Beach science in the Great Lakes

Journal of Great Lakes Research 40 (2014) 1–14

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Journal of Great Lakes Research

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Review

Beach science in the Great Lakes

Meredith B. Nevers a,⁎, Murulee N. Byappanahalli a, Thomas A. Edge b, Richard L. Whitman a

a U.S. Geological Survey, Great Lakes Science Center, Lake Michigan Ecological Research Station, 1100 N. Mineral Springs Road, Porter, IN 46304, USAb Environment Canada, Canada Centre for Inland Waters, 867 Lakeshore Road, Burlington, Ontario L7R 4A6, Canada

⁎ Corresponding author. Tel.: +1 219 926 8336x425.E-mail address: [email protected] (M.B. Nevers).

0380-1330/$ – see front matter. Published by Elsevier B.Vhttp://dx.doi.org/10.1016/j.jglr.2013.12.011

a b s t r a c t
a r t i c l e i n f o
Article history:Received 21 October 2013Accepted 16 December 2013Available online 25 January 2014

Communicated by Anett Trebitz

Keywords:Health riskEnvironmental microbiologyCoastalIndicator bacteriaModeling

Monitoring beachwaters for humanhealth has led to an increase and evolution of science in the Great Lakes, whichincludesmicrobiology, limnology, hydrology, meteorology, epidemiology, andmetagenomics, among others. In re-cent years, concerns over the accuracy of water quality standards at protecting human health have led to a signif-icant interest in understanding the risk associatedwithwater contact in both freshwater andmarine environments.Historically, surfacewaters have beenmonitored for fecal indicator bacteria (fecal coliforms, Escherichia coli, entero-cocci), but shortcomings of the analytical test (lengthy assay) have resulted in a re-focusing of scientific efforts toimprove public health protection. Research has led to the discovery of widespread populations of fecal indicatorbacteria present in natural habitats such as soils, beach sand, and stranded algae. Microbial source tracking hasbeenused to identify the source of these bacteria and subsequently assess their impact on humanhealth. As a resultofmany findings, attempts have beenmade to improvemonitoring efficiency and efficacywith the use of empiricalpredictive models and molecular rapid tests. All along, beach managers have actively incorporated new findingsinto their monitoring programs. With the abundance of research conducted and information gained over the last25 years, “Beach Science” has emerged, and the Great Lakes have been a focal point for much of the ground-breakingwork. Here, we review the accumulated research onmicrobiological water quality of Great Lakes beachesand provide a historic context to the collaborative efforts that have advanced this emerging science.

Published by Elsevier B.V. on behalf of International Association for Great Lakes Research.

Contents

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 1Development of recreational water quality standards: historical perspective . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2Discovery of FIO in natural sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2

Beach sand . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3Cladophora algae . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4Soils and upland sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

Identifying the source of fecal indicator organism contamination . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5Public health risk . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

Epidemiology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7Pathogens . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7

Improved monitoring efficiency . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8Microbiological methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8Predictive modeling . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8

Beach management and public notification . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9Initiatives and organizations . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9Future directions/needs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11

. on behalf of International Associatio

Introduction

One of themost valued natural resources in North America, the Lau-rentian Great Lakes, offer hundreds of beaches that provide recreational

n for Great Lakes Research.

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2 M.B. Nevers et al. / Journal of Great Lakes Research 40 (2014) 1–14

opportunities to millions of people. These beaches are indicative of thehealth of the Great Lakes, and they are critically important to manylocal economies around the region. In addition to recreational activities,the Great Lakes are an important source of drinking water to the com-munities living along their shorelines and an important resource forcommercial shipping and transport needs. As human populations haveincreased, the ecological pressures on the lakes and concern aboutprotecting recreationists from harmful agents (chemical, microbiologi-cal) have similarly expanded. As a result of this, environmental researchacross the lakes has flourished to help further our understanding of thebeachshed (recreational swimming areas, the associated watershed,and the associated hydrometeorological, biological, and human influ-ences). Converging and conflicting uses and requirements have led tothe need for a diverse array of beach research activities and the emer-gence of a growing body of knowledge on diverse aspects of GreatLakes beach science.

Great Lakeswaters are the repository for wastewater fromhundredsof municipalities and several large urban centers, either indirectly or di-rectly through river drainages. Water originating from publicly ownedtreatment works or septic systems may be released into the lakes astreated, partially treated or, in instances of significant weather events,untreated wastewater, carrying a variety of potentially pathogenic mi-crobes (bacteria, viruses, and protozoan parasites) to nearby beaches.If these pathogenic organisms are released in sufficient quantities andsurvive long enough, there is potential for beach-associatedwaterbornedisease outbreaks (Fong et al., 2007). Besides these point sources, bacte-rial pathogens, such as Aeromonas, Campylobacter and Salmonella, havebeen identified in environmental substrates (e.g., algae, sand/sedi-ments, and detritus) that serve as secondary habitats; these pathogenscan further elevate the human health risk during recreational activities.

Increasing pressure onwater treatment associatedwith human pop-ulation growth around the Great Lakes and similarly increasing recrea-tional use of beaches have resulted in a need for reliable, timelyestimates ofmicrobiologicalwater quality in order to best protect publichealth. A significant amount of attention has been devoted to this need,and as a result, research associating the aquatic ecology, public health,and coastal processes of nearshore beaches has become a focal point(Federal Water Pollution Control Amendments, 1972; Nevers andWhitman, 2010; US EPA, 1999). In this paper, we review the recenthistory of beach science in the Great Lakes, with a special emphasis onrecreational activities (swimming, wading) and human health. Our ob-jectives are to examine the development and current state of beach sci-ence across a range of biological and physical disciplines, includingmicrobiology, limnology, public health science, and ecology. We willsummarize findings to date and map out future directions and needs.

Development of recreational water quality standards:historical perspective

Beaches around the Great Lakes have been monitored for ambientwater quality using fecal indicator organisms (FIO) for many years,with some regular monitoring programs extending back 30 years ormore. Some of the earliest standardswere based on either total coliformbacteria or fecal coliform bacteria; however, these were generally de-rived from a history of perpetuating standards based on assumptionsrather than epidemiological studies linking bather illnesses to concen-trations of bacteria in the water (Dufour, 1984). Later refinement ofthe standards recommended the use of fecal coliforms (200 CFU/100 ml) due to an identified correlation between the presence of Salmo-nella and fecal coliforms (US EPA, 1976), rather than a direct link tohuman health. With this correlation, the United States EnvironmentalProtection Agency (US EPA) recommended use of fecal coliforms as anindicator (Table 1). Similarly, earlier versions of the Guidelines for Cana-dian Recreational Water Quality also recommended use of fecal coli-forms (200 CFU/100 ml) for monitoring water quality at beaches(Health and Welfare Canada, 1992). (See Table 1.)

In the late 1970s and early 1980s, the US EPA undertook a sizableproject to conduct several extensive epidemiological studies in bothfresh and marine waters to further refine recreational water qualitystandards, as required under the Clean Water Act of 1972 (FederalWater Pollution Control Amendments, 1972). Among the study loca-tions were two beaches along Lake Erie. In the resulting standards,Escherichia coli (E. coli) was recommended as an indicator of recentfecal contamination (US EPA, 1986), replacing the long-used fecal coli-forms, with a recommended single-sample maximum of 235 E. coliCFU/100 ml. Not until 2004were these standards promulgated (requir-ing rather than recommending that states establish E. coli monitoringstandards). This coincided with passage of the BEACH Act (BeachesEnvironmental Assessment and Coastal Health Act, 2000), which ex-tended the Clean Water Act and provided funding to states to modifyand expand their beach monitoring programs. The establishment ofmonitoring standards, however, is flexible across Great Lakes states,and implementation has led to the adoption of different standards(Nevers and Whitman, 2010). For example, the state of Wisconsinposts a swimming advisory when E. coli exceeds 235 CFU/100 mlbut closes the beach if it exceeds 1000 CFU/100 ml (WisconsinDepartment of Natural Resources, 2001). The state of Michiganposts a swimming advisory if the E. coli concentration exceeds300 CFU/100 ml (State of Michigan, 1997). As a result, public healthprotection is unequally expressed across the Great Lakes (Nevers andWhitman, 2010).

