21(6): 951–964.

    Article  Google Scholar 

  • Martins, F., M.P. Reis, R. Neves, A.P. Cravo, A. Brito, and A. Venâncio, 2006. Molluscan shellfish bacterial contamination in Ria Formosa coastal lagoon: a modelling approach. Journal of Coastal Research SI39: 1551–1555, Proceedings of the 8th International Coastal Symposium, Itajaí, SC, Brazil.

    Google Scholar 

  • Martinez, D.I., and A.J.F.C. Oliveira. 2010. Faecal bacteria in Perna perna (Linnaeus, 1758) (Mollusca: Bivalvia) for biomonitoring coastal waters and seafood quality. Brazilian Journal of Oceanography 58(special issue IVSBO): 29–35.

    Google Scholar 

  • Martinez-Manzanares, E., F. Egea, D. Castro, M.A. Moriñigo, P. Romero, and J.J. Borrego. 1991. Accumulation and depuration of pathogenic and indicator microorganisms by the bivalve mollusc, Chamelea gallina L., under controlled laboratory conditions. Journal of Food Protection 54(8): 612–618.

    Google Scholar 

  • McCambridge, J., and T.A. McMeekin. 1981. Effect of solar radiation and predacious microorganisms on survival of fecal and other bacteria. Applied and Environmental Microbiology 41(5): 1083–1087.

    CAS  Google Scholar 

  • McLaughlin, K., J.H. Ahn, R.M. Litton, and S.B. Grant. 2007. Use of salinity mixing models to estimate the contribution of creek water fecal indicator bacteria to an estuarine environment: Newport Bay, California. Water Research 41: 3595–3604.

    CAS  Article  Google Scholar 

  • McLellan, S.L., and A.K. Salmore. 2003. Evidence for localised bacterial loading as the cause of chronic beach closings in a freshwater marina. Water Research 37: 2700–2708.

    CAS  Article  Google Scholar 

  • Mieszkin, S., J.-P. Furet, G. Corthier, and M. Gourmelon. 2009. Estimation of pig fecal contamination in a river catchment by real-time PCR using two pig-specific Bacteroidales 16S rRNA genetic markers. Applied and Environmental Microbiology 75(10): 3045–3054.

    CAS  Article  Google Scholar 

  • Mill, A., T. Schlacher, and M. Katouli. 2006. Tidal and longitudinal variation of faecal indicator bacteria in an estuarine creek in south-east Queensland, Australia. Marine Pollution Bulletin 52: 881–891.

    CAS  Article  Google Scholar 

  • Moresco, V., A. Viancelli, M.A. Nascimento, D.S.M. Souza, A.P.D. Ramos, L.A.T. Garcia, C.M.O. Simões, and C.R.M. Barardi. 2012. Microbiological and physicochemical analysis of the coastal waters of southern Brazil. Marine Pollution Bulletin 64(1): 40–48.

    CAS  Article  Google Scholar 

  • Mote, B.L., J.W. Turner, and E.K. Lipp. 2012. Persistence and growth of the fecal indicator bacteria Enterococci in detritus and natural estuarine plankton communities. Applied and Environmental Microbiology 78(8): 2569–2577.

    CAS  Article  Google Scholar 

  • Motwani, M.P. 1956. Experimental and ecological studies on the adaptation of Mytilus edulis L. to salinity fluctuations. Proceedings of the National Institute of Science of India 21B(5): 227–246.

    Google Scholar 

  • Muela, A., I. García-Bringas, and I. Barcina. 2000. The effect of simulated solar radiation on Escherichia coli: the relative roles of UV-B, UV-A, and photosynthetically active radiation. Microbial Ecology 39: 65–71.

    Article  Google Scholar 

  • Munro, P.M., M.J. Gauthier, V.A. Breittmayer, and J. Bongiovanni. 1989. Influence of osmoregulation processes on starvation survival of Escherichia coli in seawater. Applied and Environmental Microbiology 55(8): 2017–2024.

    CAS  Google Scholar 

  • Noble, R.T., I.M. Lee, and K.C. Schiff. 2004. Inactivation of indicator micro-organisms from various sources of faecal contamination in seawater and freshwater. Journal of Applied Microbiology 96: 464–472.

    CAS  Article  Google Scholar 

  • Obiri-Danso, K., and K. Jones. 2000. Intertidal sediments as reservoirs for Hippurate Negative campylobacters, salmonellae and faecal indicators in three recognised bathing waters in North West England. Water Research 34(2): 519–527.

