Skip to main content

Advertisement

SpringerLink
Log in

Microbes in beach sands: integrating environment, ecology and public health

  • Reviews
  • Published:
Reviews in Environmental Science and Bio/Technology Aims and scope Submit manuscript

Abstract

Beach sand is a habitat that supports many microbes, including viruses, bacteria, fungi and protozoa (micropsammon). The apparently inhospitable conditions of beach sand environments belie the thriving communities found there. Physical factors, such as water availability and protection from insolation; biological factors, such as competition, predation, and biofilm formation; and nutrient availability all contribute to the characteristics of the micropsammon. Sand microbial communities include autochthonous species/phylotypes indigenous to the environment. Allochthonous microbes, including fecal indicator bacteria (FIB) and waterborne pathogens, are deposited via waves, runoff, air, or animals. The fate of these microbes ranges from death, to transient persistence and/or replication, to establishment of thriving populations (naturalization) and integration in the autochthonous community. Transport of the micropsammon within the habitat occurs both horizontally across the beach, and vertically from the sand surface and ground water table, as well as at various scales including interstitial flow within sand pores, sediment transport for particle-associated microbes, and the large-scale processes of wave action and terrestrial runoff. The concept of beach sand as a microbial habitat and reservoir of FIB and pathogens has begun to influence our thinking about human health effects associated with sand exposure and recreational water use. A variety of pathogens have been reported from beach sands, and recent epidemiology studies have found some evidence of health risks associated with sand exposure. Persistent or replicating populations of FIB and enteric pathogens have consequences for watershed/beach management strategies and regulatory standards for safe beaches. This review summarizes our understanding of the community structure, ecology, fate, transport, and public health implications of microbes in beach sand. It concludes with recommendations for future work in this vastly under-studied area.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Abdallaoui MS, Boutayeb H, Guessous-Idrissi N (2007) Fungal flora from the sand of two beaches of Casablanca (Morroco). Analysis and epidemiological corollary. J Mycol Med 17:58–62

    Google Scholar 

  • Abdelzaher AM, Wright ME, Ortega C et al (2010) Presence of pathogens and indicator microbes at a non-point source subtropical recreational marine beach. Appl Environ Microbiol 76:724–732

    CAS  Google Scholar 

  • Ahmed W, Richardson K, Sidhu J, Toze S (2012) Escherichia coli and Enterococcus spp. in rainwater tank samples: comparison of culture-based methods and 23S rRNA gene quantitative PCR assays. Environ Sci Technol 46:11370–11376

    CAS  Google Scholar 

  • Alam M, Sultana M, Nair GB et al (2007) Viable but nonculturable Vibrio cholerae O1 in biofilms in the aquatic environment and their role in cholera transmission. Proc Natl Acad Sci 104:17801–17806

    CAS  Google Scholar 

  • Alderisio K, 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

    CAS  Google Scholar 

  • Aldova E (1989) Serovars of Vibrio parahaemolyticus. J Hyg Epidemiol Microbiol Immunol 33:219

    CAS  Google Scholar 

  • Alm EW, Burke J, Spain A (2003) Fecal indicator bacteria are abundant in wet sand at freshwater beaches. Water Res 37:3978–3982

    Google Scholar 

  • Alm EW, 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

    Google Scholar 

  • Anderson JH (1979) In vitro survival of human pathogenic fungi in Hawaiian beach sand. Med Mycol 17:13–22

    CAS  Google Scholar 

  • Anderson S, Turner S, Lewis G (1997) Enterococci in the New Zealand environment: implications for water quality monitoring. Water Sci Technol 35:325–331

    CAS  Google Scholar 

  • Anderson KL, Whitlock JE, Harwood VJ (2005) Persistence and differential survival of fecal indicator bacteria in subtropical waters and sediments. Appl Environ Microbiol 71:3041–3048

    CAS  Google Scholar 

  • Ashbolt NJ, Dorsch MR, Cox PT, Banens B (1997) Blooming E. coli, what do they mean? In: Kay D, Fricker C (eds) Coliforms and E. coli, problem or solution?. The Royal Society of Chemistry, Cambridge

    Google Scholar 

  • Ashbolt NJ, Schoen ME, Soller JA, Roser DJ (2010) Predicting pathogen risks to aid beach management: the real value of quantitative microbial risk assessment (QMRA). Water Res 44:4692–4703

    CAS  Google Scholar 

  • Atlas RM, Bartha R (1997) Microbial ecology: fundamentals and applications. Benjamin-Cummings Pub. Co., Menlo Park, CA, pp 309–313

    Google Scholar 

  • Badgley BD, Thomas FIM, Harwood VJ (2010) The effects of submerged aquatic vegetation on the persistence of environmental populations of Enterococcus spp. Environ Microbiol 12:1271–1281

    CAS  Google Scholar 

  • Badgley BD, Ferguson J, Vanden Heuvel A et al (2011) Multi-scale temporal and spatial variation in genotypic composition of Cladophora-borne Escherichia coli populations in Lake Michigan. Water Res 45:721–731. doi:10.1016/j.watres.2010.08.041

    CAS  Google Scholar 

  • Bauer L, Alm E (2012) Escherichia coli toxin and attachment genes in sand at Great Lakes recreational beaches. J Great Lakes Res 38:129–133

    CAS  Google Scholar 

  • Bennani M, Amarouch H, Oubrim N, Cohen N (2012) Identification and antimicrobial resistance of fecal enterococci isolated in coastal Mediterranean environments of Morocco. Eur J Sci Res 70:266–275

    Google Scholar 

  • Bermudez M, Hazen TC (1988) Phenotypic and genotypic comparison of Escherichia coli from pristine tropical waters. Appl Environ Microbiol 54:979–983

    CAS  Google Scholar 

  • Bernard P, Gueho E, Pesando D (1988) Recherche de dermatophytes et de moisissures pathogènes dans les sables des plages, 1986–87. [Research on dermatophytes and pathogenic moulds in sea sand, 1986–87]

  • Beversdorf LJ, Bornstein-Forst SM, McLellan SL (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

    CAS  Google Scholar 

  • Boehm AB, Shellenbarger GG, Paytan A (2004) Groundwater discharge: potential association with fecal indicator bacteria in the surf zone. Environ Sci Technol 38:3558–3566

    CAS  Google Scholar 

  • Boiron P, Agis F, Nguyen V (1983) A study of the yeast flora of medical interest in beach of Saint Anne in Guadeloupe. Bull Soc Pathol Exot Filiales 76:351–356

    CAS  Google Scholar 

  • Bolton F, Surman S, Martin K, Wareing D, Humphrey T (1999) Presence of Campylobacter and Salmonella in sand from bathing beaches. Epidemiol Infect 122:7–13

    CAS  Google Scholar 

  • Bonadonna L, De Mattia M, Liberti R, Volterra L (1993) Presenza e distribuzione di stafilococchi in ambienti marini [Presence and distribution of staphylococci in the marine environment]. Ig Mod 99:706–714

    Google Scholar 

  • Bonilla TD, Nowosielski K, Esiobu N, McCorquodale DS, Rogerson A (2006) Species assemblages of Enterococcus indicate potential sources of fecal bacteria at a south Florida recreational beach. Mar Pollut Bull 52:807–810

    CAS  Google Scholar 

  • Bonilla TD, Nowosielski K, Cuvelier M et al (2007) Prevalence and distribution of fecal indicator organisms in South Florida beach sand and preliminary assessment of health effects associated with beach sand exposure. Mar Pollut Bull 54:1472–1482

    CAS  Google Scholar 

  • Brandão J, Wergikosky B, Rosado C et al (2002) Relatório final do projecto “Qualidade Microbiológica de areias de Praias Litorais”. Associação Bandeira Azul da Europa

  • Brennan FP, O’Flaherty V, Kramers G, Grant J, Richards KG (2010) Long-term persistence and leaching of Escherichia coli in temperate maritime soils. Appl Environ Microbiol 76:1449–1455

    CAS  Google Scholar 

  • Burton GA Jr, Gunnison D, Lanza GR (1987) Survival of pathogenic bacteria in various freshwater sediments. Appl Environ Microbiol 53:633–638