In Canada, there is no federal legislation equivalent to the CleanWater or BEACH Acts in the U.S., and recreational water quality general-ly falls under provincial jurisdiction. Health Canada recently updatedthe 1992 Guidelines for Canadian Recreational Water Quality, and re-placed fecal coliforms with E. coli (200 CFU/100 ml) for freshwaterbeaches (Health Canada, 2012). However, the federal guidelines inCanada are not legally enforceable standards, except where adoptedby the appropriate provincial/territorial agency. In the latter case, suchan agency may choose to apply more stringent water quality valuesand objectives as deemed necessary. In Ontario, for instance, beachesmust meet the provincial water quality objective of 100 E. coli/100 ml(Ministry of Environment, 1994).

Mounting criticismover the lengthy assay time (24–48 h) for cultur-ing FIO (both E. coli and enterococci) and the lack of real-time results ledUS EPA to initiate another broad set of epidemiological studies in theearly 2000s, including Great Lakes beaches along Lakes Michigan andErie (Wade et al., 2006, 2008). A new set of recreational water qualitycriteria were developed that included the retention of culturable E. coliand enterococci as indicators, and also the addition of enterococci asmeasured by the rapid test quantitative polymerase chain reaction(qPCR) (US EPA, 2012). These criteria were released in 2012 and haveyet to be developed into standards by affected states or implementedin monitoring programs, but several jurisdictions and research projectsby academic institutions and government agencies have been testingthe qPCR analyses (Lavender and Kinzelman, 2009; Nevers et al.,2013). The recently updated Guidelines for Canadian RecreationalWater Quality have re-affirmed the 200 CFU/100 ml E. coli level, andhave provided new guidance for secondary contact recreational activi-ties, fecal pollution source tracking, and considering fecal contaminationof beach sand (Health Canada, 2012).

Discovery of FIO in natural sources

Fecal indicator organisms (FIO) have been investigated in beachwaters around the Great Lakes for many years. One of the earlieststudies was conducted by the International Joint Commission (IJC) in1913; while it focused on drinking water, nonetheless it identifiedthe extensive fecal contamination of nearshore waters around theGreat Lakes, particularly in connecting channels (International JointCommission, 1918). This early IJC study conducted surveillance for bac-teria now known to be more similar to total coliforms. Subsequent

Table 1Establishment of recreational water quality standards for the Great Lakes.

Agency Type of study Great Lakes studylocation

Years of analysis Finding Freshwater single-samplestandard established (year)

Reference

Individual states None 1922–1963 Not based on any known healtheffect

50–2400 total coliformMPN/100 ml, depending onstate

(Senn, 1963)

U.S. Public HealthService

Prospectiveepidemiological

Lake Michigan:Chicago, Illinois

1948–1950s No correlation betweenswimming-associated gastroenter-itis and fecal coliforms at LakeMichigan site (gastroenteritis cor-related with fecal coliforms at OhioRiver site)

200 fecal coliformMPN/100 ml (1976)

(Stevenson, 1953; US EPA,1976) (“Red Book”)

U.S. EnvironmentalProtection Agency

Prospectiveepidemiological

Lake Erie: Erie,Pennsylvania

1978–1982 Highly credible gastrointestinalillness correlated withconcentration of E. coli andenterococci

235 E. coli CFU/100 ml 61enterococci CFU/100 ml(1986)

(Dufour, 1984; US EPA, 1986)

U.S. Prospectiveepidemiological

Lake Michigan:Indiana and Michi-gan; Lake Erie: Ohio

2003–2004 NEEAR (National Epidemiologicaland Environmental Assessment ofRecreational Water Quality)-gastrointestinal illness correlatedwith concentration of enterococci(culturable and qPCR)

235 E. coli CFU/100 ml 70enterococci CFU/100 ml1000 enterococciCCE/100 ml (2012)

(US EPA, 2012; Wade et al.,2006; Wade et al., 2008)

3M.B. Nevers et al. / Journal of Great Lakes Research 40 (2014) 1–14

surveys for fecal coliform bacteria, andmore recently, E. coli, continue toshow the widespread presence of FIO impacting recreational waters inGreat Lakes connecting channels and near large urban centers.

Research into the spatial distribution of FIO led to the discovery thatsome of these bacteria were present and surviving in areas that had notrecently received human fecal pollution. Early studies indicated thatfecal coliform bacteria might survive in submerged sediment near sew-age outfalls, with the potential to become secondary sources of FIO tothe overlying water (Rittenberg et al., 1958). In the 1980s, Palmer(1988) found that re-suspension of sediments under the water columnat Toronto beaches caused loadings in excess of 100 fecal coliforms/(m2 s) and significant increases in water fecal coliform concentrationsin shallow beach areas. Similarly, Palmateer et al. (1989) found sedi-ments in an agricultural drain to Lake Huron were contaminated with106 E. coli/100 g, and that their re-suspension could be contributing tobeach postings near the river mouth. Seyfried et al. (1985b) also foundFIO levels to be about ten times higher in beach sand sediments thanthose in the overlying beach water. Additional studies in the GreatLakes have confirmed the presence of these bacteria in a variety of envi-ronments, independent of recent human sewage contamination events(see reviews by Byappanahalli and Ishii, 2011; Whitman et al., 2011).

Beach sand

Along marine coasts, beach sand was identified as harboring FIO(Ghinsberg et al., 1994; World Health Organization, 2003). Evidence ofsimilar occurrence in temperate freshwater locations was describedlater for beaches along Lake Michigan (Twinning et al., 1993; Whitmanand Nevers, 2003) (Table 2), Lake Superior (Ishii et al., 2007), LakeOntario (Edge and Hill, 2007), and Lake Huron and the St. Clair River

Table 2E. coli counts in sand and water at 63rd Street Beach, Chicago, 2000. Reprinted withpermission from the American Society for Microbiology. Whitman, R.L. and Nevers, M.B.2003. Foreshore sand as a source of Escherichia coli in nearshore water of a Lake Michiganbeach. Appl. Environ. Microbiol. 69:5555–5562.

Sample source Mean count Median Geometric mean

(CFU/100 ml) ± SD

Foreshore sand 1.1 × 104 ± 8.5 × 102 4.8 × 103 4.0 × 103

Submerged sand 2.6 × 103 ± 7.6 × 102 7.6 × 102 7.2 × 102

Water (all) 1.11 × 102 ± 1.3 × 102 6.0 × 101 4.3 × 101

Water 45 cm 1.6 × 102 ± 1.8 × 102 8.4 × 101 6.2 × 101

Water 90 cm 7.5 × 101 ± 9.3 × 101 3.6 × 101 2.6 × 101

Offshore water 3.4 × 101 ± 4.4 × 101 1.0 × 101 1.2 × 101

(Alm et al., 2003). High concentrations of E. coli have been found inbeach sand at Great Lakes beaches asmeasured per 100 ml of interstitialsand pore water as well as per gram of dry sand. Edge and Hill (2007)measured E. coli concentrations as high as 1.14 × 105 CFU/g dry sandat Bayfront Park Beach (Hamilton Harbour, Lake Ontario), while Edgeet al. (2010) and Kon et al. (2007) measured E. coli concentrations insand interstitial pore water as high as 2.6 × 106 CFU/100 ml atSunnyside Beach in Toronto (Lake Ontario) and 1.6 × 106 CFU/100 mlat Ashfield Township Park Beach on Lake Huron.