    CAS  Article  Google Scholar 

  • Oliver, D.M., A.L. Heathwaite, R.D. Fish, D.R. Chadwick, C.J. Hodgson, M. Winter, and A. Butler. 2009. Scale appropriate modelling of diffuse microbial pollution from agriculture. Progress in Physical Geography 33(3): 358–377.

    Article  Google Scholar 

  • Oren, A., and L. Vlodavsky. 1985. Survival of Escherichia coli and Vibrio harveyi in Dead Sea water. FEMS Microbiology Letters 31(6): 365–371.

    Article  Google Scholar 

  • Ouattara, N.K., J. Passerat, and P. Servais. 2011. Faecal contamination of water and sediment in the rivers of the Scheldt drainage network. Environmental Monitoring and Assessment 183: 243–257.

    Article  Google Scholar 

  • Parker, J.K., D. McIntyre, and R.T. Noble. 2010. Characterizing fecal contamination in stormwater runoff in coastal North Carolina, USA. Water Research 44: 4186–4194.

    CAS  Article  Google Scholar 

  • Perkins, F.O., D.S. Haven, R.M. Alamo, and M.W. Rhodes. 1980. Uptake and elimination of bacteria in shellfish. Journal of Food Protection 43: 124–126.

    Google Scholar 

  • Plusquellec, A., M. Beucher, and Y. Le Gal. 1983. Enumeration of the bacterial contamination of bivalves in monitoring the marine bacteria pollution. Marine Pollution Bulletin 14: 260–263.

    Article  Google Scholar 

  • Plusquellec, A., M. Beucher, D. Prieur, and Y. Le Gal. 1990. Contamination of the mussel, Mytilus edulis Linnaeus, 1758, by enteric bacteria. Journal of Shellfish Research 9(1): 95–101.

    Google Scholar 

  • Pommepuy, M., J.F. Guillaud, E. Dupray, A. Derrien, F. LeGuyader, and M. Cormier. 1992. Enteric bacteria survival factors. Water Science and Technology 25(12): 93–103.

    CAS  Google Scholar 

  • Pommepuy, M., D. Hervio-Heath, M.P. Caprais, M. Gourmelon, J.C. Le Saux, and F. Le Guyader. 2005. Fecal contamination in coastal areas: an engineering approach. In Oceans and human health: pathogens in the marine environment, ed. S. Belkin and R.R. Colwell. New York: Springer.

    Google Scholar 

  • Prieur, D., G. Mével, J.-L. Nicolas, A. Plusquellec, and M. Vigneulle. 1990. Interactions between bivalve molluscs and bacteria in the marine environment. Oceanography and Marine Biology: an Annual Review 28: 277–352.

    Google Scholar 

  • Prins, T.C., N. Dankers, and A.C. Smaal. 1994. Seasonal variation in the filtration rates of a semi-natural mussel bed in relation to seston composition. Journal of Experimental Marine Biology and Ecology 176: 69–86.

    Article  Google Scholar 

  • Reeves, R.L., S.B. Grant, R.D. Mrse, C.M.C. Oancea, B.F. Sanders, and A.B. Boehm. 2004. Scaling and management of fecal indicator bacteria in runoff from a coastal urban watershed in southern California. Environmental Science and Technology 38: 2637–2648.

    CAS  Article  Google Scholar 

  • Riisgård, H.U. 2001. On measurement of filtration rates in bivalves—the stony road to reliable data: review and interpretation. Marine Ecology Progress Series 211: 275–291.

    Article  Google Scholar 

  • Riisgård, H.U., P.P. Egede, and I.B. Saavedra. 2011. Feeding behaviour of the mussel, Mytilus edulis: new observations, with a minireview of current knowledge. Journal of Marine Biology 2011, Article ID 312459.

  • Riou, P., J.C. Le Saux, F. Dumas, M.P. Caprais, S.F. Le Guyader, and M. Pommepuy. 2007. Microbial impact of small tributaries on water and shellfish quality in shallow coastal areas. Water Research 41: 2774–2786.

    CAS  Article  Google Scholar 

  • Rodgers, P., C. Soulsby, C. Hunter, and J. Petry. 2003. Spatial and temporal bacterial quality of a lowland agricultural stream in northeast Scotland. The Science of the Total Environment 314–316: 289–302.

    Article  CAS  Google Scholar 

  • Rödström, E.M., and P.R. Jonsson. 2000. Survival and feeding activity of oyster spat (Ostrea edulis L) as a function of temperature and salinity with implications for culture policies on the Swedish West coast. Journal of Shellfish Research 19(2): 799–808.