    Google Scholar 

  • Byappanahalli MN, Fujioka RS (1998) Evidence that tropical soil environment can support the growth of Escherichia coli. Water Sci Technol 38:171–174

    CAS  Google Scholar 

  • Byappanahalli M, Fujioka R (2004) Indigenous soil bacteria and low moisture may limit but allow faecal bacteria to multiply and become a minor population in tropical soils. Water Sci Technol 50:27–32

    CAS  Google Scholar 

  • Byappanahalli M, Fowler M, Shively D, Whitman R (2003a) Ubiquity and persistence of Escherichia coli in a midwestern stream. Appl Environ Microbiol 69:4549–4555

    CAS  Google Scholar 

  • Byappanahalli MN, Shively DA, Nevers MB, Sadowsky MJ, Whitman RL (2003b) Growth and survival of Escherichia coli and enterococci populations in the macro-alga Cladophora (Chlorophyta). FEMS Microbiol Ecol 46:203–211

    CAS  Google Scholar 

  • Byappanahalli MN, Whitman RL, Shively DA, Sadowsky MJ, Ishii S (2006a) Population structure, persistence, and seasonality of autochthonous Escherichia coli in temperate, coastal forest soil from a Great Lakes watershed. Environ Microbiol 8:504–513

    CAS  Google Scholar 

  • Byappanahalli MN, Whitman RL, Shively DA, Ting WTE, Tseng CC, Nevers MB (2006b) Seasonal persistence and population characteristics of Escherichia coli and enterococci in deep backshore sand of two freshwater beaches. J Water Health 4:313–320

    Google Scholar 

  • Byappanahalli MN, Sawdey R, Ishii S, Shively DA, Ferguson J, Whitman RL, Sadowsky MJ (2009) Seasonal stability of Cladophora-associated Salmonella in Lake Michigan watersheds. Water Res 43:806–814

    CAS  Google Scholar 

  • Byappanahalli MN, Nevers MB, Korajkic A, Staley ZR, Harwood VJ (2012a) Enterococci in the environment: a review. Microbiol Mol Biol Rev 76:685–706

    CAS  Google Scholar 

  • Byappanahalli MN, Roll BM, Fujioka RS (2012b) Evidence for occurrence, persistence, and growth potential of Escherichia coli and enterococci in Hawaii’s soil environments. Microbes Environ 27:164–170

    Google Scholar 

  • Byappanahalli MN, Yan T, Hamilton MJ, Ishii S, Fujioka RS, Whitman RL (2012c) The population structure of Escherichia coli isolated from subtropical and temperate soils. Sci Total Environ 417–418:273–279. doi:10.1016/j.scitotenv.2011.12.041

    Google Scholar 

  • Carrillo-Muñoz A, Torres Rodríguez J, Madrenys-Brunet N, Dronda-Ayza A (1990) Comparative study on the survival of 5 species of dermatophytes and S. brevicaulis in beach sand, under laboratory conditions. Rev Iberoam Micol 7:36–38

    Google Scholar 

  • Chabasse D, Laine P, Simitzis-Le-Flohic A, Martineau B, Hourch ME, Becaud J (1986) Sanitary study of surface water and of the beach of a water sports and leisure complex. J Hyg 96:393–401

    CAS  Google Scholar 

  • Chase E, Harwood VJ (2011) Comparison of the effects of environmental parameters on growth rates of Vibrio vulnificus biotypes I, II, and III by culture and quantitative PCR analysis. Appl Environ Microbiol 77:4200–4207

    CAS  Google Scholar 

  • Chen G, Walker SL (2012) Fecal indicator bacteria transport and deposition in saturated and unsaturated porous media. Environ Sci Technol 46:8782–8790

    CAS  Google Scholar 

  • Converse RR, Kinzelman JL, Sams EA et al (2012) Dramatic improvements in beach water quality following gull removal. Environ Sci Technol 46:10206–10213

    CAS  Google Scholar 

  • Costerton JW, Cheng K, Geesey GG, Ladd TI, Nickel JC, Dasgupta M, Marrie TJ (1987) Bacterial biofilms in nature and disease. Ann Rev Microbiol 41:435–464

    CAS  Google Scholar 

  • Crowe AS, Meek GA (2009) Groundwater conditions beneath beaches of Lake Huron, Ontario, Canada. Aquat Ecosyst Health Manag 12:444–455

    Google Scholar 

  • Crowe AS, Milne J (2013) Relationship between dry and wet beach ecosystems and E. coli levels in groundwater below beaches of the Great Lakes, Canada. In: Ribeiro L, Stigter TY, Chambel A, de Melo MTC, Monteiro JP, Medeiros A (eds) Groundwater and ecosystems, vol 18, 1st edn. CRC Press, Leiden, pp 237–251

    Google Scholar 

  • Cui H, Yang K, Pagaling E, Yan T (2013) Spatial and temporal variation in enterococcal abundance and its relationship to the microbial community in Hawaii beach sand and water. Appl Environ Microbiol 79:3601–3609

    CAS  Google Scholar 

  • Cunningham AB, Characklis WG, Abedeen F, Crawford D (1991) Influence of biofilm accumulation on porous media hydrodynamics. Environ Sci Technol 25:1305–1311

    CAS  Google Scholar 

  • Dabrowa N, Landau J, Newcomer V, Plunkett O (1964) A survey of tide-washed coastal areas of southern California for fungi potentially pathogenic to man. Mycopathol Mycol Appl 24:137–150. doi:10.1007/bf02075556

    Google Scholar 

  • Dabrowski J (1982) Isolation of the Shigella genus bacteria from the beach sand and water of the bay of Gdańsk. Bull Inst Marit Trop Med Gdynia 33:49

    CAS  Google Scholar 

  • Davies CM, Long JAH, Donald M, Ashbolt NJ (1995) Survival of fecal microorganisms in marine and freshwater sediments. Appl Environ Microbiol 61:1888–1896

    CAS  Google Scholar 

  • Davies-Colley RJ, Bell RG, Donnison AM (1994) Sunlight inactivation of enterococci and fecal coliforms in sewage effluent diluted in seawater. Appl Environ Microbiol 60:2049–2058

    CAS  Google Scholar 

  • de Oliveira AJFC, Pinhata JMW (2008) Antimicrobial resistance and species composition of Enterococcus spp. isolated from waters and sands of marine recreational beaches in Southeastern Brazil. Water Res 42:2242–2250

    Google Scholar 

  • de Oliveira AJFC, de França PTR, Pinto AB (2010) Antimicrobial resistance of heterotrophic marine bacteria isolated from seawater and sands of recreational beaches with different organic pollution levels in southeastern Brazil: evidences of resistance dissemination. Environ Monit Assess 169:375–384

    Google Scholar 

  • de Sieyes NR, Yamahara KM, Layton BA, Joyce EH, Boehm AB (2008) Submarine discharge of nutrient-enriched fresh groundwater at Stinson Beach, California is enhanced during neap tides. Limnol Oceanogr 53:1434–1445

    Google Scholar 

  • de Sieyes NR, Yamahara KM, Paytan A, Boehm AB (2011) Submarine groundwater discharge to a high-energy surf zone at Stinson Beach, California, estimated using radium isotopes. Estuar Coasts 34:256–268

    CAS  Google Scholar 

  • Desmarais TR, Solo-Gabriele HM, Palmer CJ (2002) Influence of soil on fecal indicator organisms in a tidally influenced subtropical environment. Appl Environ Microbiol 68:1165–1172

    CAS  Google Scholar 

  • Díaz J, Rendueles M, Díaz M (2010) Straining phenomena in bacteria transport through natural porous media. Environ Sci Pollut Res 17:400–409

    Google Scholar 

  • Doorduyn Y, Van Den Brandhof W, Van Duynhoven Y, Wannet W, Van Pelt W (2006) Risk factors for Salmonella Enteritidis and Typhimurium (DT104 and non-DT104) infections in The Netherlands: predominant roles for raw eggs in Enteritidis and sandboxes in Typhimurium infections. Epidemiol Infect 134:617–626

    CAS  Google Scholar 

  • Dowidart A, Abdel-Monem MH (1990) Effect of chemical pollution on bacterial counts in El-Temsah Lake area, Ismailia, Egypt. J Egypt Public Health Assoc 65:305–328