Beach sand may serve as a sink or a source of FIO in overlying water(see recent reviews byHalliday andGast, 2011, Richard L.Whitman, U.S.Geological Survey, 2013, personal communication). While shorelinebirds may contribute to the FIO found in sand, the extent of input varieswidely (Edge and Hill, 2007; Lu et al., 2011), with some influence foundas far as 150 moffshore in LakeOntario (Edge andHill, 2007); however,birds may not account for all of the FIO present (McLellan and Salmore,2003). Multiple sources can introduce FIO to the sand environment:some prominent sources might include shoreline birds (e.g., gulls,geese) (Alderisio and DeLuca, 1999; Fogarty et al., 2003; Haack et al.,2003; Kinzelman et al., 2008), direct human shedding during recrea-tional activities (Elmir et al., 2007; Papadakis et al., 1997), stranded veg-etation (algae, beach wrack, marsh) containing FIO (Anderson et al.,1997; Englebert et al., 2008a; Imamura et al., 2011; Ishii andSadowsky, 2008; Whitman et al., 2003), and diffuse sources (run off,wave-induced surges and related processes) (Ge et al., 2010). However,once these bacteria enter the sand environment, they can survive andmay even grow in moist subsurface sand under certain conditions. Forinstance, at two beaches along southern Lake Michigan, E. coli and en-terococci were consistently recovered in moist subsurface sand nearthe groundwater table over a period of 15 months (Byappanahalliet al., 2006). Further, bacteria in beach sand were able to persistthroughout the summer swimming season in high concentrations ata Chicago beach, maintaining a steady population (Whitman andNevers, 2003; Whitman et al., 2006).

There is growing evidence that pathogenic bacteria, such asStaphylococcus aureus (Mendes et al., 1993), Vibrio spp. (Ghinsberget al., 1995), Salmonella and Campylobacter (Bolton et al., 1999),and pathogenic fungi (Sabino et al., 2011; World Health Organization(WHO), 2003) can survive/remain infectious in beach sand. Evidencefrom the Great Lakes indicates the presence of potentially pathogenicstrains of E. coli in beach sands along Lake Huron and Lake St. Clair; how-ever, the absence of genes coding for toxins in this study indicated thepresence of pathogen was likely minimal (Bauer and Alm, 2012). Viru-lent markers associated with shiga-toxin producing E. coli (STEC), albeit


in low frequencies, potentially coming from human and animal sources(Haack and Duris, 2013) have also been found in rivers near a beach onsouthern Lake Michigan. Recent evidence of contamination in Lake Su-perior sands has included the presence of Enterococcus faecalis, a poten-tial opportunistic pathogen (Ran et al., 2013).

Khan et al. (2009) found that both culture and qPCR-based detectionmethods enumerated higher numbers of Aeromonas bacteria in intersti-tial pore water of foreshore sand than in adjacent surface water at twofreshwater beaches on Lake Ontario. Foreshore sand served as a reser-voir for higher numbers of aeromonads similar to this phenomenonfor FIO. However, Khan et al. (2009) did not specifically confirm thepathogenicity of any Aeromonas isolates recovered from beach sand.

Campylobacter species such as C. jejuni and C. lari have been com-monly detected in beach sand in Hamilton Harbour (Lake Ontario) atbeaches that are impacted by bird fecal droppings (Edge, unpublisheddata). The frequency of detection and numbers of Campylobacter werehigher in beach sand than those in adjacent surface water at these twobeaches. Campylobacterwas detectedmore commonly in beach sand in-terstitial samples (27%) than that in adjacent ankle (9%) or chest (5%)depth surface water samples at Lake Simcoe beaches (Khan et al.,2013b). Among 67 beach sand interstitial samples from Lake Simcoebeaches, C. jejuni (18%) was most common followed by C. lari (10%).Campylobacter coli was not detected. Campylobacter concentrations inLake Simcoe beach sands were low, occurring at minimum detectionlevels of about 3–30 cells/L of interstitial sand pore water.

Additionally, the presence of markers of human fecal contamination(e.g., Bacteroides HF183) may also indicate contamination from sourcessuch as sewage, increasing chances of human pathogens in beach sand(Eichmiller et al., 2013). Concern over human exposure to these patho-gens during sand recreation, such as digging and burying in sand(Heaney et al., 2009; Whitman et al., 2009), may be warranted. Effortsto mitigate sand microbial contamination remain challenging.

Cladophora algae

Cladophora is nearly ubiquitous in the lower Great Lakes (Depew etal., 2011; Higgins et al., 2008), and can reach nuisance levels in nutrient-rich areas along the coast. Beaches along the Great Lakes often accumu-late large amounts of Cladophora algae in the summer, with massivemats causing unsightly conditions along shorelines. Investigations of

A

0.0 1.0 2.0 3.0 4.0 5.0 6

Bradford (WI)

North Beach (WI)

Illinois State Park (IL)

Waukegan (IL)

63rd Street (IL)

Washington Park (IN)

Good Harbor Bay (MI)

Sleeping Bear Bay (MI)

Platte Bay (MI)

S. Manitou Island (MI)

Median

Bea

ch

E. coli (log CFU/g)

Fig. 1. Log10mean concentrations (±1 standard error) of E. coli (A) and enterococci (B) in CladopandMichigan (MI). Reprintedwith permission from the American Society forMicrobiology.Whof Escherichia coli and enterococci in Cladophora (Chlorophyta) in nearshore water and beach s

the bacterial community present in these algal mats revealed concen-trations of FIO that were much higher than present in water (usually1–2.5 log at these beaches) and even some pathogens at several loca-tions around Lake Michigan (Byappanahalli et al., 2009a; Ishii et al.,2006a; Whitman et al., 2003) (Fig. 1). Besides these bacteria, a widerange of microbial communities and macrophytic organisms havebeen found in Cladophora mats (Olapade et al., 2006; Zulkifly et al.,2012), suggesting a complex ecological niche, which Zulkifly et al.(2013) refer to as an “ecological engineer.” Because the mats are highlytransient, being moved or removed by wave activity, they have the po-tential to be a significant source of FIO contamination to the nearshorebeach. Studies have shown a good correlation in E. coli densities betweenCladophoramats and surrounding water, suggesting that the presence ofalgal mats may elevate E. coli levels (Vanden Heuvel et al., 2010).

In addition to abundant FIO, human pathogens have been identifiedin algae along a point source river in LakeMichigan, including Salmonella,Shigella, Campylobacter, and Shiga-toxin producing E. coli (Ishii et al.,2006b). Byappanahalli et al. (2009a) found nearly identical strains ofSalmonella with DNA fingerprint similarities of 92–95% in Cladophoramats collected from streams and a beach along southern Lake Michigan,indicating that these bacteria were growing in the algal mats (Fig. 2).Whether any residual bacteria survive in algal remnants during winteris not clear; high genetic diversity among Salmonellawith strains tightlyclustering both by sampling location and year seem to suggest thatthe relationship between Salmonella and Cladophora is mostly casual.At a beach near Milwaukee, the community was dominated by highconcentrations of FIO, sulfate-reducing bacteria, and Cytophaga-Flavobacterium-Bacteroides cluster (Olapade et al., 2006).

The change in E. coli community over time and space has also beenexamined in molecular studies; Byappanahalli et al. (2007) examinedsmall-scale temporal and spatial distributions of E. coli communities inLake Michigan and found high diversity. At multiple locations aroundLake Michigan, there was remarkable similarity between sites but dif-ferent populations between years (Byappanahalli et al., 2009b); this in-dicates a loose or opportunistic relationship between enteric bacteriaand Cladophora mats — i.e., surviving enteric bacterial strains(E. coli, Salmonella) in the water column can establish on the algaeand grow under certain conditions (e.g., in decaying Cladophora dur-ing summer). The discovery of high E. coli densities in Cladophora(Whitman et al., 2003) and occurrence of genotypically diverse

B

.0 7.0 0.0 1.0 2.0 3.0 4.0 5.0 6.0 7.0

Median

enterococci (log CFU/g)

hora collected from10LakeMichigan beaches inWisconsin (WI), Illinois (IL), Indiana (IN),itman, R.L., Shively, D.A., Pawlik, H., Nevers,M.B. and Byappanahalli, M.N. 2003. Occurrenceand of Lake Michigan. Appl. Environ. Microbiol. 69:4714–4719.