    Google Scholar 

  • Rogers, S., and J. Haines. 2005. Detecting and mitigating the environmental impact of fecal pathogens originating from confined animal feeding operations: review. EPA/600/R-06/021, September 2005. www.epa.gov/nrmrl/pubs/600r06021/600r06021.pdf. Accessed 28 Nov 2011.

  • Rosenfeld, L.K., C.D. McGee, G.L. Robertson, M.A. Noble, and B.H. Jones. 2006. Temporal and spatial variability of fecal indicator bacteria in the surf zone off Huntington Beach, CA. Marine Environmental Research 61: 471–493.

    CAS  Article  Google Scholar 

  • Rozen, Y., and S. Belkin. 2001. Survival of enteric bacteria in seawater. FEMS Microbiology Reviews 25: 513–529.

    CAS  Article  Google Scholar 

  • Rowse, A.J., and G.H. Fleet. 1984. Effects of water temperature and salinity on elimination of Salmonella charity and Escherichia coli from Sydney Rock oysters (Crassostrea commercialis). Applied and Environmental Microbiology 48(5): 1061–1063.

    CAS  Google Scholar 

  • Salomon, J.-C., and M. Pommepuy. 1990. Mathematical model of bacterial contamination of the Morlaix Estuary (France). Water Research 24(8): 983–994.

    Google Scholar 

  • Schultz-Fademrecht, C., M. Wichern, and H. Horn. 2008. The impact of sunlight on inactivation of indicator microorganisms both in river water and benthic films. Water Research 42: 4771–4779.

    CAS  Article  Google Scholar 

  • Scott, T.M., J. Caren, G.R. Nelson, T.M. Jenkins, and J. Lukasik. 2004. Tracking sources of fecal pollution in a South Carolina watershed by ribotyping Escherichia coli: a case study. Environmental Forensics 5: 15–19.

    CAS  Article  Google Scholar 

  • Servais, P., T. Garcia-Armisen, I. George, and G. Billen. 2007. Fecal bacteria in the rivers of the Seine drainage network (France): sources, fate and modelling. Science of the Total Environment 375(1–3): 152–167.

    CAS  Article  Google Scholar 

  • Shanks, O.C., C. Nietch, M. Simonich, M. Younger, D. Reynolds, and K.G. Field. 2006. Basin-wide analysis of the dynamics of fecal contamination and fecal source identification in Tillamook Bay, Oregon. Applied and Environmental Microbiology 72(8): 5537–5546.

    CAS  Article  Google Scholar 

  • Sinton, L.W. 2005. Biotic and abiotic effects. In Oceans and human health: pathogens in the marine environment, ed. S. Belkin and R.R. Colwell. New York: Springer.

    Google Scholar 

  • Sinton, L.W., R.J. Davies-Colley, and R.G. Bell. 1994. Inactivation of enterococci and fecal coliforms from sewage and meatworks effluents in seawater chambers. Applied and Environmental Microbiology 60: 2040–2048.

    CAS  Google Scholar 

  • Sinton, L.W., R.K. Finlay, and P.A. Lynch. 1999. Sunlight inactivation of fecal bacteriophages and bacteria in sewage-polluted seawater. Applied and Environmental Microbiology 65(8): 3605–3613.

    CAS  Google Scholar 

  • Sinton, L., C. Hall, and R. Braithwaite. 2007. Sunlight inactivation of Campylobacter jejuni and Salmonella enterica, compared with Escherichia coli, in seawater and river water. Journal of Water and Health 5(3): 357–365.

    Article  Google Scholar 

  • Sinton, L.W., C.H. Hall, P.A. Lynch, and R.J. Davies-Colley. 2002. Sunlight inactivation of fecal indicator bacteria and bacteriophages from waste stabilization pond effluent in fresh and saline waters. Applied and Environmental Microbiology 68(3): 1122–1131.

    CAS  Article  Google Scholar 

  • Smith, P., C. Carroll, B. Wilkins, P. Johnson, S.N. Gabhainn, and L.P. Smith. 1999. The effect of wind speed and direction on the distribution of sewage-associated bacteria. Letters in Applied Microbiology 28(3): 184–188.

    CAS  Article  Google Scholar 

  • Šolić, M., and N. Krstulović. 1992. Separate and combined effects of solar radiation, temperature, salinity, and pH on the survival of faecal coliforms in seawater. Marine Pollution Bulletin 24(8): 411–416.

    Article  Google Scholar 

  • Šolić, M., N. Krstulović, S. Josić, and D. Curać. 1999. The rate of concentration of faecal coliforms in shellfish under different environmental conditions. Environment International 25(8): 991–1000.