    Google Scholar 

  • Dunkell DO, Bruland GL, Evensen CI, Walker MJ (2011) Effects of feral pig (Sus scrofa) exclusion on enterococci in runoff from the forested headwaters of a Hawaiian watershed. Water Air Soil Pollut 221:313–326

    CAS  Google Scholar 

  • Dunn AM, Silliman SE, Dhamwichukorn S, Kulpa CF (2005) Demonstration of microbial transport into the capillary fringe via advection from below the water table. J Hydrol 306:50–58

    Google Scholar 

  • Edge TA, Hill S (2007) Multiple lines of evidence to identify the sources of fecal pollution at a freshwater beach in Hamilton Harbour, Lake Ontario. Water Res 41:3585–3594

    CAS  Google Scholar 

  • Edge T, Hill S (2009) P315 Occurrence of ampicillin resistance in E. coli from Lake Ontario beaches and nearby sources of fecal pollution in the Toronto Hamilton area. Int J Antimicrob Agents 34:S125

    Google Scholar 

  • Edge TA, Hill S, Seto P, Marsalek J (2010) Library-dependent and library-independent microbial source tracking to identify spatial variation in faecal contamination sources along a Lake Ontario beach (Ontario, Canada). Water Sci Technol 62:719–727

    CAS  Google Scholar 

  • Elmanama AA, Fahd MI, Afifi S, Abdallah S, Bahr S (2005) Microbiological beach sand quality in Gaza Strip in comparison to seawater quality. Environ Res 99:1–10

    CAS  Google Scholar 

  • Elmir SM, Wright ME, Abdelzaher A et al (2007) Quantitative evaluation of bacteria released by bathers in a marine water. Water Res 41:3–10

    CAS  Google Scholar 

  • Elmir SM, Shibata T, Solo-Gabriele HM et al (2009) Quantitative evaluation of enterococci and Bacteroidales released by adults and toddlers in marine water. Water Res 43:4610–4616

    CAS  Google Scholar 

  • Enns AA, Vogel LJ, Abdelzaher AM et al (2012) Spatial and temporal variation in indicator microbe sampling is influential in beach management decisions. Water Res 46:2237–2246

    CAS  Google Scholar 

  • Esiobu N, Mohammed R, Echeverry A et al (2004) The application of peptide nucleic acid probes for rapid detection and enumeration of eubacteria, Staphylococcus aureus and Pseudomonas aeruginosa in recreational beaches of S. Florida. J Microbiol Methods 57:157–162

    CAS  Google Scholar 

  • Esiobu N, Green M, Echeverry A et al (2013) High numbers of Staphylococcus aureus at three bathing beaches in South Florida. Int J Environ Health Res 23:46–57. doi:10.1080/09603123.2012.699027

    Google Scholar 

  • Ettema R, Mutel CF (2004) Hans Albert Einstein: innovation and compromise in formulating sediment transport by rivers. J Hydraul Eng 130:477–487

    Google Scholar 

  • Feng F, Goto D, Yan T (2010) Effects of autochthonous microbial community on the die-off of fecal indicators in tropical beach sand. FEMS Microbiol Ecol 74:214–225

    CAS  Google Scholar 

  • Feng Z, Reniers A, Haus BK, Solo-Gabriele HM (2013) Modeling sediment-related enterococci loading, transport, and inactivation at an embayed nonpoint source beach. Water Resour Res 49:693–712

    CAS  Google Scholar 

  • Filipkowska Z, Janczukowicz W, Krzemieniewski M, Pesta J (2000) Microbiological air pollution in the surroundings of the wastewater treatment plant with activated-sludge tanks aerated by horizontal rotors. Pol J Environ Stud 9:273–280

    Google Scholar 

  • Flood C, Ufnar J, Wang S, Johnson J, Carr M, Ellender R (2011) Lack of correlation between enterococcal counts and the presence of human specific fecal markers in Mississippi creek and coastal waters. Water Res 45:872–878

    CAS  Google Scholar 

  • Fogarty LR, Haack SK, Wolcott MJ, Whitman RL (2003) Abundance and characteristics of the recreational water quality indicator bacteria Escherichia coli and enterococci in gull faeces. J Appl Microbiol 94:865–878

    CAS  Google Scholar 

  • Foppen JW, van Herwerden M, Schijven J (2007) Transport of Escherichia coli in saturated porous media: dual mode deposition and intra-population heterogeneity. Water Res 41:1743–1753

    CAS  Google Scholar 

  • Foppen JW, Lutterodt G, Röling WFM, Uhlenbrook S (2010) Towards understanding inter-strain attachment variations of Escherichia coli during transport in saturated quartz sand. Water Res 44:1202–1212

    CAS  Google Scholar 

  • Francy DS, Darner RA (1998) Factors affecting Escherichia coli concentrations at Lake Erie public bathing beaches. US Geological Survey, Columbus, OH

    Google Scholar 

  • Francy DS, Gifford AM, Darner RA (2003) Escherichia coli at Ohio bathing beaches—distribution, sources, wastewater indicators, and predictive modeling. U.S. Geological Survey, Columbus, OH

    Google Scholar 

  • Frenzel SA, Couvillion CS (2002) Fecal-indicator bacteria in streams along a gradient of residential development. J Am Water Resour Assoc 38:265–273

    Google Scholar 

  • Fries JS, Characklis GW, Noble RT (2006) Attachment of fecal indicator bacteria to particles in the Neuse River Estuary, NC. J Environ Eng 132:1338–1345

    CAS  Google Scholar 

  • Fujioka RS (2001) Monitoring coastal marine waters for spore-forming bacteria of faecal and soil origin to determine point from non-point source pollution. Water Sci Technol 44:181–188

    CAS  Google Scholar 

  • Fujioka RS, Byappanahalli MN (2003) Proceedings and report: tropical water quality indicator workshop, SR-2004-01. University of Hawaii, Water Resources Research Center, Honolulu, HI, pp 1–95

    Google Scholar 

  • Fujioka RS, Tenno K, Kansako S (1988) Naturally occurring fecal coliforms and fecal streptococci in Hawaii’s freshwater streams. Toxic Assess 3:613–630

    Google Scholar 

  • Fujioka R, Sian-Denton C, Borja M, Castro J, Morphew K (1999) Soil: the environmental source of Escherichia coli and enterococci in Guam’s streams. J Appl Microbiol Symp Suppl 85:83S–89S

    Google Scholar 

  • Gauthier F, Archibald F (2001) The ecology of fecal indicator bacteria commonly found in pulp and paper mill water systems. Water Res 35:2207–2218

    CAS  Google Scholar 

  • Ge Z, Nevers MB, Schwab DJ, Whitman RL (2010) Coastal loading and transport of Escherichia coli at an embayed beach in Lake Michigan. Environ Sci Technol 44:6731–6737

    CAS  Google Scholar 

  • Ge Z, Whitman RL, Nevers MB, Phanikumar MS (2012a) Wave-induced mass transport affects daily Escherichia coli fluctuations in nearshore water. Environ Sci Technol 46:2204–2211. doi:10.1021/es203847n

    CAS  Google Scholar 

  • Ge Z, Whitman RL, Nevers MB, Phanikumar MS, Byappanahalli MN (2012b) Evaluating the role of an embayed beach as a reservoir and a net source of fecal contamination. Limnol Oceanogr 57:362–381

    Google Scholar 

  • Ghinsberg RC, Bar Dov L, Rogol M, Sheinberg Y, Nitzan Y (1994) Monitoring of selected bacteria and fungi in sand and sea water along the Tel Aviv coast. Microbios 77:29–40

    CAS  Google Scholar 

  • Ghinsberg R, Dror R, Nitzan Y (1999) Isolation of Vibrio vulnificus from sea water and sand along the Dan region coast of the Mediterranean. Microbios 97:7–17

    CAS  Google Scholar 

  • Ginn TR, Wood BD, Nelson KE, Scheibe TD, Murphy EM, Clement TP (2002) Processes in microbial transport in the natural subsurface. Adv Water Resour 25:1017–1042