Percent Relative Similarity

2005

2006

2007

30 40 50 60 70 80 90 100

Fig. 2. Dendrogram showing the relatedness of Salmonella strains isolated fromCladophora as determined by HFERP DNA fingerprint analysis using the Box A1R primer.DNA fingerprint similarities were calculated by using the curve-based, cosine coefficientand dendrogramswere generated by the unweighted pair-groupmethod using arithmeticaverage (UPGMA). Triangles represent genetically unique (i.e., ≥92% similarity)Salmonella isolates clustering into distinct groups; numbers to the right of each trianglerepresent the number of isolates in that group. Reprinted with permission from theInternational Water Association. Byappanahalli, M.N., Sawdey, R., Ishii, S., Shively, D.A.,Ferguson, J., Whitman, R.L. and Sadowsky, M.J. 2009. Seasonal stability of Cladophora-associated Salmonella in Lake Michigan watersheds. Water Res. 43:806–814.


populations, not only over time and space (Byappanahalli et al.,2007), but also on a short-term basis (Badgley et al., 2010), supportthis hypothesis.

Complicating the presence of FIO and other pathogens in Cladophora,laboratory studies have shown that the FIO are capable of growth inCladophora mats. E. coli and enterococci readily grew in plain algalwashings under laboratory conditions (35 °C), with counts increasingby 100 (enterococci)-1000 (E. coli) fold within 24 h (Byappanahalliet al., 2003a). Similarly, when dried algal mats stored at 4 °C wererehydrated, E. coli increased by as much as 100,000-fold in 24 h, sug-gesting that drying does not necessarily kill E. coli and that residual pop-ulations can recover when conditions improve. Englebert et al. (2008b)conducted additional laboratory studies to determine if the samegrowth response occurred in pathogenic bacteria and found that whileE. coli numbers increased significantly, Salmonella and Shigellawere un-able to persist for extended periods of time (Englebert et al., 2008b).While the temperature of algae mats on the beach likely reach temper-atures conducive to FIO growth, field experiments have yet to corrobo-rate these laboratory findings.

Soils and upland sources

In addition to these shoreline sources, other environmental sourcesof FIO have been identified within the beachshed that could influencewater quality. Upland forest soils in the Great Lakes basin can containhigh concentrations of FIO; in a study in a protected State Park alongLake Michigan, forest soil, stream bank soil, and stream sediment all

contained E. coli (Byappanahalli et al., 2003b). It was further determinedthat these populations maintained high concentrations throughout thecalendar year (Byappanahalli et al., 2006), indicating E. coli to be partof the soil microbiota.

Similarly, Ishii et al. (2006a) recovered E. coli from soils in Lake Supe-rior watersheds, with the highest and lowest densities in summer toearly fall (June–October) and winter to late spring (February–May), re-spectively.While the original source of these bacteria is often unknown,two lines of evidence – (a) thepresence of unique genotypes and (b) thebacterial ability to grow in temperate soils under certain conditions –support that these bacteria have adapted to become part of the indige-nous microflora. E. coli and enterococci have also been identified infreshwater springs, seeps, and deep subsurface beach sand (Whitmanet al., 2006) (see also reviews by Byappanahalli and Ishii, 2011;Whitman et al., 2011). All of these sources have the potential to contam-inate nearshore water when transported by surface runoff or streamflow.

The discovery of the ubiquity of FIO in natural sources shifted theparadigm of bacterial survival from an understanding of short-lived,transient fecal-associated organisms to widespread, persistent popula-tions possibly capable of growth in natural environments (see recent re-views Byappanahalli and Ishii, 2011; Whitman et al., 2011). There issome speculation that environmental E. coli and enterococci play arole in nutrient cycling and other ecological functions. For instance, sev-eral species within the genus of Enterococcus (e.g., E. faecalis, E. faecium,E. casseliflavus) are naturally found in terrestrial (Muller et al., 2001; Ottet al., 2001) and aquatic (Badgley et al., 2010) vegetation; studies in theGreat Lakes have shown high levels of E. coli and enterococci in beachCladophora and wetland plants (Whitman et al., 2005). Collectively,these findings highlight the (a) widespread occurrence of FIO innonenteric habitats and (b) the need for bettermethods to detect, quan-tify, and perhaps partition sources.

Identifying the source of fecal indicator organism contamination

Despite the discovery of the ubiquity of FIO in natural environmentsof the Great Lakes basin beyond recreational waters, their potential im-pact on public health is generally unknown. While human pathogens/virulent markers have been detected in many of these sources, ques-tions remain about original source, transport from source to beachwater, survival, and concentrations necessary for infection. Severalstudies have sought to characterize components of these questions(Byappanahalli and Whitman, 2009; Byappanahalli et al., 2009a; Chunet al., 2013; Duris et al., 2009), but a coordinated understanding is stillelusive.

Early studies identified the importance of urban storm water, sani-tary and combined sewer overflows, and wastewater effluents forimpacting recreational water quality in Sault Ste. Marie, Toronto, Sarnia(Tsanis et al., 1995), and Windsor, Ontario (Dutka and Marsalek, 1993;Marsalek and Rochefort, 2004; Marsalek et al., 1994, 1996). A varietyof hydrodynamic models were used to investigate storm water andmunicipal wastewater impacts on these beaches in order to guideremediation efforts to reduce the high numbers of beach postingsin these urban areas. Other studies have pointed to the importanceof groundwater as a potential transport route to deliver contami-nants to the shoreline at beaches under certain scenarios (Croweand Meek, 2009).

As discussed in previous sections, FIO in most environmental watersis often amixture of bacterial populations from anthropogenic (humansand domesticated animals) and non-anthropogenic sources (SadowskyandWhitman, 2010). Thus, determining the source of fecal contamina-tion at beaches has become an important driver for advances in fieldssuch as microbial source tracking (Edge and Schaefer, 2006; Field andSamadpour, 2007; Santo Domingo et al., 2007; Scott et al., 2002;Stoeckel et al., 2004; US EPA, 2005). Using microbial source tracking,researchers may be able to determine where bacteria present in


swimming water or beach sand likely originated which would provideinsight for the health risk associated with human contact. Given the nu-merous potential sources of FIO (Byappanahalli et al., 2012; Fergusonand Signoretto, 2011), discernment of a human source provides a farbetter idea of human health risk in the associated lake. Methodsof source tracking include the use of chemical markers, microbio-logical markers, or genotypic markers, all of which have differentuse applications. Collectively, a suite of these markers is desirablefor source tracking; however, cost, technical complexity, andother considerations prohibit or limit this type of application inroutine monitoring.

A variety ofmicrobial source tracking (MST)methods have been ap-plied at Great Lakes beaches in studies to identify the source of fecal pol-lution causing beach closings. These studies have used both library-dependent and library-independent MST methods. Library-dependentmethods are based on selecting an FIO, such as E. coli, and establishinga reference library of characteristics of E. coli isolates from individualfecal pollution sources (e.g., cattle, poultry, birds). The library could bea database of characteristics such as DNA fingerprints, biochemical fin-gerprinting, or antimicrobial resistance profiles of E. coli. The DNA fin-gerprints of E. coli isolates obtained from beach environments(“unknowns”) can then be compared to the DNA fingerprints in the li-brary (“knowns”) to make inferences about the source of the beachE. coli.