    Article  Google Scholar 

  • Solo-Gabriele, H.M., M.A. Wolfert, T.R. Desmarais, and C.J. Palmer. 2000. Sources of Escherichia coli in a coastal subtropical environment. Applied and Environmental Microbiology 66(1): 230–237.

    CAS  Article  Google Scholar 

  • Sonier, R., E. Mayrand, A.D. Boghen, M. Oullette, and V. Mallet. 2008. Concentration of Escherichia coli in sediments as an indicator of the sanitary status of oyster (Crassostrea virginica) aquaculture sites. Journal of Applied Ichthyology 24: 678–684.

    Article  Google Scholar 

  • Stapleton, C.M., M.D. Wyer, D. Kay, M. Bradford, N. Humphrey, J. Wilkinson, B. Lin, L. Yang, R.A. Falconer, J. Watkins, C.A. Francis, J. Crowther, N.D. Paul, K. Jones, and A.T. McDonald. 2007. Fate and transport of particles in estuaries, volume I. Environment Agency Science Report SC000002.

  • Stumpf, C.H., M.F. Piehler, S. Thompson, and R.T. Noble. 2010. Loading of fecal indicator bacteria in North Carolina tidal creek headwaters: hydrographic patterns and terrestrial runoff relationships. Water Research 44: 4704–4715.

    CAS  Article  Google Scholar 

  • Tedetti, M., and R. Sempéré. 2006. Penetration of ultraviolet radiation in the marine environment. A review. Photochemistry and Photobiology 82: 389–397.

    CAS  Article  Google Scholar 

  • Timoney, J.F., and A. Abston. 1984. Accumulation and elimination of Escherichia coli and Salmonella typhimurium by hard clams in an in vitro system. Applied and Environmental Microbiology 47(5): 986–988.

    CAS  Google Scholar 

  • Toothman, B.R., L.B. Cahoon, and M.A. Mallin. 2009. Phosphorus and carbohydrate limitation of fecal coliform and fecal enterococcus within tidal creek sediments. Hydrobiologia 636: 401–412.

    CAS  Article  Google Scholar 

  • Touron, A., T. Berthe, G. Gargala, M. Fournier, M. Ratajczak, P. Servais, and F. Petit. 2007. Assessment of faecal contamination and the relationship between pathogens and faecal bacterial indicators in an estuarine environment (Seine, France). Marine Pollution Bulletin 54: 1441–1450.

    CAS  Article  Google Scholar 

  • Troussellier, M., J.-L. Bonnefont, C. Courties, A. Derrien, E. Dupray, M. Gauthier, M. Gourmelon, F. Koux, P. Lebaron, Y. Martin, and M. Pommepuy. 1998. Responses of enteric bacteria to environmental stresses in seawater. Oceanologica Acta 21(6): 965–981.

    Article  Google Scholar 

  • Uncles, R.J., J.A. Stephens, and C. Harris. 2006. Runoff and tidal influences on the estuarine turbidity maximum of a highly turbid system: the upper Humber and Ouse Estuary, UK. Marine Geology 235: 213–228.

    Article  Google Scholar 

  • Valiela, I., M. Alber, and M. LaMontagne. 1991. Fecal coliform loadings and stocks in Buttermilk Bay, Massachusetts, USA, and management implications. Environmental Management 15(5): 659–674.

    Article  Google Scholar 

  • van Dolah, R.F., G.H.M. Riekerk, D.C. Bergquist, J. Felber, D.E. Chestnut, and A.F. Holland. 2008. Estuarine habitat quality reflects urbanization at large spatial scales in South Carolina’s coastal zone. Science of the Total Environment 390: 142–154.

    Article  CAS  Google Scholar 

  • Vidon, P., L.P. Tedesco, J. Wilson, M.A. Campbell, and L.R. Casey. 2008. Direct and indirect hydrological controls on E. coli concentration and loading in midwestern streams. Journal of Environmental Quality 37: 1761–1768.

    CAS  Article  Google Scholar 

  • Wait, D.A., and M.D. Sobsey. 2001. Comparative survival of enteric viruses and bacteria in Atlantic Ocean seawater. Water Science & Technology 43(12): 139–142.

    Google Scholar 

  • Webster, L.F., B.C. Thompson, M.H. Fulton, D.E. Chesnut, R.F. van Dolah, A.K. Leigh, and G.I. Scott. 2004. Identification of sources of Escherichia coli in South Carolina estuaries using antibiotic resistance analysis. Journal of Experimental Marine Biology and Ecology 298: 179–195.