    CAS  Google Scholar 

  • Gobet A, Böer SI, Huse SM et al (2012) Diversity and dynamics of rare and of resident bacterial populations in coastal sands. ISME J 6:542–553

    Google Scholar 

  • Goodwin K, Pobuda M (2009) Performance of CHROMagar™ Staph aureus and CHROMagar™ MRSA for detection of Staphylococcus aureus in seawater and beach sand—comparison of culture, agglutination, and molecular analyses. Water Res 43:4802–4811

    CAS  Google Scholar 

  • Goodwin KD, Matragrano L, Wanless D, Sinigalliano CD, LaGier MJ (2009) A preliminary investigation of fecal indicator bacteria, human pathogens, and source tracking markers in beach water and sand. Environ Res J 3:395–417

    Google Scholar 

  • Goodwin KD, McNay M, Cao Y, Ebentier D, Madison M, Griffith JF (2012) A multi-beach study of Staphylococcus aureus, MRSA, and enterococci in seawater and beach sand. Water Res 46:4195–4207

    CAS  Google Scholar 

  • Gordon DM, Bauer S, Johnson JR (2002) The genetic structure of Escherichia coli populations in primary and secondary habitats. Microbiology 148:1513–1522

    CAS  Google Scholar 

  • Graczyk TK, Sunderland D, Tamang L, Lucy FE, Breysse PN (2007) Bather density and levels of Cryptosporidium, Giardia, and pathogenic microsporidian spores in recreational bathing water. Parasitol Res 101:1729–1731

    Google Scholar 

  • Grant SB, Sanders B, Boehm A et al (2001) Generation of enterococci bacteria in a coastal saltwater marsh and its impact on surf zone water quality. Environ Sci Technol 35:2407–2416

    CAS  Google Scholar 

  • Grimes D, Atwell R, Brayton P et al (1986) The fate of enteric pathogenic bacteria in estuarine and marine environments. Microbiol Sci 3:324

    CAS  Google Scholar 

  • Grisoli P, Rodolfi M, Villani S et al (2009) Assessment of airborne microorganism contamination in an industrial area characterized by an open composting facility and a wastewater treatment plant. Environ Res 109:135–142

    CAS  Google Scholar 

  • Haack SK, Fogarty LR, Wright C (2003) Escherichia coli and enterococci at beaches in the Grand Traverse Bay, Lake Michigan: sources, characteristics, and environmental pathways. Environ Sci Technol 37:3275–3282

    CAS  Google Scholar 

  • Halliday E, Gast RJ (2011) Bacteria in beach sands: an emerging challenge in protecting coastal water quality and bather health. Environ Sci Technol 45:370–379

    CAS  Google Scholar 

  • Hall-Stoodley L, Costerton JW, Stoodley P (2004) Bacterial biofilms: from the natural environment to infectious diseases. Nat Rev Microbiol 2:95–108

    CAS  Google Scholar 

  • Hamilton MJ, Hadi AZ, Griffith JF, Ishii S, Sadowsky MJ (2010) Large scale analysis of virulence genes in Escherichia coli strains isolated from Avalon Bay, CA. Water Res 44:5463–5473

    CAS  Google Scholar 

  • Hansen DL, Ishii S, Sadowsky MJ, Hicks RE (2011) Waterfowl abundance does not predict the dominant avian source of beach. J Environ Qual 40:1924–1931

    CAS  Google Scholar 

  • Hardina CM, Fujioka RS (1991) Soil: the environmental source of Escherichia coli and enterococci in Hawaii’s streams. Environ Toxicol Water Qual 6:185–195

    Google Scholar 

  • Harrison S, Kinra S (2004) Outbreak of Escherichia coli O157 associated with a busy bathing beach. Commun Dis Public Health 7:47–50

    CAS  Google Scholar 

  • Hartke A, Lemarinier S, Pichereau V, Auffray Y (2002) Survival of Enterococcus faecalis in seawater microcosms is limited in the presence of bacterivorous zooflagellates. Curr Microbiol 44:329–335

    CAS  Google Scholar 

  • Health Canada (2012) Guidelines for Canadian recreational water quality, 3rd edn. Health Canada, Ottawa, ON

    Google Scholar 

  • Heaney C, Sams E, Wing S, Marshall S, Brenner K, Dufour AP, Wade TJ (2009) Contact with beach sand among beachgoers and risk of illness. Am J Epidemiol 170:164–172

    Google Scholar 

  • Heaney CD, Sams E, Dufour AP et al (2012) Fecal indicators in sand, sand contact, and risk of enteric illness among beachgoers. Epidemiology 23:95–106

    Google Scholar 

  • Heim S, Lleo MM, Bonato B, Guzman CA, Canepari P (2002) The viable but nonculturable state and starvation are different stress responses of Enterococcus faecalis, as determined by proteome analysis. J Bacteriol 184:6739–6745

    CAS  Google Scholar 

  • Hussong D, Damare J, Limpert RJ, Sladen W, Weiner RM, Colwell RR (1979) Microbial impact of Canada geese (Branta canadensis) and whistling swans (Cygnus columbianus columbianus) on aquatic ecosystems. Appl Environ Microbiol 37:14–20

    CAS  Google Scholar 

  • Imamura GJ, Thompson RS, Boehm AB, Jay JA (2011) Wrack promotes the persistence of fecal indicator bacteria in marine sands and seawater. FEMS Microbiol Ecol 77:40–49

    CAS  Google Scholar 

  • Inman D, Tait R, Nordstrom C (1971) Mixing in the surf zone. J Geophys Res 76:3493–3514

    Google Scholar 

  • Ishii S, Sadowsky MJ (2008) Escherichia coli in the environment: implications for water quality and human health. Microbes Environ 23:101–108

    Google Scholar 

  • Ishii S, Ksoll WB, Hicks RE, Sadowsky MJ (2006) Presence and growth of naturalized Escherichia coli in temperate soils from Lake Superior watersheds. Appl Environ Microbiol 72:612–621

    CAS  Google Scholar 

  • Ishii S, Hansen DL, Hicks RE, Sadowsky MJ (2007) Beach sand and sediments are temporal sinks and sources of Escherichia coli in Lake Superior. Environ Sci Technol 41:2203–2209

    CAS  Google Scholar 

  • Ishii S, Yan T, Vu H, Hansen D, Hicks R, Sadowsky M (2010) Factors controlling long-term survival and growth of naturalized Escherichia coli populations in temperate field soils. Microbes Environ 25:8–14

    Google Scholar 

  • Izquierdo J, Piera G, Aledany M, Lucena F (1986) Estudio de la flora fungica de la arena de la playa de Barcelona [A study of the fungal flora of the beaches in Barcelona]

  • Johnson WP, Li X, Assemi S (2007) Deposition and re-entrainment dynamics of microbes and non-biological colloids during non-perturbed transport in porous media in the presence of an energy barrier to deposition. Adv Water Resour 30:1432–1454

    Google Scholar 

  • Jousset A (2012) Ecological and evolutive implications of bacterial defences against predators. Environ Microbiol 14:1830–1843

    Google Scholar 

  • Kaper JB, Nataro JP, Mobley HLT (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2:123–140

    CAS  Google Scholar 

  • Khan IUH, Hill S, Nowak E, Palmer ME, Jarjanazi H, Lee D-Y, Mueller M, Schop R, Weir S, Abbey A-M, Winter J, Edge TA (2013a). Investigation on the prevalence of thermophilic Campylobacter species at Lake Simcoe recreational beaches. Inland Waters 3:93–104

  • Khan IU, Hill S, Nowak E, Edge TA (2013b) Effect of incubation temperature on the detection of thermophilic Campylobacter species from freshwater beaches, nearby wastewater effluents, and bird fecal droppings. Appl Environ Microbiol 79:7639–7645

  • Khan IUH, Loughborough A, Edge TA (2009) DNA-based real-time detection and quantification of aeromonads from fresh water beaches on Lake Ontario. J Water Health 7:312–323

    CAS  Google Scholar 

  • Khiyama HM, Makemson JC (1973) Sand beach bacteria: enumeration and characterization. Appl Microbiol 26:293–297

    CAS  Google Scholar 

  • Kinzelman J, McLellan SL (2009) Success of science-based best management practices in reducing swimming bans—a case study from Racine, Wisconsin, USA. Aquat Ecosyst Health Manag 12:187–196