In one of the earlier studies, Dombek et al. (2000) used the repetitiveextragenic palindromic polymerase chain reaction (Rep-PCR) techniqueto differentiate E. coli isolates originating from human and animal fecalsources. This technique, which has been used extensively in microbialecology, epidemiology, and environmental microbiology (see Ishii andSadowsky, 2009), has been commonly used in contaminant sourceidentification in the Great Lakes. Johnson et al. (2004) used an improvedtechnique – horizontal fluorophore enhanced rep-PCR (HFERP) – togenerate a DNA fingerprint database from 2466 E. coli isolates obtainedfrom humans and animal sources; using this technique, they showedHFERP would be useful to differentiate E. coli subtypes derived fromhuman and animal origin. Similarly, Edge and Hill (Edge and Hill,2007) collected rep-PCR DNA fingerprints and antimicrobial resistanceprofiles from over 3500 E. coli isolates as part of multiple lines of evi-dence to identify bird fecal droppings as the primary source of E. colicausing beach postings at Bayfront Park Beach in Hamilton Harbour,Lake Ontario. It was previously believed that municipal wastewaterfrom four nearby sewage treatment plants discharging into the harborwas likely the primary cause of the beach postings. Library-based MSTmethods were also applied by Edge et al. (2007) and Edge et al.(2010) to identify the comparative importance of bird fecal droppings(e.g., seagull and Canada geese) relative to municipal wastewater efflu-ents as the cause of beach postings at several urban beaches in the Cityof Toronto on Lake Ontario. Kon et al. (2009) applied rep-PCR DNA fin-gerprinting of E. coli isolates to suggest that agricultural sources werethe dominant source of E. coli to a Lake Huron beach.

As library-based MST methods have become more widely recog-nized as time-consuming and expensive, and also less representativeover wider spatial and temporal boundaries, researchers have increas-ingly investigated applications of library-independentMSTmethods. Li-brary independent methods look for host-specific microorganisms inwater samples that could only have come from a human or specific an-imal gut in order to make inferences about the source of fecal pollutionimpacting a beach. Some of the early attempts described a protein/surface antigen on Enterococcus faecium that could be linked to human(sewage) contamination, but testing in the Great Lakes and elsewhereundermined these findings when the gene was also found in numerousanimal fecal samples (Byappanahalli et al., 2008; Layton et al., 2009;Whitman et al., 2007). Edge et al. (2010) applied a PCR assay for thehuman-specific Bacteroides HF183 DNA marker to identify the impor-tance of human sewage contamination at City of Toronto beach loca-tions near the mouth of the Humber River. Likewise, human-specific

Bacteroides marker was more sensitive than E. coli in detecting sewagecontamination in Lake Michigan, with the marker detected as far as2 km from the shore following sewage overflow events (Bower et al.,2005). More recently, Lu et al. (2011) applied a gull-specificCatellicoccus DNA marker to identify widespread occurrence of gullfecal contamination in water samples from beaches across the Torontowaterfront of Lake Ontario. Bacterial community analyses to identifyshared operational taxonomic units (OTUs) using metagenomics arean emerging technique to identify new microbial markers to detectsewage contamination, and that makes them attractive targets for fur-ther screening and identification (Newton et al., 2013; Unno et al.,2010). These techniques show promise, but they are still being evaluat-ed by research organizations, so potential application in monitoringprograms is difficult to estimate.

In addition to molecular-based techniques, efforts at determiningsources of contamination have been directed at the physical processesassociated with transport. Hydrodynamic modeling is used to charac-terize the movement of nearshore waters, including the behavior ofriver plumes, re-suspension of submerged or shoreline sediments, anddilution and advection from a point source. These models can be usedin two-dimensional or three-dimensional forms. While these modelshave typically been used to explain contamination fluctuations (Liuet al., 2006; Thupaki et al., 2010, in press), they can also be used totrace shoreline contamination back to its origin. Models developed foroutfalls around the Little Calumet River in southern Lake Michiganhave been used to identify episodes of point source contamination(Thupaki et al., 2013). Using particles as a surrogate for FIO, thesemodels were used to determine the extent of beach shoreline impactedby a contaminant plume emanating from the river outfall; with this in-formation, beach contamination events can be linked to increased flowfrom the river. Modeling work conducted on two beaches along LakeSt. Clair was also used to characterize contamination potentially associ-ated with the nearby Clinton River (Holtschlag et al., 2008). Two-dimensional modeling was used with reverse particle tracking to locatecontamination sources, and it was determined that contaminationtended to originate from the Clinton River in association with certainwind directions. It is likely that hydrodynamic modeling in conjunctionwithmicrobiological datawill be further applied in the future to identifycontamination sources as more examples of this useful application arepublished.

While there has been considerable progress in the use of moleculartechniques in source tracking studies (Hagedorn et al., 2011), it is ap-parent that traditional indicators, such as E. coli, can have high geneticdiversity among animal hosts such that their host-specificity can bequite spatially and temporally limited. Such high genetic diversity cancontribute to incorrect classification of sources (Johnson et al., 2004).At the same time, the host-specificity of the library-independentmicro-bial source tracking methods is also usually not 100% accurate andneeds careful evaluation before application. The problems associatedwith source identification have been extensively covered in numerousreports and published papers and books (see Hagedorn et al., 2011;Roslev and Bukh, 2011; Santo Domingo et al., 2007; US EPA, 2005).

Public health risk

Identifying source and fate of these FIO do not conclusively charac-terize the human health risk associatedwith recreational contact. Ongo-ing research has sought to link presence of FIO with human health riskthrough sanitary surveys/direct monitoring for associated pathogens,epidemiological studies, and quantitative microbial risk assessment(Dorevitch et al., 2012; Haack and Duris, 2013; Hagedorn et al., 2011).A number of such studies throughout the Great Lakes have resulted inwidely variable results (Dorevitch et al., 2011; Wade et al., 2008);beaches impacted by point source contamination are generally morelikely to pose a higher risk to human health, so thewidespread presenceof FIO at all types of beaches complicatesmanagement decision-making.

Beach/Year

Fig. 3.Comparison of estimates of expected illness rate using E. coli (EC), culturable entero-cocci (ENT), or enterococci measured by qPCR (QENT). Illness rates are based on epidemi-ological studies that regressed actual highly credible gastrointestinal illnesses (HCGI) orNEEAR (National Epidemiological and Environmental Assessment Recreational WaterStudy) gastrointestinal illness (NGI) with FIB concentrations; all results have been con-verted to NGI. Box length shows the range of the central 50% of values. The box edges in-dicated the first and third quartiles. Whiskers extend to values falling within 1.5 times theinterquartile range. Asterisks are values considered ‘outside’ and open circles are consid-ered ‘far outside.’ Reprinted with permission from Nevers, M.B., Byappanahalli, M.N. andWhitman, R.L. 2013. Choices in Recreational Water Quality Monitoring: New Opportuni-ties and Health Risk Trade-offs. Environ. Sci. Technol. 47:3073–3081. Copyright 2013American Chemical Society.


The Great Lakes have been the source of numerous human healthoutbreaks associated with either drinking water or recreational waterquality. Among recent recreational-related outbreaks, contaminatedgroundwater was implicated in a large outbreak at a Lake Erie Beach(Fong et al., 2007); a broken sewage pipe was implicated in an outbreakat a Wisconsin State Park on Lake Michigan (Dziuban et al., 2006),and an unknown source sickened hundreds participating in a triathlonin Illinois (Centers for Disease Control and Prevention, 1998). An out-break of E. coli O157:H7 was attributed to bathing at a publicbeach in Montreal, Quebec in August 2001 (Public Health Agencyof Canada, 2004). Associated, human pathogens have recently beendetected in drinking water intakes in Lake Ontario (Edge et al.,2013). The outbreaks highlight the underestimation of recreationalwater illnesses, which may only be obvious if illnesses are seriousenough to result in hospitalization. While beach water is regularlyanalyzed for FIO, efforts continue to be made to improve the reliabil-ity of water quality estimates and their relation to real humanhealth effects.