    Article  Google Scholar 

  • Weiskel, P.K., B.L. Howes, and G.R. Heufelder. 1996. Coliform contamination of a coastal embayment: sources and transport pathways. Environmental Science and Technology 30(6): 1872–1881.

    CAS  Article  Google Scholar 

  • Whitlock, J.E., D.T. Jones, and V.J. Harwood. 2002. Identification of the sources of fecal coliforms in an urban watershed using antibiotic resistance analysis. Water Research 36: 4273–4282.

    CAS  Article  Google Scholar 

  • Wilkes, G., T. Edge, V. Gannon, C. Jokinen, E. Lyautey, D. Medeiros, N. Neumann, N. Ruecker, E. Topp, and D.R. Lapen. 2009. Seasonal relationships among indicator bacteria, pathogenic bacteria, Cryptosporidium oocysts, Giardia cysts, and hydrological indices for surface waters within an agricultural landscape. Water Research 43: 2209–2223.

    CAS  Article  Google Scholar 

  • Wilkinson, J., A. Jenkins, M. Wyer, and D. Kay. 1995. Modelling faecal coliform concentrations in streams. Institute of Hydrology (IH) Report No. 127. http://nora.nerc.ac.uk/7370/. Accessed 23 Nov 2011.

  • Wilkinson, J., D. Kay, M. Wyer, and A. Jenkins. 2006. Processes driving the episodic flux of faecal indicator organisms in streams impacting on recreational and shellfish harvesting waters. Water Research 40: 153–161.

    CAS  Article  Google Scholar 

  • Wither, A., J. Greaves, I. Dunhill, M. Wyer, C. Stapleton, D. Kay, N. Humphrey, J. Watkins, C. Francis, A. McDonald, and J. Crowther. 2005. Estimation of diffuse and point source microbial pollution in the Ribble catchment discharging to bathing waters in the north west of England. Water Science and Technology 51(3–4): 191–198.

    CAS  Google Scholar 

  • Wither, A., M. Rehfisch, and G. Austin. 2003. The impact of bird populations on the microbiological quality of bathing waters. Proceedings of the Diffuse Pollution Conference, Dublin, ECSA-2 Faecal indicator organisms 6: 52–57.

  • Young-Joo, A., D.H. Kambell, and G.P. Breidenbach. 2002. Escherichia coli and total coliforms in water and sediments at lake marinas. Environmental Pollution 120: 771–778.

    Google Scholar 

  • Younger, A., M. Boulter, and M. Pyke. 1999. Determination of appropriate conditions for the depuration of razor clams. Report to Seafish Industry Authority funded by MAFF. Available at: http://www.seafish.org/media/Publications/Razor_report.pdf. Accessed 13 Jan 2012.

  • Younger, A.D., R.J. Lee, and D.N. Lees. 2003. Microbiological monitoring of bivalve mollusc harvesting areas in England and Wales - rationale and approach. In Proceedings of the 4th International Conference on Molluscan Shellfish Safety, Santiago de Compostela, Spain, June 4–8, 2002. eds. A. Villalba, B. Reguera, J.L. Romalde, and R. Beiras. Consellería de Pesca e Asuntos Marítimos, Xunta de Galicia, Intergovernmental Oceanographic Commission of UNESCO 2003.

  • Younger, A.D., and R.A. Reese. 2011. E. coli accumulation compared between mollusc species across harvesting sites in England and Wales. Cefas report to the Food Standards Agency.

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Acknowledgments

This work was funded by the Department for Environment, Food and Rural Affairs (Defra) (Projects WT1001: Factors affecting the microbial quality of shellfish and WT0923: Impact of chronic microbial pollution on shellfish). We would like to thank two anonymous reviewers for their critical inputs to this manuscript.

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  1. Centre for Environment, Fisheries & Aquaculture Science (Cefas), Aquatic Health and Hygiene Division, Food Safety Group, Weymouth Laboratory, Weymouth, Dorset, DT4 8UB, UK

    Carlos J. A. Campos, Simon R. Kershaw & Ron J. Lee

  2. European Union Reference Laboratory, Weymouth, Dorset, UK

    Carlos J. A. Campos, Simon R. Kershaw & Ron J. Lee

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  1. Carlos J. A. Campos
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Campos, C.J.A., Kershaw, S.R. & Lee, R.J. Environmental Influences on Faecal Indicator Organisms in Coastal Waters and Their Accumulation in Bivalve Shellfish. Estuaries and Coasts 36, 834–853 (2013). https://doi.org/10.1007/s12237-013-9599-y

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Keywords

  • Faecal coliforms
  • Enterococci
  • Environmental factors
  • Escherichia coli
  • Seawater
  • Shellfish