    Google Scholar 

  • Kinzelman J, Whitman RL, Byappanahalli MN, Jackson EK, Bagley RC (2003) Evaluation of beach grooming techniques on Escherichia coli density in foreshore sand at North Beach, Racine, WI. Lake Reserv Manag 19:349–354

    CAS  Google Scholar 

  • Kinzelman J, Pond K, Longmaid K, Bagley R (2004) The effect of two mechanical beach grooming strategies on Escherichia coli density in beach sand at a southwestern Lake Michigan beach. Aquat Ecosyst Health Manag 7:425–432

    Google Scholar 

  • Kinzelman J, McLellan SL, Amick A et al (2008) Identification of human enteric pathogens in gull feces at Southwestern Lake Michigan bathing beaches. Can J Microbiol 54:1006–1015

    CAS  Google Scholar 

  • Kishimoto RA, Baker GE (1969) Pathogenic and potentially pathogenic fungi isolated from beach sands and selected soils of Oahu, Hawaii. Mycologia 61(3):537–548

  • Kleinheinz GT, McDermott CM, Hughes S, Brown A (2009) Effects of rainfall on E. coli concentrations at Door County, Wisconsin beaches. Int J Microbiol, Article ID 876050. doi:10.1155/2009/876050

  • Kon T, Weir SC, Howell ET, Lee H, Trevors JT (2007) Genetic relatedness of Escherichia coli isolates in interstitial water from a Lake Huron (Canada) beach. Appl Environ Microbiol 73:1961–1967

    CAS  Google Scholar 

  • Korajkic A, McMinn BR, Harwood VJ, Shanks OC, Fout GS, Ashbolt NJ (2013) Differential decay of enterococci and Escherichia coli originating from two fecal pollution sources. Appl Environ Microbiol 79:2488–2492

    CAS  Google Scholar 

  • Kostka JE, Prakash O, Overholt WA et al (2011) Hydrocarbon-degrading bacteria and the bacterial community response in Gulf of Mexico beach sands impacted by the Deepwater Horizon oil spill. Appl Environ Microbiol 77:7962–7974

    CAS  Google Scholar 

  • Ksoll WB, Ishii S, Sadowsky MJ, Hicks RE (2007) Presence and sources of fecal coliform bacteria in epilithic periphyton communities of Lake Superior. Appl Environ Microbiol 73:3771–3778

    CAS  Google Scholar 

  • LaLiberte P, Grimes DJ (1982) Survival of Escherichia coli in lake bottom sediment. Appl Environ Microbiol 43:623–628

    CAS  Google Scholar 

  • Larrondo JV, Calvo MA (1989) Fungal density in the sands of the Mediterranean coast beaches. Mycopathologia 108:185–193

    CAS  Google Scholar 

  • Lavender JS, Kinzelman JL (2009) A cross comparison of QPCR to agar-based or defined substrate test methods for the determination of Escherichia coli and enterococci in municipal water quality monitoring programs. Water Res 43:4967–4979

    CAS  Google Scholar 

  • Lee CM, Lin TY, Lin CC, Kohbodi GA, Bhatt A, Lee R, Jay JA (2006) Persistence of fecal indicator bacteria in Santa Monica Bay beach sediments. Water Res 40:2593–2602

    CAS  Google Scholar 

  • Lévesque B, Brousseau P, Simard P, Dewailly E, Meisels M, Ramsay D, Joly J (1993) Impact of the ring-billed gull (Larus delawarensis) on the microbiological quality of recreational water. Appl Environ Microbiol 59:1228–1230

    Google Scholar 

  • Levin-Edens E, Bonilla N, Meschke JS, Roberts MC (2011) Survival of environmental and clinical strains of methicillin-resistant Staphylococcus aureus [MRSA] in marine and fresh waters. Water Res 45:5681–5686

    CAS  Google Scholar 

  • Levin-Edens E, Soge OO, No D, Stiffarm A, Meschke JS, Roberts MC (2012) Methicillin-resistant Staphylococcus aureus from Northwest marine and freshwater recreational beaches. FEMS Microbiol Ecol 79:412–420. doi:10.1111/j.1574-6941.2011.01229.x

    CAS  Google Scholar 

  • Li L, Barry D, Pattiaratchi C, Masselink G (2002) BeachWin: modelling groundwater effects on swash sediment transport and beach profile changes. Environ Model Softw 17:313–320

    Google Scholar 

  • Logan AJ, Stevik TK, Siegrist RL, Rønn RM (2001) Transport and fate of Cryptosporidium parvum oocysts in intermittent sand filters. Water Res 35:4359–4369

    CAS  Google Scholar 

  • Lovins K, Angle J, Wiebers J, Hill R (1993) Leaching of Pseudomonas aeruginosa, and transconjugants containing pR68. 45 through unsaturated, intact soil columns. FEMS Microbiol Ecol 13:105–111

    CAS  Google Scholar 

  • Lozupone CA, Knight R (2007) Global patterns in bacterial diversity. Proc Natl Acad Sci 104:11436–11440

    CAS  Google Scholar 

  • Mallin MA, Williams KE, Esham EC, Lowe RP (2000) Effect of human development on bacteriological water quality in coastal watersheds. Ecol Appl 10:1047–1056

    Google Scholar 

  • Marino F, Morinigo M, Martinez-Manzanares E, Borrego J (1995) Microbiological-epidemiological study of selected marine beaches in Malaga (Spain). Water Sci Technol 31:5–9

    Google Scholar 

  • Marsalek J, Rochfort Q (2004) Urban wet-weather flows: sources of fecal contamination impacting on recreational waters and threatening drinking-water sources. J Toxicol Environ Health Part A 67:1765–1777

    CAS  Google Scholar 

  • McCambridge J, McMeekin TA (1980) Relative effects of bacterial and protozoan predators on survival of Escherichia coli in estuarine water samples. Appl Environ Microbiol 40:907–911

    CAS  Google Scholar 

  • Mendes B, Nascimento MJ, Oliveira JS (1993) Preliminary characterization and proposal of microbiological quality standard of sand beaches. Water Sci Technol 27:453–456

    Google Scholar 

  • Mendes B, Urbano P, Alves C, Lapa N, Morais J, Nascimento J, Oliveira J (1997) Sanitary quality of sands from beaches of Azores islands. Water Sci Technol 35:147–150

    Google Scholar 

  • Mika KB, Imamura G, Chang C et al (2009) Pilot- and bench-scale testing of fecal indicator bacteria survival in marine beach sand near point sources. J Appl Microbiol 107:72–84

    CAS  Google Scholar 

  • Mohammed R, Echeverry A, Stinson C et al (2012) Survival trends of Staphylococcus aureus, Pseudomonas aeruginosa, and Clostridium perfringens in a sandy South Florida beach. Mar Pollut Bull 64:1201

    CAS  Google Scholar 

  • Mudryk Z, Perliński P, Skórczewski P (2010) Detection of antibiotic resistant bacteria inhabiting the sand of non-recreational marine beach. Mar Pollut Bull 60:207–214

    CAS  Google Scholar 

  • Mudryk ZJ, Kosiorek A, Perliński P (2013) In vitro antibiotic resistance of Vibrio-like organisms isolated from seawater and sand of marine recreation beach in the southern Baltic Sea. Hydrobiologia 702:141–150. doi:10.1007/s10750-012-1317-4

    CAS  Google Scholar 

  • Murphy EM, Ginn TR (2000) Modeling microbial processes in porous media. Hydrogeol J 8:142–158

    Google Scholar 

  • Neel JK (1948) A limnological investigation of the psammon in Douglas Lake, Michigan, with especial reference to shoal and shoreline dynamics. Trans Am Microsc Soc 67(1):1–53

  • Nestor I, Costin-Lazår L, Sovrea D, Ionescu N (1984) Detection of enteroviruses in seawater and beach sand. Zentralblatt für Bakteriologie, Mikrobiologie und Hygiene 1 Abt Originale B. Hygiene 178:527–534

    CAS  Google Scholar 

  • Nielsen P (1992) Coastal bottom boundary layers and sediment transport, vol 4. World Scientific Publishing Company Incorporated, Singapore