Epidemiology

Epidemiology-based studies for the development of water qualitystandards have targeted the Great Lakes. Scientists focused on theGreat Lakes after similar studies had been conducted at marine beachesbecause they recognized the potential for significant differences be-tween fresh and marine waters in FIO survival and the relationship be-tween FIO and human pathogens. Early studies by the US Public HealthService, including a site on LakeMichigan in Chicago (Stevenson, 1953),established a link between bather illness and water quality. Criticism ofthis study included issues with participant reporting and definitions ofexposure (Cabelli et al., 1975). Later epidemiological studies by the USEPA included beaches on Lake Erie (Dufour, 1984)wherewater sampleswere analyzed for concentrations of fecal coliforms, enterococci, andE. coli. Simultaneously, initial and follow-up interviews were conductedwith beachgoers to assess level of exposure to the swimmingwater andresulting illness. Results of the study confirmed a significant relation-ship between beachwater exposure and highly credible gastrointestinalillness (Dufour, 1984). It was also determined that fecal coliforms werenot adequate indicators of resulting illness, but both E. coli and entero-cocci concentrations were directly related to rates of illness (E. coli hadthe better result). These studies served as the basis for the recreationalwater quality standards established for the U.S. in 1986 (US EPA,1986). A prospective cohort epidemiological investigationwas conduct-ed at ten high-visitation Canada beaches in southern Ontario in 1980(Seyfried et al., 1985a). Follow-up telephone interviews found that sig-nificantlymore swimmers (7%, N = 2743) became ill compared to non-swimmers (3.0%, N = 1794). Swimmers experienced respiratory ail-ments most frequently, followed by gastrointestinal, eye, ear, skin, andallergic symptoms. Microbial water quality analyses associated withthis epidemiological study found Staphylococcus to be the most consis-tent indicator for predicting bather illness although fecal coliformswere also useful (Seyfried et al., 1985b).

After implementation of the 1986 US EPA water quality criteria(US EPA, 1986), criticism began to emerge over the use of culture-based methods because of the significant time delay between samplecollection and the availability of results. Developments in analyticalmethods, such as the use of defined substrate technology, reduced theanalytical time for traditional FIOs (E. coli, enterococci) from 24–48 hto 18–24 h. Nonetheless, same-day results have not been possiblewith culture-based techniques. This delay can be associated with a sig-nificant change in concentrations in FIO, resulting in high levels of man-agement errors (Nevers and Whitman, 2011). For this reason, a newseries of epidemiological studies were conducted by the US EPA in theearly 2000s that attempted to link health effectswith amore rapidly an-alyzed indicator. Among the study locations were three beaches alongLake Michigan and two beaches along Lake Erie. Findings supported

the 1986 criteria for culturable enterococci and also included a link be-tween health effects and enterococci as measured by qPCR, which pro-vides results in a few hours. Corroborating health effects acrossmeasurements of two endpoints complicates the application of moni-toring protocols (Nevers et al., 2013) (Fig. 3), and as of this writing,few beaches have been assessed for management implications ofadopting a newer testing protocol. Potential comparisons between thetwo endpoints have required correction factors (Lavender andKinzelman, 2009).

Pathogens

Presence of pathogens in Great Lakes beach waters is the primaryconcern for recreational contact. Several studies have attempted tocharacterize and quantify human-associated pathogens in nearshoreGreat Lakes beach waters. A study of two of the Lake Michigan beachesexamined in the EPA epidemiological studies (Washington Park andSilver Beach) identified human adenoviruses in these point-source im-pacted waters (Xagoraraki et al., 2007). Later analysis determined thatthe presence of human adenoviruses was associated with point sourcehuman fecal contamination, while the presence of enteroviruses wasnot (Aslan and Rose, 2012). Rotaviruses were also found at SilverBeach (Wong et al., 2009). In a Lake Ontario study, Candida albicansand Pseudomonas aerginosa were also identified in beach water(Sherry, 1986; Sherry et al., 1979), and it was suggested that the occur-rence of these pathogens could be related to the number of bathers andsand resuspension. Using culture and qPCR methods, Brinkman et al.(Brinkman et al., 2003) detected pathogenic Candida cells from a south-ern Lake Michigan beach, suggesting their presence may have implica-tions for the detection of fecal pollution. Pathogenic E. coli has been


found in the Great Lakes, with genes for enterohemorrhagic orenterpathogenic E. coli found in a small number of beach water samplescollected along Lake Erie (Lauber et al., 2003) and enteropathogenicE. coli found in one of 3557 strains from samples in Lake Superior(Ishii et al., 2007). Further, the emerging pathogen Arcobacter has alsobeen found in Lake Erie, a bacterium whose presence indicates humanor animal fecal contamination (Lee et al., 2012). Virulent markers asso-ciated with pathogenic E. coli have been recovered in watersheds insouthern Michigan and northern Indiana beaches of Lake Michigan(Duris et al., 2009).

Payment et al. (1982) detected enteric viruses at Montreal beachesbut did not find any correlation between occurrence of the viruses andFIO. Preliminary analyses of coliphage and bacteriophage at five beachesin southern Ontario by Palmateer et al. (1991) suggested the presenceof enteroviruses at these beaches and the need for further virologicalanalyses to understand potential health risks. More recently, investiga-tions of Bayfront Park Beach on LakeOntario have detected the commonoccurrence of Campylobacter species (Khan et al., 2013a), and the occa-sional occurrence of Cryptosporidium andGiardia at this beach impactedby bird droppings (Edge, unpublished data). Additional studies have de-tected Campylobacter at Lake Simcoe (Ontario) beaches (Khan et al.,2013b), and aeromonads at Hamilton Harbour (Lake Ontario) beaches(Khan et al., 2009). Extra-intestinal E. coli pathotypes (e.g., UPEC) andantimicrobial resistant E. coli have been detected at Bayfront ParkBeach in Hamilton Harbour (Lake Ontario) (Edge and Hill, 2005, 2007;Hamelin et al., 2006) although these strains were less common at thisbird-contaminated beach than at other sewage-impacted areas aroundthe Harbour. Kon et al. (2007) found E. coli from beach sand at a LakeHuron beach to possess few virulence and antimicrobial resistancegenes.

Because many streams/rivers empty directly near swimmingbeaches, there is potential for exposure to pathogens during recreation-al activities. The link between concentration of pathogens and tradition-al FIO has been variable. Potential sources of these pathogens mightinclude discharges from wastewater treatment plants and farmlands.Collectively these studies show that a number of human pathogens(bacteria, viruses, and protozoan parasites) can be found in beachwaters on occasion. While birds may contribute pathogens such asSalmonella and Campylobacter in nearshore waters and beach sand,sources of other human pathogens (e.g., viruses) and their flux are notwell understood.

While the basis for the 1986 criteria has been confirmed in subse-quent studies by US EPA, there are several assumptions associatedwith those epidemiological studies that have been identified as poten-tially impacting the relationship between FIO and health effects atother types of beaches. It is significant that theUS EPA studieswere con-ducted at point source contaminated beaches where the potential forhuman fecal contamination, and thus pathogens, is likely to be highdue to surface runoff or combined and sanitary sewer overflows.

Improved monitoring efficiency

Microbiological methods

Early applications of FIO monitoring predominantly employed mul-tiple tube fermentation andmembrane filtration.With the expansion ofresearch on nonpoint sources of FIO since the early 1980s and criticismof the method for real-time estimates of water quality, there has beenemphasis on improving existing methods or developing newermethods. Generally, the requirements of any method should includean indicator with an established link to human illness as well as rigorfor use in regular water quality monitoring. The recommended analyti-cal method for the indicators was membrane filtration (US EPA, 1986),requiring a 24-hour culturing assay.

Method development has included the refinement of defined sub-strate technology (e.g., Colilert and Quanti-Tray approach), which

slightly decreases analytical time and is easier to use. Neither traditionalmembrane filtration nor defined substrate technology is ideal for ana-lyzing turbid samples, so many environmental substrates, such as soiland sediments, beach sand, and vegetation, are still analyzed usingmul-tiple tube fermentation.

In addition to culturing alternatives, efforts have been directed to-ward alternate methods that rely on chemical or genetic characteristicsof the FIO. Among these are immunomagnetic separation/adenosine tri-phosphatemethods thatmeasure the level of luminescence from bacte-ria that are bound to beads (Lee and Deininger, 2004). In this method, awater sample is filtered, and the remaining FIO are bound to magneticbeads; the solution is then purified to include only the ATP from theFIO, which is combined with the enzyme luciferin/luciferase, and lightemission is measured from the final solution using amicroluminometer(Lee and Deininger, 2004). The test was developed for beach watersusing samples collected at beaches along Lake Erie and Lake St. Clair(Lee and Deininger, 2004). The technique has been compared to cultur-ing methods for FIO in Cuyahoga River samples, near Lake Erie, and re-sults provide comparable estimates of beach water quality (Bushonet al., 2009). This approach to monitoring has not gained widespreaduse, although testing in concert with other studies continues in theGreat Lakes (Francy et al., 2013b).

Significant efforts to decrease further the analytical time for FIO havecentered on the use of quantitative polymerase chain reaction (qPCR)(Dorevitch et al., 2011; Haugland et al., 2005). This method relies onthe detection of FIO-specific DNA fragments present in contaminatedrecreational water. Using molecular techniques, DNA is extracted fromthe microbial community in a water sample; if present, the target FIOare magnified by making numerous copies and quantified from theresulting solution. Despite the availability of this rapid testing method,lack of consistency between culturable and qPCR-based methods forFIO, specifically enterococci, has been criticized.While the twomethodstarget different endpoints (culturable enterococci cells vs. enterococciDNA), both have shown a correlation between concentration in surfacewater and resulting human illnesses (Wade et al., 2006, 2008). Howev-er, the differential health protection provided by these two methods(Nevers et al., 2013) raises more questions about the application ofqPCR. Recently released water quality criteria included the use ofqPCR for estimating health effects for recreational waters; epidemiolog-ical studies supporting the findings were conducted by US EPA includ-ing locations along Lake Michigan.

Predictive modeling

Alternate methods for managing water quality have also been ex-plored, separate from those based on microbiological analytical tech-niques. Predictive modeling has been developed and initiated atnumerous Great Lakes beaches; several monitoring agencies are active-ly implementing this technique on beaches along Lakes Michigan, Erie,and Ontario. Based on statistical relationships between water andweather conditions and FIO, predictivemodels are developed using em-pirical datasets; and concentration of FIO on a given day is predicted.Input variables may include water turbidity, wave height, wind direc-tion, or amount of recent precipitation. With these measurements, amathematical calculation is used to predict the FIO concentrationbased on historical relationships between FIO and hydrometeorologicaldata. The most widely used technique is linear regression (Nevers andBoehm, 2011), but additional experimentation with modeling hasincorporated partial least squares (Brooks et al., 2013), recursivepartitioning (Boehm et al., 2007), and path analysis (Whitman et al.,2001). Thepredicted FIO concentration provides real-timewater qualityestimates that are generally more protective of public health than thoseof the culturing techniques widely used.

Some of the first predictivemodels, historically, to be developed andimplemented for monitoring have been at Great Lakes beaches. AlongLake Michigan, several Indiana beaches were the focus of early


predictive modeling development (Nevers and Whitman, 2005b). Thefive subject beaches have also been actively managed using a predictivemodel, and refinement of the model takes place annually. In Lake Erie,predictive models have been used at two public beaches since 2006(Francy et al., 2006) with refinements incorporated each beach season.Accuracy varies between beaches and years, but correct predictionsranged from 62–81% for the Ohio beaches in 2007 (Francy, 2009).

Development of predictive models can require a significant amountof initial data collection, and continuous updating and refinement areneeded so as to include a wide range of conditions experienced at abeach. As models have become more widespread across the GreatLakes, certain predictors have emerged as surrogates for the primaryforcing factors influencing FIO concentration. Among these are typicallywater turbidity, wind direction, andwave height, all of which tend to bepositively correlated with FIO concentration, as well as sunlight, whichtends to be negatively correlated with FIO.

As more beaches have experimented with predictive modeling, cer-tain overall beach characteristics have emerged that help determinewhat beaches are good candidates for predictive models. Beaches im-pacted by a point source of contamination are the best candidates formodeling because the influence of the point source can be determinedthrough surrogate measurements (Francy, 2009; Nevers et al., 2007).Also, beaches that aremoderately contaminated (i.e., that experience el-evated FIO concentrations 10–30% of the time) tend to be more readilymodeled (Francy, 2009).

More advanced modeling activities have attempted to account forthe physical factors influencing changes in FIO concentrations in thelake. Mechanistic models examine the fate and transport of FIO inwater using an understanding of the underlying physical and biologicalprocesses (Nevers and Boehm, 2011). These types of models have beendeveloped successfully at several river outfalls to describemovement ofFIO contained in the river plume toward the coastal beach. A mechanis-tic model was developed for the outfall of the Little Calumet River alongsouthern Lake Michigan (Thupaki et al., 2013) which was used to sup-port existing statistical models (Nevers and Whitman, 2005a). Thistype of model can be for both predicting where contamination willspread and determining contamination source.

Beach management and public notification

Along with research investigating sources, fate, and transport of FIOassociated with recreational beaches, beach management has alsoevolved in recent years. Advances in methods of communication, ex-panded/intensive monitoring and actions to decrease levels of FIO con-tamination as well as efforts to identify contamination sources havecontributed to beach management improvements (Kinzelman andMcLellan, 2009). The interaction between research scientists and man-agement is a critical component of meeting coordinated beach needs.

Emerging methods for beach monitoring that provide more timelyresults have gradually been incorporated into existing monitoring pro-grams throughout the Great Lakes. Beaches on Lake Erie in Ohio havesome of the longest-running predictive modeling programs used formanaging beach access (Francy, 2009). As part of a funded effort, pre-dictive models have been incorporated into monitoring programsthroughout the U.S. portion of the Great Lakes (Francy et al., 2013a).Chicago beaches along Lake Michigan have an advanced modeling andnotification system that has been incorporated into their monitoringprogram that uses a series of multiple buoys and weather stations de-ployed along the city's lakefront, withmodeling results readily availablethrough their website and through text messaging.

As a result of research identifying birds as a primary or secondarysource of FIO contamination (Edge and Hill, 2007; Haack et al., 2003;Hansen et al., 2009; Hartmann et al., 2013; Lu et al., 2011), beach man-agers have experimented with methods to decrease or limit gullpopulations at beaches, including the use of dogs as gull deterrent andoiling eggs to prevent/reduce hatching (Converse et al., 2009). A

comprehensive study at Racine,Wisconsin beacheswas able to quantifythe effect of gull deterrence by dogs on decreasing the concentration ofFIO in the swimming water (Converse et al., 2012). Other advancingconcepts for limiting avian impact include the use of monofilamentlines to prevent birds from landing in certain areas, increased availabil-ity of waste receptacles, broadcasting of gull distress calls, and nativegrass planting (Cook et al., 2008). Time-lapse cameras to assess recrea-tional patterns to estimate exposure risks in non-swimmers have beenattempted as well (Sunger et al., 2012).

The abundance of FIO in beach sand and the potential for loading tothe nearshore beach water has also been a focus of remediation efforts.Specific types of beach grooming can decrease FIO concentrations byaerating the sand, with the potential to decrease beach swimming advi-sories (Kinzelman et al., 2003, 2004). An abundance ofmanagement ap-proaches has been attempted at beaches in Racine,Wisconsin, includingbeach grooming variations, re-grading of the beach face to promote im-proved drainage, and the re-direction of storm water drains; these ef-forts have led to an observable decrease in swimming advisories(Kinzelman and McLellan, 2009). Management activities in Chicago in-cluded the use of a filtering in-water barrier (Przybyla-Kelly et al.,2013), gull harassment, grass plantings, and public notification (CathyBreitenbach, Chicago Park District, 2013, personal communication).