    Google Scholar 

  • Noble RT, Griffith JF, Blackwood AD et al (2006) Multitiered approach using quantitative PCR to track sources of fecal pollution affecting Santa Monica Bay, California. Appl Environ Microbiol 72:1604–1612

    CAS  Google Scholar 

  • Obiri-Danso K, Jones K (1999) Distribution and seasonality of microbial indicators and thermophilic campylobacters in two freshwater bathing sites on the River Lune in northwest England. J Appl Microbiol 87:822–832

    CAS  Google Scholar 

  • Obiri-Danso K, Jones K (2000) Intertidal sediments as reservoirs for hippurate negative campylobacters, salmonellae and faecal indicators in three EU recognised bathing waters in north west England. Water Res 34:519–527

    CAS  Google Scholar 

  • Olapade OA, Depas MM, Jensen ET, McLellan SL (2006) Microbial communities and fecal indicator bacteria associated with Cladophora mats on beach sites along Lake Michigan shores. Appl Environ Microbiol 72:1932–1938

    CAS  Google Scholar 

  • Oliver JD (2010) Recent findings on the viable but nonculturable state in pathogenic bacteria. FEMS Microbiol Rev 34:415–425

    CAS  Google Scholar 

  • Oshiro R, Fujioka R (1995) Sand, soil, and pigeon droppings: sources of indicator bacteria in the waters of Hanauma Bay, Oahu. Hawaii Water Sci Technol 31:251–254

    Google Scholar 

  • Ostrolenk M, Kramer N, Cleverdon RC (1947) Comparative studies of enterococci and Escherichia coli as indices of pollution. J Bacteriol 53:197–203

    CAS  Google Scholar 

  • Palmer M (1988) Bacterial loadings from resuspended sediments in recreational beaches. Can J Civ Eng 15:450–455

    Google Scholar 

  • Papadakis JA, Mavridou A, Richardson SC, Lampiri M, Marcelou U (1997) Bather-related microbial and yeast populations in sand and seawater. Water Res 31:799–804

    CAS  Google Scholar 

  • Perkins S, Gyr P, James G (2000) The influence of biofilm on the mechanical behavior of sand. ASTM Geotech Test J 23:300–312

    Google Scholar 

  • Phillips MC, Solo-Gabriele HM, Piggot AM, Klaus JS, Zhang YJ (2011a) Relationships between sand and water quality at recreational beaches. Water Res 45:6763–6769

    CAS  Google Scholar 

  • Phillips MC, Solo-Gabriele HM, Reniers AJ, Wang JD, Kiger RT, Abdel-Mottaleb N (2011b) Pore water transport of enterococci out of beach sediments. Mar Pollut Bull 62:2293–2298

    CAS  Google Scholar 

  • Pianetti A, Bruscolini F, Sabatini L, Colantoni P (2004) Microbial characteristics of marine sediments in bathing area along Pesaro-Gabicce coast (Italy): a preliminary study. J Appl Microbiol 97:682–689

    CAS  Google Scholar 

  • Piggot AM, Klaus JS, Johnson S, Phillips MC, Solo-Gabriele HM (2012) Relationship between enterococcal levels and sediment biofilms at recreational beaches in South Florida. Appl Environ Microbiol 78:5973–5982

    CAS  Google Scholar 

  • Plano LRW, Garza AC, Shibata T et al (2011) Shedding of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus from adult and pediatric bathers in marine waters. BMC Microbiol 11:5

    Google Scholar 

  • Pommepuy M, Butin M, Derrien A, Gourmelon M, Colwell R, Cormier M (1996) Retention of enteropathogenicity by viable but nonculturable Escherichia coli exposed to seawater and sunlight. Appl Environ Microbiol 62:4621–4626

    CAS  Google Scholar 

  • Power ML, Littlefield-Wyer J, Gordon DM, Veal DA, Slade MB (2005) Phenotypic and genotypic characterization of encapsulated Escherichia coli isolated from blooms in two Australian lakes. Environ Microbiol 7:631–640

    CAS  Google Scholar 

  • Prado B, Bernal P, Contreras M, Saavedra M, Del Moral A, Joyas A (1994) Numerical taxonomy of staphylococci isolated from water and beach sand from Valparaíso and viña del Mar, Chile. Rev Latinoam Microbiol 36:71

    CAS  Google Scholar 

  • Price W, Burchell M II, Hunt W, Chescheir G (2013) Long-term study of dune infiltration systems to treat coastal stormwater runoff for fecal bacteria. Ecol Eng 52:1–11

    Google Scholar 

  • Rijnaarts HHM, Norde W, Bouwer EJ, Lyklema J, Zehnder AJB (1996) Bacterial deposition in porous media related to the clean bed collision efficiency and to substratum blocking by attached cells. Environ Sci Technol 30:2869–2876

    CAS  Google Scholar 

  • Ripp S, Nivens DE, Werner C, Sayler GS (2001) Vertical transport of a field-released genetically engineered microorganism through soil. Soil Biol Biochem 33:1873–1877

    CAS  Google Scholar 

  • Rivera S, Hazen T, Toranzos G (1988) Isolation of fecal coliforms from pristine sites in a tropical rain forest. Appl Environ Microbiol 54:513–517

    CAS  Google Scholar 

  • Roberts MC, Soge OO, Giardino MA, Mazengia E, Ma G, Meschke JS (2009) Vancomycin-resistant Enterococcus spp. in marine environments from the West Coast of the USA. J Appl Microbiol 107:300–307

    CAS  Google Scholar 

  • Robertson JB, Edberg SC (1997) Natural protection of spring and well drinking water against surface microbial contamination. I. Hydrogeological parameters. Crit Rev Microbiol 23:143–178

    CAS  Google Scholar 

  • Romero OC, Straub AP, Kohn T, Nguyen TH (2011) Role of temperature and Suwannee river natural organic matter on inactivation kinetics of rotavirus and bacteriophage MS2 by solar irradiation. Environ Sci Technol 45:10385–10393

    CAS  Google Scholar 

  • Roses Codinachs M, Isern Vins AM, Ferrer Escobar MD, Fernandez Perez F (1988) Microbiological contamination of the sand from the Barcelona city beaches. Rev Sanid Hig Publica 62:1537–1544

    CAS  Google Scholar 

  • Ross N, Villemur R, Deschênes L, Samson R (2001) Clogging of a limestone fracture by stimulating groundwater microbes. Water Res 35:2029–2037

    CAS  Google Scholar 

  • Rusch A, Huettel M, Reimers CE, Taghon GL, Fuller CM (2003) Activity and distribution of bacterial populations in Middle Atlantic Bight shelf sands. FEMS Microbiol Ecol 44:89–100

    CAS  Google Scholar 

  • Russell TL, Yamahara KM, Boehm AB (2012) Mobilization and transport of naturally occurring enterococci in beach sands subject to transient infiltration of seawater. Environ Sci Technol 46:5988–5996

    CAS  Google Scholar 

  • Russell TL, Sassoubre LM, Wang D et al (2013) A Coupled Modeling and Molecular Biology Approach to Microbial Source Tracking at Cowell Beach, Santa Cruz, CA, United States. Environ Sci Technol 47:10231–10239

    CAS  Google Scholar 

  • Sabino R, Sampaio P, Carneiro C, Rosado L, Pais C (2011a) Isolates from hospital environments are the most virulent of the Candida parapsilosis complex. BMC Microbiol 11:180

    Google Scholar 

  • Sabino R, Veríssimo C, Cunha MA et al (2011b) Pathogenic fungi: an unacknowledged risk at coastal resorts? New insights on microbiological sand quality in Portugal. Mar Pollut Bull 62:1506–1511

    CAS  Google Scholar 

  • Salmore A, Hollis E, McLellan S (2006) Delineation of a chemical and biological signature for stormwater pollution in an urban river. J Water Health 4:247–262

    CAS  Google Scholar 

  • Sampson RW, Swiatnicki SA, Osinga VL, Supita JL, McDermott CM, Kleinheinz GT (2006) Effects of temperature and sand on E. coli survival in a northern lake water microcosm. J Water Health 4:389–393