Initiatives and organizations

The Great Lakes community has taken an international leadershiprole in organizing local and basin-wide efforts to improve recreationalwater quality. At the regional scale, highly active groups develop plansfor beach remediation, improvement of monitoring, and reduction ofsource contamination of area beaches. Examples include the NorthwestIndiana E. coli Task Force, a group of academic, state, federal and envi-ronmental professionals who met monthly for nearly ten years beforetransforming into a nationwide effort. Similar groupswere contempora-neously underway in Milwaukee, Wisconsin, Cuyahoga County, Ohio,Macomb County, Michigan and in Canada, in the cities of Hamiltonand Toronto as well as along the shores of Lakes Huron and Ontario.These groups sensitized their local and political officials, developed pro-grams, sought outside funding, and formed teams that provided earlyinsight into the nature of and potential solutions to beach pollution is-sues. With the development of the national beach program fundedand structured by the BEACH Act, these regional groups transitionedinto more formal and hierarchical effort, with each state headed by abeach coordinator who worked closely with the US EPA through a re-gional beach coordinator.

In 2001, leaders from the former local organizations and other inter-ested parties met under leadership of Richard Whitman (USGS), DougAlley (IJC) and Judy Beck (EPA) in Muskegon, Michigan to form theGreat Lakes Beach Association (GLBA) (http://www.great-lakes.net/glba/). Approximately 25 people attended the first meeting, and halfof those volunteered for service positions in the new organization.Many of that subset became the original board members with RichardWhitman serving as the first president. With membership numberingover 1000 in 2013, theGLBA plays a vital role in providing advice, devel-oping strategy, and sharing information through their listserve,Beachnet (http://glin.net/glba/beachnet.html), and annual meetings.Because the GLBA has a scope that expands beyond the Great Lakesbasin, it has enjoyed strong membership balanced between Canadaand the United States while extending to numerous countries beyond.The importance and role of GLBA are well established among beachagencies; for example, theUnited States Geological Survey commissionsthe GLBA to provide feedback on its own agenda and direction for theirbeach health program. The International Joint Commission beach healthworking group charged the GLBA to develop priorities for better man-agement, research, and public health of beaches. The GLBA annualmeeting provides a platform for Beach 101, an intensive training bythe US EPA on current topics and emerging practices generally focused

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http://glin.net/glba/beachnet.html)


for beach managers. Special symposia during the annual meeting arealso organized to address special themes or problems facing coastal rec-reational waters.

The need for improved scientific management of Great Lakes watershas become more visible in part due to grass roots efforts describedabove but also with recognition by the federal government that cleanbeaches are not only a local but also a national concern affecting theeconomy, quality of life, public health, and national pride. This hastranslated into support at agency, national, and bi-national levels.Good examples of bi-national efforts include the International JointCommission working groups, particularly the Water Quality Board, theBoard of Great Lakes Health Professionals, Science Advisory Board, andactivities of the Great Lakes Commission. The most significant effort inthe United States is the passing of the BEACHAct of 2000, which fundedstates to develop monitoring programs and invest in source identifica-tion and sanitary surveys of coastal waters. Another major effort togather information on the remediation and restoration of beaches wasprovided to local, academic and federal agencies under the GreatLakes Restoration Initiative. This initiative provided $25 million forbeach projects since 2010 for local, state, and cooperating agencies toidentify problems and solutions to issues affectinghigh priority beaches,an effort that again placed the Great Lakes in a pioneering status inbeach science and restoration efforts. Other important federal effortsthat addressed beach improvement include the NOAA Oceans andHuman Health Initiative, USGS Ocean Research Priorities Plan, and theGreat Lakes Observing System, all of which are part of the Internationaland United States Ocean Action Plan. These initiatives have in turnspawned coordination groups, including a Beach Health InteragencyTeam to coordinate federal efforts at beaches. In Canada, The GreatLakes Action Plan has directed funding to support projects and researchcontributing to reductions in beach closures in Areas of Concern aroundthe Great Lakes.

• PATH• EPI• MDL• NPS• MST• MTHD

Chicago

Milwaukee

Green Bay

Duluth

Toled

Detro

• Sau

Fig. 4. Locations of data collection and studies discussed in this manuscript. Type of study indic(NPS), microbial source tracking (MST), methods (MTHD).

Future directions/needs

A considerable amount of information has been gained over the past20 years on the occurrence and transport of FIO and the associatedhuman health risk at Great Lakes beaches (Fig. 4), but there are manyfurther steps needed to improve water quality. Data gaps still exist be-cause the majority of studies have been conducted in areas of concen-trated populations and along the southern regions of the lakes. Fewerstudies have considered beaches affected by nonpoint sources of con-tamination, particularly on the northern lakes (Kleinheinz et al., 2006;Sampson et al., 2005); but more effort is needed to establish the healthrisk associated with these diffuse sources. Nationally, a few epidemio-logical studies have been conducted at this type of location (Calderonet al., 1991; Colford et al., 2007; Shibata et al., 2010); but broad, fresh-water studies have not been conducted across the Great Lakes. Whilethe majority of swimming exposure is associated with large urban cen-ters due to population size, most beaches in the Great Lakes are not im-pacted by heavy sewage input; and the overall health risk for theselocations is poorly understood. Further, the focus of health risk willneed to shift from the concept of FIO to human health outcome whichis beginning to be examined (Nevers et al., 2013; Wymer et al., 2013).With a number of monitoring options available for beach managers,an understanding of human health risk associated with individualchoices is needed.

With the broad range of studies conducted, synthesis of findings todate will help to establish a conceptual model for broader areas of thelakes, a concept that has been developing in some regions (Nevers andWhitman, 2008; Whitman and Nevers, 2008). Incorporating beachuse, population, land use, wastewater disposal, hydrometeorologicalconditions, and bacterial ecology could provide a global view ofrecreational water quality in the Great Lakes. Several of these piecesare being investigated separately, but incorporation across disciplines

Clevelando

it

Toronto

Windsor

lt Ste. Marie

Niagara

ated by color; pathogens (PATH), epidemiology (EPI), modeling (MDL), non-point sources


will improve our ability to locate and mitigate sources of pathogens.This type of global perspectivewould be valuable acrossmany fields, in-cluding nearshore eutrophication, harmful algal blooms, chemical con-tamination, and wildlife health.

Application of findings will also advance beach science, includingtesting location-specific results in diverse areas and using results to im-prove beach status. While the science is being conducted in areas of re-search concentration, beachmanagers need to apply findings to beachesthroughout their jurisdictions. This urges the testing of monitoring al-ternatives at a variety of locations and also theflexibility tomodifymon-itoring protocols to match the location needs. Emphasis is also neededon advancing restoration efforts to improve water quality directly, par-ticularly at beaches experiencing persistent high levels of FIO. The GreatLakes Restoration Initiative has been the impetus for many of thesetypes of projects, which have included physically altering the beach,eliminating or minimizing point sources of microbiological contamina-tion, or locating and removing chemical contaminants.

The Great Lakes has been one of the centers of development forbeach science, and findings developed in the region have had an impactnationally and internationally. As the stresses on the lakes increasewithpopulation growth, much of the research will have to be expandedacross regions and across disciplines. Cooperation with marine cohortsand international scientists and managers will help to strengthen thescience and maximize our understanding and application of these keypieces of information. With a more complete understanding of the sys-tem and a coordinated effort toward improvement of the beach qualityand ecology, nearshore ecosystems and human health can be betterprotected, providing millions of people healthy recreational opportuni-ties and improved water quality.

Acknowledgments

Over the years, the authors of this manuscript have worked with anumber of organizations, including cities and municipalities, state andfederal agencies, as well as academic institutions throughout the GreatLakes.Weappreciate the support received fromour partners and collab-orators. Thank you to Kasia Przybyla-Kelly and Peter Esselman for theirthoughtful reviews and comments. This work was funded in part by aninteragency grant from U.S. EPA through the Great Lakes RestorationInitiative. This article is Contribution 1812 of the USGS Great Lakes Sci-ence Center.

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