    Google Scholar 

  • Sanchez PS, Agudo EG, Castro FG, Alves MN, Martins MT (1986) Evaluation of the sanitary quality of marine recreational waters and sands from beaches of the São Paulo State, Brazil. Water Sci Technol 18:61–72

    CAS  Google Scholar 

  • Sato MIZ, Di Bari M, Lamparelli CC, Truzzi AC, Coelho MCLS, Hachich EM (2005) Sanitary quality of sands from marine recreational beaches of São Paulo, Brazil. Braz J Microbiol 36:321–326

    Google Scholar 

  • Sauer EP, VandeWalle JL, Bootsma MJ, McLellan SL (2011) Detection of the human specific Bacteroides genetic marker provides evidence of widespread sewage contamination of stormwater in the urban environment. Water Res 45:4081–4091

    CAS  Google Scholar 

  • Schuch AP, Menck CFM (2010) The genotoxic effects of DNA lesions induced by artificial UV-radiation and sunlight. J Photochem Photobiol B 99:111–116

    CAS  Google Scholar 

  • Seyfried PL, Tobin RS, Brown NE, Ness PF (1985) A prospective study of swimming-related illness. II. Morbidity and microbiologial quality of water. Am J Public Health 75:1071–1075

    CAS  Google Scholar 

  • Shah AH, Abdelzaher AM, Phillips M et al (2011) Indicator microbes correlate with pathogenic bacteria, yeasts and helminthes in sand at a subtropical recreational beach site. J Appl Microbiol 110:1571–1583

    CAS  Google Scholar 

  • Shatti JA, Abdullah THA (1999) Marine pollution due to wastewater discharge in Kuwait. Water Sci Technol 40:33–39

    Google Scholar 

  • Shibata T, Solo-Gabriele HM (2012) Quantitative microbial risk assessment of human illness from exposure to marine beach sand. Environ Sci Technol 46:2799–2805. doi:10.1021/es203638x

    CAS  Google Scholar 

  • Sinigalliano CD, Gidley M, Shibata T et al (2007) Impacts of Hurricanes Katrina and Rita on the microbial landscape of the New Orleans area. Proc Natl Acad Sci 104:9029–9034

    CAS  Google Scholar 

  • Skalbeck JD, Kinzelman JL, Mayer GC (2010) Fecal indicator organism density in beach sands: impact of sediment grain size, uniformity, and hydrologic factors on surface water loading. J Great Lakes Res 36:707–714

    Google Scholar 

  • Soge OO, Meschke JS, No DB, Roberts MC (2009) Characterization of methicillin-resistant Staphylococcus aureus and methicillin-resistant coagulase-negative Staphylococcus spp. isolated from US West Coast public marine beaches. J Antimicrob Chemother 64:1148–1155

    CAS  Google Scholar 

  • Solo-Gabriele HM, Wolfert MA, Desmarais TR, Palmer CJ (2000) Sources of Escherichia coli in a coastal subtropical environment. Appl Environ Microbiol 66:230–237

    CAS  Google Scholar 

  • Sousa MLR (1990) Micoses. [Fungi.] National Institute of Health (INSA), Centre of Epidemiologic Surveillance of Transmissible Diseases (Epidemiology Bulletin No. 5), Lisbon

  • Staff M, Musto J, Hogg G, Janssen M, Rose K (2012) Salmonellosis outbreak traced to playground sand, Australia, 2007–2009. Emerg Infect Dis 18:1159–1161

    Google Scholar 

  • Stevens JL, Evans GE, Aguirre KM (2012) Human beach use affects abundance and identity of fungi present in sand. J Coast Res 28:787–792

    Google Scholar 

  • Stocker R (2012) Marine microbes see a sea of gradients. Science 338:628–633

    CAS  Google Scholar 

  • Suter E, Juhl AR, O’Mullan GD (2011) Particle association of Enterococcus and total bacteria in the lower Hudson River estuary, USA. J Water Resour Prot 3:715–725

    CAS  Google Scholar 

  • Sutherland BM (1981) Photoreactivation. BioScience 31:439–444

    CAS  Google Scholar 

  • Tiefenthaler L, Stein E, Schiff K (2011) Levels and patterns of fecal indicator bacteria in stormwater runoff from homogenous land use sites and urban watersheds. J Water Health 9:279–290

    CAS  Google Scholar 

  • Twinning TL, Whitman RL, Hoff BE (1993) Occurrence of E. coli in open beach groundwaters of Indiana Dunes National Lakeshore. In: 109th annual meeting of the Indiana Academy of Science, West Lafayette, Indiana

  • US EPA (2008) Cruise ship discharge assessment report. EPA 842-R-07-005. U.S. Environmental Protection Agency, Office of Water, Washington, DC

  • Vally H, Whittle A, Cameron S, Dowse GK, Watson T (2004) Outbreak of Aeromonas hydrophila wound infections associated with mud football. Clin Infect Dis 38:1084–1089

    Google Scholar 

  • Van Donsel DJ, Geldreich EE, Clarke NA (1967) Seasonal variations in survival of indicator bacteria in soil and their contribution to storm-water pollution. Appl Microbiol 15:1362–1370

    Google Scholar 

  • Vanden Heuvel A, McDermott C, Pillsbury R et al (2010) The green alga, Cladophora, promotes E. coli growth and contamination of recreational waters in Lake Michigan. J Environ Qual 39:333–344

    CAS  Google Scholar 

  • Vieira RHSF, Rodrigues DP, Menezes EA, Evangelista NSS, Reis EMF, Barreto LM, Gonçalves FA (2001) Microbial contamination of sand from major beaches in Fortaleza, Ceará State, Brazil. Braz J Microbiol 32:77–80

    Google Scholar 

  • Vijayavel K, Fujioka R, Ebdon J, Taylor H (2010) Isolation and characterization of the Bacteroides host strain HB-73 used to detect sewage specific phases in Hawaii. Water Res 44:3714–3724

    CAS  Google Scholar 

  • Vijayavel K, Sadowsky MJ, Ferguson JA, Kashian DR (2013) The establishment of the nuisance cyanobacteria Lyngbya wollei in Lake St. Clair and its potential to harbor fecal indicator bacteria. J Great Lakes Res 39:560–568

    Google Scholar 

  • Vogel C, Rogerson A, Schatz S, Laubach H, Tallman A, Fell J (2007) Prevalence of yeasts in beach sand at three bathing beaches in South Florida. Water Res 41:1915–1920

    CAS  Google Scholar 

  • Walk ST, Alm EW, Calhoun LM, Mladonicky JM, Whittamn TS (2007) Genetic diversity and population structure of Escherichia coli isolated from freshwater beaches. Environ Microbiol 9:2274–2288

    Google Scholar 

  • Wang A, Lin B, Sleep BE, Liss SN (2011) The impact of biofilm growth on transport of Escherichia coli O157: H7 in sand. Ground Water 49:20–31

    CAS  Google Scholar 

  • Wanjugi P, Harwood VJ (2013) The influence of predation and competition on the survival of commensal and pathogenic fecal bacteria in aquatic habitats. Environ Microbiol 15:517–526

    Google Scholar 

  • Weinzirl J, Newton EB (1915) The fate of bacteria in frozen meat held in cold storage, and its bearing on a bacteriological standard for condemnation. Am J Public Health 5:833–835

    CAS  Google Scholar 

  • Whitlock JE, Jones DT, Harwood VJ (2002) Identification of the sources of fecal coliforms in an urban watershed using antibiotic resistance analysis. Water Res 36:4273–4282

    CAS  Google Scholar 

  • Whitman RL, Nevers MB (2003) Foreshore sand as a source of Escherichia coli in nearshore water of a Lake Michigan beach. Appl Environ Microbiol 69:5555–5562

    CAS  Google Scholar 

  • Whitman RL, Horvath TG, Goodrich ML, Nevers MB, Wolcott MJ, Haack SK (2001) Characterization of E. coli levels at 63rd street beach. Report to the City of Chicago, Department of the Environment and the Chicago Park District, Chicago, IL

  • Whitman RL, Shively DA, Pawlik H, Nevers MB, Byappanahalli MN (2003) Occurrence of Escherichia coli and enterococci in Cladophora (Chlorophyta) in nearshore water and beach sand of Lake Michigan. Appl Environ Microbiol 69:4714–4719

    CAS  Google Scholar 

  • Whitman RL, Nevers MB, Korinek GC, Byappanahalli MN (2004) Solar and temporal effects on Escherichia coli concentration at a Great Lakes swimming beach. Appl Environ Microbiol 70:4276–4285

    CAS  Google Scholar 

  • Whitman RL, Byers SE, Shively DA, Ferguson DM, Byappanahalli MN (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

    CAS  Google Scholar 

  • Whitman RL, Nevers MB, Byappanahalli MN (2006) Examination of the watershed-wide distribution of Escherichia coli along southern Lake Michigan: an integrated approach. Appl Environ Microbiol 72:7301–7310

    CAS  Google Scholar 

  • Whitman RL, Przybyla-Kelly K, Shively DA, Nevers MB, Byappanahalli MN (2009) Hand-mouth transfer and potential for exposure to E. coli and F + coliphage in beach sand, Chicago, IL. J Water Health 7:623–629. doi:10.2166/wh.2009.115

    Google Scholar 

  • Williams AP, Avery LM, Killham K, Jones DL (2007) Persistence, dissipation, and activity of Escherichia coli O157:H7 within sand and seawater environments. FEMS Microbiol Ecol 60:24–32

    CAS  Google Scholar 

  • Woessner WW, Ball PN, DeBorde DC, Troy TL (2005) Viral transport in a sand and gravel aquifer under field pumping conditions. Ground Water 39:886–894

    Google Scholar 

  • World Health Organization (2003) Microbial aspects of beach sand quality. In: Guidelines for safe recreational water environments: coastal and fresh waters, vol 1, coastal and fresh waters. World Health Organization, Geneva, Switzerland, pp 118–127

  • Wright ME, Solo-Gabriele HM, Elmir S, Fleming LE (2009) Microbial load from animal feces at a recreational beach. Mar Pollut Bull 58:1649–1656

    CAS  Google Scholar 

  • Wright M, Abdelzaher A, Solo-Gabriele H, Elmir S, Fleming L (2011) The inter-tidal zone is the pathway of input of enterococci to a subtropical recreational marine beach. Water Sci Technol 63:542–549

    CAS  Google Scholar 

  • Xin P, Robinson C, Li L, Barry DA, Bakhtyar R (2010) Effects of wave forcing on a subterranean estuary. Water Resour Res 46:W12505

    Google Scholar 

  • Yallop M, Paterson D, Wellsbury P (2000) Interrelationships between rates of microbial production, exopolymer production, microbial biomass, and sediment stability in biofilms of intertidal sediments. Microb Ecol 39:116–127

    CAS  Google Scholar 

  • Yamahara KM, Layton BA, Santoro AE, Boehm AB (2007) Beach sands along the California coast are diffuse sources of fecal bacteria to coastal waters. Environ Sci Technol 41:4515–4521

    CAS  Google Scholar 

  • Yamahara KM, Walters SP, Boehm AB (2009) Growth of enterococci in unaltered, unseeded beach sands subjected to tidal wetting. Appl Environ Microbiol 75:1517–1524

    CAS  Google Scholar 

  • Yamahara KM, Sassoubre LM, Goodwin KD, Boehm AB (2012) Occurrence and persistence of bacterial pathogens and indicator organisms in beach sand along the California coast. Appl Environ Microbiol 78:1733–1745

    CAS  Google Scholar 

  • Zehms TT, McDermott CM, Kleinheinz GT (2008) Microbial concentrations in sand and their effect on beach water in Door County, Wisconsin. J Great Lakes Res 34:524–534

    CAS  Google Scholar 

  • Zhang Q, Yan T (2012) Correlation of intracellular trehalose concentration with desiccation resistance of soil Escherichia coli populations. Appl Environ Microbiol 78:7407–7413. doi:10.1128/aem.01904-12

    CAS  Google Scholar 

  • Zhu X, Wang JD, Solo-Gabriele HM, Fleming LE (2011) A water quality modeling study of non-point sources at recreational marine beaches. Water Res 45:2985–2995

    CAS  Google Scholar 

Download references

Acknowledgments

This paper is a direct outcome of “Linking Fecal Indicator Bacteria in Beach Sand and Water” Workshop held during the 2011 Great Lakes Beach Association Conference, Michigan City, IN; September 26–28. We thank Tim Wade of the U.S. EPA for input and helpful comments.

Author information

Authors and Affiliations

  1. Great Lakes Science Center, United States Geological Survey, 1100 N. Mineral Springs Road, Porter, IN, 46304, USA

    Richard L. Whitman, Meredith B. Nevers, Muruleedhara Byappanahalli, Zhongfu Ge & Kasia Przybyla-Kelly

  2. Department of Integrative Biology, University of South Florida, SCA 110, 4202 E. Fowler Ave., Tampa, FL, 33620, USA

    Valerie J. Harwood

  3. Canada Centre for Inland Waters, Environment Canada, 867 Lakeshore Road, Burlington, ON, L7R 4A6, Canada

    Thomas A. Edge & Allan Crowe

  4. Environmental Health Division, Ottawa County Health Department, 12251 James Street, Suite 200, Holland, MI, 49424, USA

    Kannappan Vijayavel

  5. Remediation and Redevelopment Division, Department of Environmental Quality, State of Michigan, 525 W. Allegan St., Lansing, MI, 48909, USA

    Kannappan Vijayavel

  6. Reference Unit for Systemic Infections and Zoonosis, Department of Infectious Diseases, National Institute of Health Dr. Ricardo Jorge, Av. Padre Cruz, 1649-016, Lisbon, Portugal

    João Brandão

  7. Department of Soil, Water, and Climate, BioTechnology Institute, University of Minnesota, St Paul, MN, 55108, USA

    Michael J. Sadowsky & Christopher Staley

  8. Department of Biology, Institute for Great Lakes Research, Central Michigan University, Mount Pleasant, MI, 48859, USA

    Elizabeth Wheeler Alm

  9. Environmental Health Sciences Department, Fielding School of Public Health, University of California Los Angeles, 640 Charles E. Young Drive South, Los Angeles, CA, 90024, USA

    Donna Ferguson

  10. Woods Hole Oceanographic Institute, Woods Hole, MA, 02543, USA

    Elizabeth Halliday

  11. Department of Public Health, City of Racine, 730 Washington Avenue, Room 109, Racine, WI, 53403, USA

    Julie Kinzelman

  12. Environmental Research and Innovation Centre, University of Wisconsin, Oshkosh, 800 Algoma Boulevard, Oshkosh, WI, 54901, USA

    Greg Kleinheinz

  13. Department of Civil, Architectural, and Environmental Engineering, University of Miami, 1251 Memorial Drive, McArthur Building Room 252, Coral Gables, FL, 33146, USA

    Helena M. Solo-Gabriele

  14. Oceans and Human Health Center, School of Marine and Atmospheric Science, University of Miami Rosenstiel, 4600 Rickenbacker Causeway, Miami, FL, 33149, USA

    Helena M. Solo-Gabriele

  15. Department of Civil and Environmental Engineering, University of Western Ontario, 1151 Richmond St., London, ON, N6A 3K7, Canada

    Zachery Staley

Authors
  1. Richard L. Whitman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Valerie J. Harwood
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Thomas A. Edge
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Meredith B. Nevers
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Muruleedhara Byappanahalli
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kannappan Vijayavel
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. João Brandão
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Michael J. Sadowsky
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Elizabeth Wheeler Alm
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Allan Crowe
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Donna Ferguson
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Zhongfu Ge
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Elizabeth Halliday
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Julie Kinzelman
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Greg Kleinheinz
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Kasia Przybyla-Kelly
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Christopher Staley
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Zachery Staley
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Helena M. Solo-Gabriele
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Helena M. Solo-Gabriele.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Whitman, R.L., Harwood, V.J., Edge, T.A. et al. Microbes in beach sands: integrating environment, ecology and public health. Rev Environ Sci Biotechnol 13, 329–368 (2014). https://doi.org/10.1007/s11157-014-9340-8

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11157-014-9340-8

Keywords

Search

Navigation